Heart Rate Variability: New Perspectives on Physiological Mechanisms, Assessment of Self-regulatory Capacity, and Health risk

Rollin McCraty; Fred Shaffer

doi:10.7453/gahmj.2014.073

Heart Rate Variability: New Perspectives on Physiological Mechanisms, Assessment of Self-regulatory Capacity, and Health risk

McCraty, Rollin; Shaffer, Fred 2015-01-01 00:00:00 GLOBAL ADVANCES IN HEALTH AND MEDICINE rEVIEW Heart rate Variability: new perspectives on physiological Mechanisms, assessment of self-regulatory Capacity, and Health risk 心率变异性：关于生理机制、自律能力和健康风险评估的新观点 Variabilidad de frecuencia cardiaca: Nuevas perspectivas sobre mecanismos fisiológicos, valoración de la capacidad autorreguladora y riesgo de la salud Rollin McCraty, PhD; United States; Fred Shaffer, PhD, BCB, United States author affiliations aBstraCt 摘要 ofrece nuevas perspectivas sobre Institute of HeartMath, Heart rate variability, the change in 心率变异性 (HRC)（在相邻心跳之 los mecanismos subyacentes al Boulder Creek, the time intervals between adjacent 间的时间间隔的变化）是相互依存 ritmo de muy baja frecuencia de la California, (Dr McCraty); Center for Applied heartbeats, is an emergent property of 的调节系统的一种紧急特性，在不 variabilidad de la frecuencia cardia- Psychophysiology, interdependent regulatory systems 同时段内发生，以适应环境和心理 ca. Se analiza la interpretación de Truman State University, that operates on different time scales 挑战。这篇文章简要回顾了心脏的 los ritmos de la variabilidad de la Kirksville, Missouri, to adapt to environmental and psy- 神经调节，在心率变异性的极低频 frecuencia cardiaca en el contexto (Dr Shaffer). chological challenges. This article 率节奏机制方面，提供了一些新的 del riesgo para la salud y la valor- Correspondence briefly reviews neural regulation of 观点。在健康风险和生理及心理自 ación de la capacidad autorregula- Rollin McCraty, PhD the heart and offers some new per- 我调节能力评估讨论的背景下解读 toria fisiológica y psicológica. Los [email protected] spectives on mechanisms underlying HRV 节律。伴有心血管系统输入功 centros reguladores cardiovascula- Citation the very low frequency rhythm of 能的更高级的大脑中枢集成输入的 res de la médula espinal y del bulbo Global Adv Health Med. heart rate variability. Interpretation of 脊髓和延髓心血管监管中心，通过 raquídeo integran entradas de cen- 2015;4(1):46-61. DOI: heart rate variability rhythms in the 交感和副交感神经传出通路调节心 tros cerebrales superiores con 10.7453/gahmj.2014.073 context of health risk and physiologi- 率和血压。我们还讨论了先天性心 entradas de sistemas cardiovascula- Key Words cal and psychological self-regulatory 脏神经系统和心脏大脑连接通路， res aferentes para ajustar la fre- Heart rate variability, capacity assessment is discussed. The 借以传入信息并可以影响皮质下 cuencia cardiaca y la tensión arte- physiological mecha- cardiovascular regulatory centers in 区，皮质前区和运动皮质区的活 rial por vías eferentes simpáticas y nisms, self-regulatory capacity, health risk the spinal cord and medulla integrate 动。此外，审查了使用实时的 HRV parasimpáticas. También hablamos inputs from higher brain centers with 反馈以提高自我调节能力。我们的 sobre el sistema cardiaco nervioso disclosures afferent cardiovascular system inputs 结论是，心脏节律的特征在于在更 intrínseco y las vías de conexión The authors completed the ICMJE Form for to adjust heart rate and blood pressure 长的时段上既有复杂性又有稳定 corazón-cerebro, a través de las Disclosure of Potential via sympathetic and parasympathetic 性，这反映出这些内部自我调节系 cuales la información aferente Conflicts of Interest. efferent pathways. We also discuss the 统的生理和心理功能状态。 puede influir sobre la actividad en Dr McCraty disclosed intrinsic cardiac nervous system and las áreas subcortical, frontocortical that he is employed by the Institute of the heart-brain connection pathways, y de la corteza motora. Además, se HeartMath, which sells sInOpsIs through which afferent information revisa el uso de retroalimentación one of the several heart can influence activity in the subcor- La variabilidad de la frecuencia car- de variabilidad de la frecuencia car- rate variability feedback diaca, o modificación de los inter- devices that are men- tical, frontocortical, and motor cor- diaca a tiempo real para aumentar tioned in the article. tex areas. In addition, the use of real- valos de tiempo entre los latidos la capacidad autorreguladora. Dr Shaffer had no consecutivos del corazón, es una time HRV feedback to increase self- Concluimos que los ritmos cardia- conflicts to disclose. regulatory capacity is reviewed. We propiedad emergente de los siste- cos se caracterizan tanto por su mas reguladores interdependientes conclude that the heart’s rhythms are complejidad como por su estabili- characterized by both complexity and que opera sobre diferentes escalas dad sobre escalas temporales más temporales para adaptarse a los stability over longer time scales that largas que reflejan los estados fun- reflect both physiological and psycho- retos ambientales y psicológicos. cionales tanto fisiológicos como Este artículo revisa brevemente la logical functional status of these inter- psicológicos de estos sistemas nal self-regulatory systems. regulación nerviosa del corazón y internos autorreguladores. IntrOduCtIOn condition. However, with the introduction of signal Since Walter Cannon introduced the concept of processing technologies that can acquire continuous homeostasis, the study of physiology has been based time series data from physiological processes such as on the principle that all cells, tissues, and organs heart rate (HR), blood pressure (BP), and nerve activi- strive to maintain a static or constant “steady-state” ty, it has become abundantly apparent that biological 46 Volume 4, Number 1 • January 2015 • www.gahmj.com Review hEART RATE VARIABILITY: NEw PERSPEcTIVES processes vary in complex and nonlinear ways, even anxiety, depression, asthma, and sudden infant 23-26 during so called “steady-state” conditions. These death. Reduced HRV may correlate with disease observations have led to the understanding that and mortality because it reflects reduced regulatory healthy, optimal function is a result of continuous, capacity and ability to adaptively respond to physio- dynamic, bi-directional interactions among multiple logical challenges such as exercise. For example, in the neural, hormonal, and mechanical control systems at Chicago Health, Aging, and Social Relations Study, both local and central levels. In concert, these physi- separate metrics for the assessment of autonomic bal- ological and psychological regulatory systems are ance and overall cardiac autonomic regulation were never truly at rest and are certainly never static. For developed and tested in a sample of 229 participants. example, we now know that the normal resting In this study, overall regulatory capacity was a signifi- rhythm of the heart is highly variable rather than cant predictor of overall health status, but autonomic being monotonously regular, which was the wide- balance was not. In addition, cardiac regulatory capac- spread notion for many years. ity was negatively associated with the prior incidence of myocardial infarction. The authors suggest that HEart ratE VarIaBILIty cardiac regulatory capacity reflects a physiological The investigation of the heart’s complex rhythms state that is more relevant to health than the indepen- or what is now called heart rate variability (HRV) dent sympathetic or parasympathetic controls or the began with the emergence of modern signal processing autonomic balance between these controls as indexed in the 1960s and 1970s, and has rapidly expanded in by different measures of HRV. more recent times. The irregular behavior of the heart- When speaking of autonomic balance, it should beat is readily apparent when HR is examined on a be kept in mind that a healthy system is constantly and beat-to-beat basis, but is overlooked when a mean value dynamically changing. Therefore, an important indica- over time is calculated. These fluctuations in HR result tor of the health status of the regulatory systems is the from complex, nonlinear interactions among a number capacity to respond to and adjust the relative auto- of different physiological systems. HRV is thus consid- nomic balance (eg, HR) to the appropriate state for the ered a measure of neurocardiac function that reflects context the person is engaged in at any given moment. heart–brain interactions and autonomic nervous sys- In other words, does the HR dynamically respond? Is it 3,4 tem (ANS) dynamics. higher during the daytime or when someone is dealing An optimal level of HRV within an organism with challenging tasks and lower when at rest or dur- reflects healthy function and an inherent self-regulatory ing sleep? The inability of the physiological self-regula- 4-10 capacity, adaptability, or resilience. Too much insta- tory systems to adapt to the current context and situa- bility, such as arrhythmias or nervous system chaos, is tion is associated with numerous clinical conditions. detrimental to efficient physiological functioning and Also distinct, altered, circadian patterns in 24-hour energy utilization. However, too little variation indi- heart rates are associated with different and specific 29,30 cates age-related system depletion, chronic stress, psychiatric disorders, particularly during sleep. pathology, or inadequate functioning in various levels HR estimated at any given time represents the net 2,11,12 of self-regulatory control systems. effect of the neural output of the parasympathetic The importance of HRV as an index of the func- (vagus) nerves, which slow HR, and the sympathetic tional status of physiological control systems was nerves, which accelerate it. In a denervated human noted as far back as 1965 when it was found that fetal heart where there are no connections from the ANS to distress is preceded by reductions in HRV before any the heart following its transplantation, the intrinsic changes occur in HR itself. In the 1970s, reduced rate generated by the pacemaker (SA node) is about 100 HRV was shown to predict autonomic neuropathy in beats per minute (bpm). Parasympathetic activity 14-16 diabetic patients before the onset of symptoms. predominates when HR is below this intrinsic rate dur- Reduced HRV was also found to be a greater risk factor ing normal daily activities and when at rest or sleep. of death post–myocardial infarction than other known When HR is above about 100 bpm, the relative balance risk factors. It has clearly been shown that HRV shifts and sympathetic activity predominates. declines with age and age-adjusted values should be Therefore, HR best reflects the relative balance between used in the context of risk prediction. Age-adjusted the sympathetic and parasympathetic systems. The HRV that is low has been confirmed as a strong, inde- average 24-hour HR in healthy people is approximately pendent predictor of future health problems in both 73 bpm. Higher HRs are independent markers of mor- healthy people. Age-adjusted HRV correlates with all- tality in a wide spectrum of conditions. 19,20 cause mortality. In prospective studies reduced It is important to note the natural relationship HRV has been the strongest independent predictor of between HR and amount of HRV. As HR increases the progression of coronary atherosclerosis. A num- there is less time between heartbeats for variability to ber of studies have shown that reduced HRV is associ- occur, thus HRV decreases. At lower HRs there is more ated with measures of inflammation in subjects with time between heartbeats and variability naturally no apparent heart disease. Reduced HRV is also increases. This is called cycle length dependence, and observed in patients with autonomic dysfunction, it persists in the healthy elderly to a variable degree, Review www.gahmj.com • January 2015 • Volume 4, Number 1 47 GLOBAL ADVANCES IN HEALTH AND MEDICINE even at a very advanced age. However, elderly patients in direct contrast to vagal stimulation, which is almost with ischemic heart disease or other pathologies instantaneous. Thus, any sudden change in HR, up or develop less variability at increasingly lower HRs and down or between one beat and the next, is primarily 33,34 ultimately lose the relationship between HR and vari- parasympathetically mediated. ability, to the point that variability does not increase Patient age may mediate the relationship between with reductions in HR. Even in healthy subjects, the reduced HRV and regulatory capacity of physiological effects of cycle length dependence should be taken control systems. Age-related reductions in HRV may into account when assessing HRV. HR values should reflect the loss of neurons in the brain and spinal cord, also always be reported, especially when HRs are resulting in degraded signal transmission and reduced increased due to factors like stress reactions, medica- regulatory capacity. Reduced physiological regulato- tions, and physical activity. ry capacity may contribute to functional gastrointes- 35,36 Efferent (descending) sympathetic nerves target tinal disorders, inflammation, and hypertension. the SA node via the intrinsic cardiac nervous system and the bulk of the myocardium. Action potentials HEart ratE VarIaBILIty anaLysIs MEtHOds conducted by these motor neurons trigger norepineph- HRV can be assessed with various analytical rine and epinephrine release, which increases HR and approaches, although the most commonly used are strengthens the contractility of the atria and ventricles. frequency domain (power spectral density) analysis Following the onset of sympathetic stimulation, there and time domain analysis. The interactions between is a delay of up to 5 seconds before the stimulation autonomic neural activity, BP, respiration, and higher induces a progressive increase in HR, which reaches a level control systems produce both short and longer 4,12,37 steady level in 20 to 30 seconds if the stimulus is con- term rhythms in HRV measurements. The most tinuous. Even a brief sympathetic stimulus can affect common form for observing these changes is the HR the HR and the HRV rhythm for 5 to 10 seconds. The tachogram, a plot of the sequence of time intervals relatively slow response to sympathetic stimulation is between heartbeats (Figure 1). High stress: public speaking High energy expenditure: exercise Figure 1 An example of the heart rate (HR) tachogram, a plot of the sequence of time intervals between heartbeats over an 8-hour period in ambulatory recording taken from a 36-year-old male. Each of the traces is 1 hour long, with the starting time of the hour on the left hand side of the figure. The time between each vertical line is 5 minutes. The vertical axis within each of the hourly tracings is the time between heartbeats (inter-beat-intervals) ranging between 400 and 1200 milliseconds (label shown on second row). The hours beginning at 10:45 through 12:45 were during a time when he was in a low-stress classroom setting. His overall HR increased, and the range of the HRV is considerably less during the hour starting at 13:45 (public speaking), when he was presenting to the class. In this case, the relative autonomic nervous system balance is shifted to sympathetic predominance due to the emotional stress around presenting to a group of his peers. Once the presentation completed near the end of the hour, his HR dropped and normal HRV was restored. In the following hours, he was listening to others present and providing feedback. In the hour starting at 17:45, he was engaged in physical exercise (walking up a long steep hill) starting about 20 minutes into the hour where his HR is increased and the HRV is reduced due to cycle-length dependence effects. 48 Volume 4, Number 1 • January 2015 • www.gahmj.com Review hEART RATE VARIABILITY: NEw PERSPEcTIVES HEart ratE VarIaBILIty FrEQuEnCy Bands and Low-frequency Band pHysIOLOGICaL MECHanIsMs The LF range is between 0.04 Hz and 0.15 Hz, The European Society of Cardiology and the North which equates to rhythms or modulations with periods American Society of Pacing and Electrophysiology Task that occur between 7 and 25 seconds. This region was Force Report on HRV divided heart rhythm oscillations previously called the “baroreceptor range” or “mid-fre- into 4 primary frequency bands: high-frequency (HF), quency band” by many researchers, since it primarily low-frequency (LF), very-low-frequency (VLF), and reflects baroreceptor activity while at rest. ultra-low-frequency (ULF). Most HRV analysis is done Baroreceptors are stretch-sensitive mechanoreceptors in 5-minute segments (of a 24-hour recording), although located in the chambers of the heart and vena cavae, other recording periods are often used. When other carotid sinuses (which contain the most sensitive recording lengths are analyzed, the length of the record- mechanoreceptors), and the aortic arch. As discussed ing should be reported since this has large effects on previously, the vagus nerves are a major conduit both HRV frequency and time domain values. though which afferent (ascending) neurological sig- nals from the heart are relayed to the brain, including High-frequency Band baroreflex signals. Baroreflex gain is commonly calcu- The HF range is from 0.15 Hz to 0.4 Hz, which lated as the beat-to-beat change in HR per unit of equates to rhythms with periods that occur between change in systolic BP. Decreased baroreflex gain is 2.5 and 7 seconds. This band reflects parasympathetic related to aging and impaired regulatory capacity. or vagal activity and is frequently called the respiratory The cardiovascular system resonance frequency band because it corresponds to the HR variations relat- is a distinctive high-amplitude peak in the HRV ed to the respiratory cycle known as respiratory sinus power spectrum around 0.1 Hz. It has long been estab- arrhythmia. The mechanisms linking the variability of lished that it is caused by a delay in the feedback loops HR to respiration are complex and involve both central within the baroreflex system between the heart and 38 48,49 and reflex interactions. During inhalation, the cardio- brain. In humans and many other mammals, the respiratory center inhibits vagal outflow resulting in resonance frequency of the system is approximately accelerating the HR. Conversely, during exhalation, 0.1 Hz, which is also characteristic of the coherent vagal outflow is restored resulting in slowing the HR. state described later. Although the magnitude of the oscillation is variable, The sympathetic nervous system does not appear in healthy people it can be increased by slow, deep to have much influence in rhythms above 0.1 Hz, while breathing. In younger healthy individuals, it is not the parasympathetic system can be observed to affect uncommon to see an obvious increase in the HF band heart rhythms down to 0.05 Hz (20-sec rhythm). 40,41 at night with a decrease during the day. Therefore, during periods of slow respiration rates, In terms of psychological regulation, reduced vagal activity can easily generate oscillations in the 50-52 vagally mediated HRV has been linked to reduced self- heart rhythms that cross over into the LF band. regulatory capacity and cognitive functions that Therefore, respiratory-related efferent vagally mediat- involve the executive centers of the prefrontal cortex. ed influences are particularly present in the LF band This is consistent with the finding that lower HF power when respiration rates are below 8.5 breaths per min- is associated with stress, panic, anxiety, or worry. ute (approximately 1 breath every 7 seconds) or when 52,53 Lowered parasympathetic activity, rather than reduced an individual sighs or takes a deep breath. sympathetic functioning, appears to account for the In ambulatory 24-hour HRV recordings, it has reduced HRV in aging. been suggested that the LF band reflects sympathetic A number of studies have shown that total vagal activity and the LF/HF ratio has been controversially blockade essentially eliminates HF oscillations and used to assess the balance between sympathetic and 42,43 54-56 reduces power in the LF range. Some investigators parasympathetic activity. A number of research- have used pharmacological blockade (eg, atropine) ers have challenged this perspective and have persua- and found greatly reduced HRV, including the LF and sively argued that in resting conditions, the LF band VLF bands. As a result, they have concluded that all reflects baroreflex activity and not cardiac sympa- 39,57-61 HRV is produced by parasympathetic mechanisms (eg, thetic innervation. 44,45 breathing) However, these investigations did not take into account that atropine and related agents Very-low-frequency Band have much broader effects than only blocking para- The VLF is the power in the range between 0.0033 sympathetic activity. These substances also target the and 0.04 Hz, which equates to rhythms or modulations intrinsic cardiac nervous system, especially the local with periods that occur between 25 and 300 seconds. circuit neurons, which are critical in cardiac control, Although all 24-hour clinical measures of HRV reflect- afferent communication, and the generation of HRV. ing low HRV are linked with increased risk of adverse It has been shown that atropine and similar substanc- outcomes, the VLF band has stronger associations with 46 20,62-64 es also affect sympathetic neurons, so it would be all-cause mortality than the LF and HF bands. expected that these blockades would affect HRV across Low VLF power has been shown to be associated with all frequency bands. arrhythmic death and posttraumatic stress disorder Review www.gahmj.com • January 2015 • Volume 4, Number 1 49 GLOBAL ADVANCES IN HEALTH AND MEDICINE (PTSD). Additionally, low power in this band has been Following up on these results, Armour and col- 67,68 associated with high inflammation and has been leagues developed methods to obtain long-term single- correlated with low levels of testosterone. In contrast, neuron recordings from a beating heart, and simultane- other biochemical markers, such as those mediated by ously, from extrinsic cardiac neurons. Figure 2 shows the hypothalamic-pituitary-adrenal (HPA) axis axis (eg, the VLF rhythm obtained from an afferent neuron cortisol), did not. Longer time periods using 24-hour located in the intrinsic cardiac nervous system in a dog HRV recordings should be obtained to provide compre- heart. In this case, the VLF rhythm is generated from hensive assessment of VLF and ULF fluctuations. intrinsic sources and cannot be explained by sources Historically, the physiological explanation and such as movement. The black bar at the bottom of the mechanisms involved in the generation of the VLF figure labeled “rapid ventricular pacing” shows the component have not been as well defined as the LF and time period where efferent spinal neurons were stimu- HF components. This region has been largely ignored lated. The resulting increase in efferent sympathetic even though it is the most predictive of adverse out- activity clearly elevates the amplitude of the afferent comes. Long-term regulatory mechanisms and ANS neuron’s intrinsic VLF rhythm (top row). activity related to thermoregulation, the renin-angio- Work by Armour and other investigators imply tensin system, and other hormonal factors appear to that the VLF rhythm is generated by the stimulation of 71,72 contribute to this band. afferent sensory neurons in the heart, which in turn Recent work by Armour has shed new light on the activate various levels of the feedback and feed-forward primary mechanisms underlying the VLF rhythm. This loops in the heart’s intrinsic cardiac nervous system, line of research began after some surprising results neurons in the extrinsic cardiac ganglia, and spinal 57,76 from a study looking at HRV in auto-transplanted column. Thus, the VLF rhythm appears to be pro- hearts in dogs. In auto-transplants, the heart is removed duced by the heart itself and may be an intrinsic and placed back in the same animal so there is no need rhythm that is fundamental to health and wellbeing. for anti-rejection medications. The primary purpose of This cardiac origin of the VLF rhythm is also supported the study was to determine if the autonomic nerves re- by studies showing that sympathetic blockade does not innervated the heart posttransplant. Monthly 24-hour affect VLF power. Furthermore, VLF activity remains in HRV recordings were done over a 1-year period on all quadriplegics, whose sympathetic innervation of the the dogs with auto-transplanted hearts as well as the heart and lungs is disrupted. control dogs. The nerves did re-innervate but in a way Thus, experimental evidence suggests that the that was not accurately reflected in HRV. It showed that VLF rhythm is intrinsically generated by the heart the intrinsic cardiac nervous system has neuroplasticity and that the amplitude and frequency of these oscilla- and re-structured its neural connections. The truly sur- tions are modulated by efferent sympathetic activity. prising result was that these de-innervated hearts had Normal VLF power appears to indicate healthy func- higher levels of HRV, including HRV that is typically tion, and increases in resting VLF power and or shift- associated with respiration, than control dogs immedi- ing of their frequency can reflect efferent sympathetic ately posttransplant. These levels were sustained over a activity. The modulation of the frequency of this 73 78 1-year period. This was unexpected as there is very rhythm due to physical activity, stress responses, little HRV in human transplant recipients. and other factors that increase efferent sympathetic Average: 90-sec rhythm Range: 75-100 sec (0.013 - 0.1 Hz) Neuronal Activity 20 /5 sec Activated neurons LV IMP (mmHg) Rapid ventricular pacing 0 50 100 150 200 250 300 350 400 450 500 550 600 650 700 750 800 850 900 950 Figure 2 Long-term single-neuron recordings from an afferent neuron in the intrinsic cardiac nervous system in a beating dog heart. The top row shows neural activity. The second row is the actual neural recording. The third row is the left ventricular pressure. This intrinsic rhythm has an average period of 90 seconds with a range between 75 to 100 seconds (0.013 Hz - 0.01 Hz), which falls within the VLF band. Used with permission from Dr J. Andrew Armour. 50 Volume 4, Number 1 • January 2015 • www.gahmj.com Review hEART RATE VARIABILITY: NEw PERSPEcTIVES activation can cause it to cross over into the lower easily detected in healthy individuals. region of the LF band during ambulatory monitoring Circadian rhythms, core body temperature, or during short-term recordings when there is a sig- metabolism, hormones, and intrinsic rhythms gener- nificant emotional stressor. ated by the heart all contribute to lower frequency rhythms (eg, VLF and ULF) that extend below 0.04 Hz. ultra-low-frequency Band In healthy individuals, there is an increase in VLF The ultra-low-frequency band (ULF) falls below power that occurs during the night and peaks before 79,80 0.0033 Hz (333 seconds or 5.6 minutes). Oscillations or waking. This increase in autonomic activity events in the heart rhythm with a period of 5 minutes or appears to correlate with the morning cortisol peak. greater are reflected in this band and it can only be assessed with 24-hour and longer recordings. The cir- power spectral analysis cadian oscillation in HR is the primary source of the Power spectral analysis is used to separate the ULF power, although other very slow-acting regulatory complex HRV waveform into its component rhythms processes, such as core body temperature regulation, that operates within different frequency ranges (Figure metabolism, and the renin-angiotensin system likely 3). Spectral analysis provides information regarding add to the power in this band. The Task Force Report how power is distributed (the variance and amplitude on HRV suggests that 24-hour recordings should be of a given rhythm) as a function of frequency (the time divided into 5-minute segments and that HRV analysis period of a given rhythm). The main advantages of should be performed on the individual segments prior spectral analysis are that it supplies both frequency to the calculation of mean values. This effectively filters and amplitude information on the specific rhythms out any oscillations with periods longer than 5 minutes. that exist in the HRV waveform, providing a means to However, when spectral analysis is applied to entire quantify these oscillations over any given period. The 24-hour records, several lower frequency rhythms are values are expressed as the power spectral density, Original VLF LF HF 4:29 AM 4:34 AM 4:39 AM 4:44 AM 50% 25 40% 30% 20% 10% 0% 0.00 0.05 0.10 0.15 0.20 0.25 0.30 0.35 0.40 VLF LF HF Frequency (Hz) Figure 3 A typical heart rate variability (HRV) recording over a 15-minute period during resting conditions in a healthy individual. The top tracing shows the original HRV waveform. Filtering techniques were used to separate the original waveform into VLF, LF, and HF bands as shown in the lower traces. The bottom of the figure shows the power spectra (left) and the percentage of power (right) in each band. abbreviations: HF, high frequency; LF, low frequency; PSD: power spectral density; VLF, very low frequency. Review www.gahmj.com • January 2015 • Volume 4, Number 1 51 Heart Rate Power Spectral Density (ms /Hz) Normalized Power GLOBAL ADVANCES IN HEALTH AND MEDICINE which is the area under the curve (peak) in a given seconds. This measure reflects the ebb and flow of all the bandwidth of the spectrum. The power or height of the factors that contribute to HRV. In 24-hour recordings, peak at any given frequency indicates the amplitude the SDNN is highly correlated with ULF and total and stability of the rhythm. The frequency reflects the power. In short-term resting recordings, the primary period of time over which the rhythm occurs. For source of the variation is parasympathetically mediated, example, a 0.1 Hz frequency has a period of 10 seconds. especially with slow, deep breathing protocols. However, in ambulatory and longer term recordings the SDNN autonomic Balance and the Low-frequency:High- values are highly correlated with lower frequency frequency ratio rhythms. Thus, low age-adjusted values predict morbid- The autonomic balance hypothesis assumes that ity and mortality. For example, patients with moderate the sympathetic and parasympathetic competitively SDNN values (50-100 milliseconds) have a 400% lower regulate HR (accentuated antagonism), where risk of mortality than those with low values (0-50 milli- 81,82 increased sympathetic activity is paired with seconds) in 24-hour recordings. decreased parasympathetic activity. While some orthostatic challenges can produce reciprocal chang- standard deviation of the normal-to-normal Index es in sympathetic activation and vagal withdrawal, The SDNN index is the mean of the standard devia- psychological stressors can also result in independent tions of all the NN intervals for each 5-minute segment. changes in sympathetic or parasympathetic activity. Therefore, this measurement only estimates variability It is now generally accepted that both branches of the due to the factors affecting HRV within a 5-minute ANS are simultaneously active. period. In 24-hour HRV recordings, it is calculated by The ratio of LF to HF power is controversial due to first dividing the 24-hour record into 288 five-minute the issues regarding the LF band described above. It is segments and then calculating the standard deviation often assumed that a low LF:HF ratio reflects greater of all NN intervals contained within each segment. The parasympathetic activity relative to sympathetic activ- SDNN index is the average of these 288 values. The ity. However, this ratio is often shifted due to reduc- SDNN index is believed to primarily measure auto- tions in LF power. Therefore, the LF:HR ratio should be nomic influence on HRV. This measure tends to corre- interpreted with caution and the mean values of HF late with VLF power over a 24-hour period. and LF power taken into consideration. In contrast, a high LF:HF ratio may indicate higher sympathetic the root Mean square of successive differences activity relative to parasympathetic activity as can be The RMSSD is the root mean square of successive observed when people engage in meeting a challenge differences between normal heartbeats. This value is that requires effort and increased sympathetic activa- obtained by first calculating each successive time dif- tion. Alternatively, it can indicate increased parasym- ference between heartbeats in milliseconds. Each of the pathetic activity as occurs during slow breathing. values is then squared and the result is averaged before Again, the same cautions must be taken into consider- the square root of the total is obtained. The RMSSD ation, especially in short-term recordings. reflects the beat-to-beat variance in HR and is the pri- mary time domain measure used to estimate the vagal- tIME dOMaIn MEasurEMEnts OF HEart ratE ly mediated changes reflected in HRV. The RMSSD is VarIaBILIty correlated with HF power and therefore also reflects Time domain measures are the simplest to calcu- self-regulatory capacity as discussed earlier. late. Time domain measures do not provide a means to adequately quantify autonomic dynamics or determine nEurOBIOLOGy OF sELF-rEGuLatIOn the rhythmic or oscillatory activity generated by the dif- Considerable evidence from clinical, physiologi- ferent physiological control systems. However, since cal, and anatomical research has identified cortical, they are always calculated the same way, data collected subcortical and medulla oblongata structures by different researchers are comparable but only if the involved in self-regulation. Oppenheimer and recordings are exactly the same length of time and the Hopkins mapped a detailed hierarchy of cardiac con- data are collected under the same conditions. Time trol structures among the cortex, amygdala and other domain indices quantify the amount of variance in the subcortical structures, all of which can modify cardio- inter-beat-intervals (IBI) using statistical measures. The vascular-related neurons in the lower levels of the three most important and commonly reported time neuraxis (Figure 4). They suggest that the amygdala domain measures are the standard deviation of normal- is involved with refined integration of emotional con- to-normal (SDNN), the SDNN index, and the root mean tent in higher centers to produce cardiovascular square of successive differences (RMSSD) are the most responses that are appropriate for the emotional commonly reported metrics. aspects of the current circumstances. The insular cortex and other centers such as the the standard deviation of the normal-to-normal orbitofrontal cortex and cingulate gyrus can overcome The SDNN is the standard deviation of the normal- (self-regulate) emotionally entrained responses by to-normal (NN) sinus-initiated IBIs measured in milli- inhibiting or enhancing them. They also point out that 52 Volume 4, Number 1 • January 2015 • www.gahmj.com Review hEART RATE VARIABILITY: NEw PERSPEcTIVES Insular and Prefrontal Cortex Bed Nucleus Central Nucleus Lateral Paraventricular Stria Terminals Hypothalamus Amygdala Hypothalamus Periaqueductal Gray Dorsal Vagal Rostral Ventrolateral Complex Medulla Figure 4 Schematic diagram showing the relationship of the principal descending neural pathways from the insular and prefrontal cortex to subcortical structures and the medulla oblongata as outlined by Oppenheimer and Hopkins. The insular and prefrontal cortexes are key sites involved in modulating the heart’s rhythm, particularly during emotionally charged circumstances. These structures alone with other centers such as the orbitofrontal cortex and cingulate gyrus can inhibit or enhance emotional responses. The amygdala is involved with refined integration of emotional content in higher centers to produce cardiovascular responses that are appropriate for the emotional aspects of the current circumstances. Imbalances between the neurons in the insula, amygdala and hypothalamus may initiate cardiac rhythm disturbances and arrhythmias. The structures in the medulla represent an interface between incoming afferent informa- tion from the heart, lungs and other body systems and outgoing efferent neuronal activity. imbalances between the neurons in the insula, amyg- uals are stressed or threatened and prolonged prefron- dala and hypothalamus may initiate cardiac rhythm tal inactivity can lead to hypervigilance, defensive- disturbances and arrhythmias. The data suggest that ness, and social isolation. the insular and medial prefrontal cortexes are key sites involved in modulating the heart’s rhythm, particular- Vagal Control system ly during emotionally charged circumstances. The cardiovascular control system is highly dis- Thayer and Lane have also have described the tributed throughout the central nervous system and same set of neural structures which they call the cen- interacts both widely and reciprocally with many tral autonomic network (CAN). The CAN is involved other neural control systems, especially with the respi- in cognitive, affective, and autonomic regulation. The ratory system. The final common output pathways for CAN is related to HRV and linked to cognitive perfor- the cardiorespiratory control system are located in the mance. In their model, the CAN links the nucleus of medulla oblongata. The medulla contains many neu- tractus solitarius (NTS) in the medulla with the ante- rons that act as interneurons and premotor neurons as rior cingulate, insula, prefrontal cortex, amygdala, and well as separate neuronal populations for respiratory hypothalamus through a series of feedback and feed- and cardiovascular regulation. The cell groups forming forward loops. They also propose that this network is the cardiorespiratory control system have an intimate an integrated system for internal self-regulation by relationship, which allows for a highly integrated regu- which the brain controls the heart, other visceromotor lation of motor output. The medulla represents an organs, and neuroendocrine and behavioral responses interface between incoming afferent information and that are critical for goal-directed behavior, adaptabili- outgoing efferent neuronal activity. An important ty, and sustained health. They suggest that these function of the cardiorespiratory control system is the dynamic connections explain why vagally mediated respiratory modulation of both sympathetic and para- HRV is linked to higher-level executive functions and sympathetic outflow that is present in the activity pat- reflects the functional capacity of the brain structures terns of spinal preganglionic neurons. that support working memory and emotional and The NTS of the medulla oblongata integrates affer- physiological self-regulation. They have shown that ent sensory information from proprioceptors (body vagally mediated HRV is correlated with prefrontal position), chemoreceptors (blood chemistry), and cortical performance and the ability to inhibit unwant- mechanoreceptors (also called baroreceptors) from the ed memories and intrusive thoughts. Furthermore, the heart, lungs, and face. The NTS connects to the dorsal prefrontal cortex can be taken “offline” when individ- motor nucleus of the vagus nerve and the nucleus Review www.gahmj.com • January 2015 • Volume 4, Number 1 53 GLOBAL ADVANCES IN HEALTH AND MEDICINE ambiguous (NA). Neurocardiology research indicates variability in HR and BP. The medulla oblongata is the that the efferent vagal fibers that innervate the heart major structure integrating incoming afferent informa- are primarily A-fibers, the largest and fastest conduct- tion from the heart, lungs and face with inputs from ing axons that originate from somata located primarily cortical and subcortical structures and is the source of in the NA. The NA also receives and integrates informa- the respiratory modulation of the activity patterns in tion from the cortical and subcortical systems. Thus, sympathetic and parasympathetic outflow. The intrin- the vagal regulatory centers respond to peripheral sen- sic cardiac nervous system integrates mechanosensi- sory (afferent) inputs and higher brain center inputs to tive and chemosensitive neuron inputs with efferent adjust efferent neuronal outflows, which results in the information from both the sympathetic and parasym- vagally mediated beat-to-beat changes in HR. pathetic inputs from the brain. As a complete system, it Since BP regulation is a central role of the cardio- affects HRV, vasoconstriction, venoconstriction, and vascular system, the factors that alter BP also affect cardiac contractility in order to regulate HR and BP. beat-to-beat fluctuations and therefore, the heart rhythms. Intrinsic cardiac afferent sensory neurons afferent Modulation of Cardiac and Brain activity transduce and distribute mechanical and chemical The field of neurocardiology has extensively information regarding the heart to the intrinsic car- explored the anatomy and functions of the intrinsic diac nervous system. The afferent impulses from the cardiac nervous system along with its connections 75,86 intrinsic cardiac neurons travel via the vagal nerves to with the brain. While efferent regulation of the the nodose ganglia and then to the NTS. The NTS has heart by the vagus nerves is generally well known, the connections with the NA and spinal cord resulting in majority of fibers in the vagus nerves are afferent in modulation of activity patterns in both parasympa- nature. Furthermore, more vagal fibers are related to thetic and sympathetic outflow to the heart and the cardiovascular pathways than other organs. Complex blood vessels. There is controversy regarding any patterns of cardiovascular afferent nerve activity occur inhibitory role of parasympathetic efferent pregangli- across time scales from milliseconds to minutes. The onic neurons in the dorsal motor vagal (DMV) com- intrinsic cardiac nervous system has both short-term plex of the medulla as a number of anatomical studies and long-term memory functions, which can influence suggest that virtually all efferent projections from the HRV and afferent activity related to BP, rhythm, rate, 83 70,88,89 DMV are to subdiaphragmatic structures. and hormonal factors. The intrinsic cardiac neu- The vagus nerves innervate the intrinsic cardiac rons (sensory, interconnecting, afferent, and motor) nervous system. A few of these connections synapse on can operate independently of central neuronal com- motor neurons in the intrinsic cardiac nervous system mand, and their network is sufficiently extensive to be that project directly to the SA node (and other tissues in characterized as its own “little brain” in the heart 84,90 the heart) where they trigger acetylcholine release to (Figure 5). The afferent nerves play a critical role in slow HR. However, the majority of the efferent pre- physiological regulation and affect the heart’s rhythm ganglionic vagal neurons (~80%) connect to local cir- and HRV. Efferent sympathetic and parasympathetic cuitry neurons in the intrinsic cardiac nervous system activity is integrated in the heart’s intrinsic nervous where motor information is integrated with inputs system, with the signals arising from the mechanosen- from mechanosensitive and chemosensory neurons in sory and chemosensory neurons in the heart (Figure 6). the heart. Thus, efferent sympathetic and parasympa- The neural output of the intrinsic cardiac nervous sys- thetic activity is integrated in and with the activity tem then travel to the brain via afferent pathways in occurring in the heart’s intrinsic nervous system. This the spinal column and vagus nerve. Intrinsic cardiac includes the input signals from the mechanosensitive afferent neurons project to nodose and dorsal root gan- and chemosensory neurons within the heart, all of glia, the spinal cord, brainstem, hypothalamus, thala- 4,46,91 which ultimately contribute to beat-to-beat cardiac mus, or amygdala and then to the cerebral cortex. functional changes. John and Beatrice Lacey were the first to suggest a The response time of a single efferent vagal causal role of the heart in modulating cognitive func- impulse on the sinus node is very short and results in tions such as sensory-motor and perceptual perfor- 92-94 an immediate response that typically occurs within the mance. They suggested that cortical functions are cardiac cycle in which it occurs and affects only 1 or 2 modulated via afferent input from pressure sensitive 33 93 heartbeats after its onset. After cessation of vagal neurons in the heart, carotid arteries, and aortic arch. stimulation, HR rapidly increases to its previous level. Their research focused on activity occurring within a An increase in HR can also be achieved by reduced single cardiac cycle, and they confirmed that cardio- vagal activity (vagal withdrawal). Thus, any sudden vascular activity influences perception and cognitive change in HR, up or down, or between 1 beat and the performance. Research by Velden and Wölk later dem- 33,34 next, are primarily parasympathetically mediated. onstrated that cognitive performance fluctuated at a In summary, the cardiorespiratory control system rhythm around 10 Hz and showed that the modula- is complex, and information from many inputs is inte- tion of cortical function via the heart’s influence was grated at multiple levels of the system, all of which are due to afferent inputs on the neurons in the thalamus, 95,96 important for the generation of normal beat-to-beat which globally synchronizes cortical activity. An 54 Volume 4, Number 1 • January 2015 • www.gahmj.com Review hEART RATE VARIABILITY: NEw PERSPEcTIVES Figure 5 Microscopic image of interconnected intrinsic cardiac ganglia in the human heart. The thin, light blue structures are multiple axons that connect the ganglia. Used with permission from Dr J. Andrew Armour. important aspect of their work was the finding that it tems, it can pull the other systems into increased syn- is the “pattern and stability” (of the rhythm) of the chronization and more efficient function. For example, heart’s afferent inputs, rather than the number of neu- frequency pulling and entrainment can easily be seen ral bursts within the cardiac cycle, that are important between the heart, respiratory, and BP rhythms as well in modulating thalamic activity, which in turn has as between very-low-frequency brain rhythms, cranio- global effects on brain function. sacral rhythms, and electrical potentials measured 52,102 There has since been a growing body of research across the skin. indicating that afferent information processed by the We (McCraty and colleagues) introduced the term intrinsic cardiac nervous system can influence activi- physiological coherence to describe the degree of order, 4,97,98 58 ty in the frontocortical areas and motor cortex, harmony, and stability in the various rhythmic activi- affecting psychological factors such as attention level, ties within living systems over any given time period. 99 100 motivation, perceptual sensitivity, and emotion- This harmonious order signifies a coherent system that al processing. has an efficient or optimal function directly related to the ease and flow in life processes. By contrast, an COHErEnCE erratic, discordant pattern of activity denotes an inco- The various concepts and measurements embraced herent system whose function reflects stress and inef- under the term coherence have become central to fields ficient utilization of energy in life processes. as diverse as quantum physics, cosmology, physiology, Specifically, heart coherence (also referred to as cardiac and brain and consciousness research. Coherence coherence or resonance) can be measured by HRV always implies connectedness, correlations, stability analysis wherein a person’s heart rhythm pattern and efficient energy utilization. For example, we refer to becomes more ordered and sine-wave like at a frequen- people’s speech or thoughts as coherent if the words fit cy of around 0.1 Hz (10 seconds). A coherent heart together well and incoherent if they are uttering mean- rhythm is defined as a relatively harmonic, sine wave– ingless nonsense or ideas that make no sense as a whole. like, signal with a very narrow, high-amplitude peak in In physics and physiology, the term coherence is used to the LF region of the HRV power spectrum with no describe the degree of synchronization between differ- major peaks in the VLF or HF regions. Coherence is ent oscillating systems. This type of coherence is called assessed by identifying the maximum peak in the 0.04 cross-coherence which occurs when two or more of the Hz to 0.26 Hz range of the HRV power spectrum, calcu- body’s oscillatory systems, such as respiration and heart lating the integral in a window 0.030 Hz wide, centered rhythms, become entrained and operate at the same on the highest peak in that region, and then calculating frequency. The term auto-coherence describes coherent the total power of the entire spectrum. The coherence activity within a single oscillatory system. An example ratio is formulated as: (Peak Power/[Total Power – Peak is a system that exhibits sine wave like oscillations; the Power]). Physiological coherence includes specific more stable the frequency, amplitude and shape, the approaches for quantifying the various types of coher- higher the degree of coherence. When coherence is ence measures, such as cross-coherence (frequency increased in a system that is coupled with other sys- entrainment between respiration, BP, and heart Review www.gahmj.com • January 2015 • Volume 4, Number 1 55 GLOBAL ADVANCES IN HEALTH AND MEDICINE Figure 6 The neural communication pathways interacting between the heart and the brain are responsible for the generation of heart rate variability. The intrinsic cardiac nervous system integrates information from the extrinsic nervous system and from the sensory neu- rites within the heart. The extrinsic cardiac ganglia located in the thoracic cavity have connections to the lungs and esophagus and are indirectly connected via the spinal cord to many other organs such as the skin and arteries. The vagus nerve primarily consists of afferent fibers that connect to the medulla after passing through the nodose ganglion. Used with permission from the Institute of HeartMath, Boulder Creek, California. rhythms), synchronization among systems (eg, syn- information is encoded in the dynamic patterns of chronization between various electro-encephalogra- physiological activity. The afferent pathways from the phy [EEG] rhythms and the cardiac cycle), auto-coher- heart and blood vessels are given more relevance in ence (stability of a single waveform such as respiration this model due to the significant degree of afferent or HRV patterns), and system resonance. cardiovascular input to the brain and the consistent Interestingly, we have found that positive emo- generation of dynamic patterns generated by the heart. tions such as appreciation and compassion, as opposed It is our thesis that positive emotions in general, as to negative emotions such as anxiety, anger, and fear, well as self-induced positive emotions, shift the sys- are reflected in a heart rhythm pattern that is more tem as a whole into a more globally coherent and har- 4,5,103 coherent. The coherent state has been correlated monious physiological mode associated with with a general sense of wellbeing, and improvements improved system performance, ability to self-regulate, in cognitive, social, and physical performance. We and overall wellbeing. The psychophysiological coher- have observed this association between emotions and ence model predicts that different emotions are reflect- heart rhythm patterns in studies conducted in both ed in state-specific patterns in the heart’s rhythms laboratory and natural settings and for both spontane- independent of the amount of HRV or HR. Recent 52,102 ous and intentionally generated emotions. independent work has verified this by demonstrating We introduced the Heart Rhythm Coherence a 75% accuracy in detection of discrete emotional Hypothesis, which states that the pattern and stability states from the HRV signal using a neural network of beat-to-beat HR activity encodes information over approach for pattern recognition. Several studies in “macroscopic time scales” (ie, over many seconds to healthy subjects, which helped inform the model, minutes rather than only within a single cardiac cycle) show that during the experience of positive emotions, that can impact cognitive performance and emotional a sine wave–like pattern naturally emerges in the 4,8 experience. The coherence model takes a dynamic heart’s rhythms without any conscious changes in 52,103 systems approach that focuses on increasing individu- breathing. This is likely due to more organized als’ self-regulatory capacity through self-management outputs of the subcortical structures involved in pro- techniques that induce a physiological shift reflected cessing emotional information described by Pribram, 60 83 11 in the heart’s rhythms. We suggest that rhythmic Porges, Oppenheimer and Hopkins, and Thayer, activity in living systems reflects the regulation of in which the subcortical structures influence the oscil- interconnected biological, social, and environmental latory output of the cardiorespiratory control system networks and that important biologically relevant in the medulla oblongata. 56 Volume 4, Number 1 • January 2015 • www.gahmj.com Review hEART RATE VARIABILITY: NEw PERSPEcTIVES Heart rate Variability Coherence Increases Vagal opment of emotional experience and the social engage- afferent traffic ment system. As human beings, we are not limited to One of the properties of sensory neurons is that fight, flight, or freeze responses. We can self-regulate they are most responsive to increases in rate of change and initiate pro-social behaviors when we encounter in the function to which they are tuned to detect (eg, challenges, disagreements, or stressors. Porges sug- HR, BP). During periods of increased cardiac coher- gests that the healthy function of the social engage- ence, there is typically an increased range of variabili- ment system depends upon the proper functioning of ty in both BP and HR, which is detected as increases in the vagus nerves, which act as a “vagal brake,” and that the rate of change by the sensory neurons, resulting in measurements of vagal activity could serve as a mark- increased firing rates that increase vagal afferent traf- er for one’s ability to self-regulate. His theory also sug- fic. There is also a more ordered pattern of activity. A gests that the evolution and healthy function of the recent study using heartbeat-evoked potentials ANS determines the boundaries for the range of one’s showed that using paced breathing at a 10-second emotional expression, quality of communication, and rhythm increased both the range of HRV and the the ability to self-regulate emotions and behaviors. coherence in the rhythms as expected and also increased the N200 amplitude potential in the EEG self-regulation techniques that Increase Cardiac heartbeat–evoked potentials, which indicates Coherence increased afferent input. There is a paradigm shift occurring in the treat- Anatomical and stimulation studies have shown ment of diverse disorders like depression, epilepsy, that the thalamic pain pathways in the spinal cord are and pain by using vagal nerve stimulation, which 128-130 inhibited by increases in vagal afferent nerve traffic stimulates afferent neural pathways. New per- 105-107 over normal intrinsic levels. Several studies have spectives are emerging on behavioral intervention demonstrated that teaching patients self-regulation approaches that teach people self-regulation strategies techniques that increase HRV coherence is associated that include a physiological aspect such as HRV bio- with reduced pain and physical activity limita- feedback and that naturally increase vagal traffic. For 108,109 tions. In a study of patients with severe brain example, there are many studies showing that the injury, it was found that emotion–self-regulation train- practice of breathing at 6 breaths per minute, sup- ing resulted in significantly higher coherence ratios ported by HRV biofeedback, induces the coherence 111,131-136 and higher attention scores. Ratings of participants’ rhythm and has a wide range of benefits. emotional control correlated with improved HRV In addition to clinical applications, HRV coher- coherence measures. Regular practice of HRV bio- ence feedback training is often used to support self- feedback results in lasting improvements in baroreflex regulation skill acquisition in educational, corporate, gain, independent of cardiovascular and respiratory law enforcement, and military settings. Several sys- effects. This indicates neuroplasticity within the baro- tems that assess the degree of coherence in the user’s reflex system, likely within the intrinsic cardiac ner- heart rhythms are available. The majority of these vous system. Thus, repeated sessions of heart coher- systems—such as the emWavePro, or Inner Balance ence practice can reset the baroreflex system resulting for iOS devices (HeartMath, Inc, Boulder Creek, in increased afferent nerve activity noninvasively. California), Relaxing Rhythms (Wild Divine, Boulder City, Nevada), and the Stress Resilience Training resilience and self-regulatory Capacity System (Ease Interactive, San Diego, California)—use HRV also indicates psychological resiliency and a noninvasive earlobe or finger pulse sensor and dis- behavioral flexibility, reflecting an individual’s capac- play the user’s heart rhythm to provide feedback on ity to self-regulate and effectively adapt to changing their level of coherence. 27,112 social or environmental demands. A growing Emotional self-regulation strategies may contrib- number of studies have specifically linked vagally ute to improved health and performance. Alone or in 9,10,113 mediated HRV to self-regulatory capacity, emo- combination with HRV coherence biofeedback train- 114,115 7,116 tional regulation, social interactions, one’s ing, these strategies have been shown to increase resil- sense of coherence, the personality character traits ience and accelerate recovery from stressors or trau- 118 119 5,8,136,137 of self-directedness, and coping styles. ma. Self-induced positive emotions can initi- More recently, several studies have shown an ate a shift to increased cardiac coherence without any association between higher levels of vagally-mediated conscious intention to change the breathing 52,103 resting HRV and performance on cognitive perfor- rhythm. Typically, when people are able to self- mance tasks requiring the use of executive func- activate a positive or calming feeling rather than tions. HRV coherence can be increased in order to remaining focused on their breathing, they enjoy the 4,120-122 improve cognitive function as well as a wide shift in feeling and are able to sustain high levels of range of clinical outcomes that have been shown to coherence for much longer time periods. 5,51,123-127 reduce healthcare costs. Heart-focused self-regulation techniques and Porges suggests that the evolution of the ANS, assistive technologies that provide real-time HRV specifically the vagus nerves, was central to the devel- coherence feedback provide a systematic process for Review www.gahmj.com • January 2015 • Volume 4, Number 1 57 GLOBAL ADVANCES IN HEALTH AND MEDICINE self-regulating thoughts, emotions, and behaviors and tions in systolic and diastolic BP, total cholesterol, increasing physiological coherence. Many of these fasting glucose, overall stress, anger, fatigue and hostil- techniques (eg, Heart-Focused Breathing, Freeze ity. Similar results were obtained in several studies 139 138,142 Frame, Quick Coherence ) are designed to enable with police officers. people to intervene in the moment they start to experi- In addition to the emotional self-regulation tech- ence stress reactions or unproductive thoughts or niques, there are other approaches that also increase emotions. With practice, one is able to use one of the HRV coherence. For example, a study of Zen monks techniques to shift into a more coherent physiological found that monks with greater experience in medita- state before, during, and after challenging or adverse tion tended to have more coherent heart rhythms dur- situations, thus optimizing mental clarity, emotional ing their resting recording, while the ones who had composure, and stability. been monks for less than 2 years did not. A study of The first step in most of the techniques developed autogenic training also showed increased HRV coher- by the Institute of HeartMath is called Heart-Focused ence and found that cardiac coherence was strongly Breathing, which includes putting one’s attention in correlated with EEG alpha activity. The authors sug- the center of the chest (area of the heart) and imagin- gested that cardiac coherence could be a general mark- ing the breath is flowing in and out of the chest area er for the meditative state. However, this does not while breathing a little slower and deeper than usual. suggest that all meditation or prayer styles increase Conscious regulation of one’s respiration at a 10-sec- coherence, unless the coherence state is driven by a ond rhythm (0.1Hz) increases cardiac coherence and focus on breathing at a 10-second rhythm or the acti- 145-148 starts the process of shifting into a more coherent vation of a positive emotion. For example, a 4,124 state. With conscious control over breathing, an study examining HRV while reciting rosary or bead individual can slow the rate and increase the depth of prayers and yoga mantras found that a coherent the breathing rhythm. This takes advantage of physi- rhythm was produced by rhythmically breathing but ological mechanisms to modulate efferent vagal activ- not by random verbalization or breathing. The authors ity and thus the heart rhythm. This increases vagal ascribed the mechanisms for this finding to a breath- afferent nerve traffic and increases the coherence (sta- ing pattern of 6-cycles per minute. In a study of the bility) in the patterns of vagal afferent nerve traffic. In effects of five different types of prayer on HRV, it was turn, this influences the neural systems involved in found that all types of prayer elicited increased cardiac regulating sympathetic outflow, informing emotional coherence. However, prayers of gratefulness and heart- experience, and synchronizing neural structures felt love resulted in definitively higher coherence lev- 4 148 underlying cognitive processes. els. It has also been shown that tensing the large Several studies using various combinations of muscles in the legs in a rhythmical manner at a 10-sec- these self-regulation techniques have found signifi- ond rhythm can induce a coherent heart rhythm. cant correlations between HRV coherence and improvements in cognitive function and self-regulato- COnCLusIOn ry capacity. For example, a study of middle school HRV is an emergent property of interdependent students with attention deficit hyperactivity disorder regulatory systems that operate on different time showed a wide range of significant improvements in scales to adapt to environmental and psychological short and long-term memory, ability to focus, and sig- challenges. The physiological mechanisms that con- nificant improvements in behaviors both at home and tribute to HRV are complex and involve the neuraxis in school. A study of 41 fighter pilots engaging in that spans from the prefrontal and insular cortex to flight simulator tasks found a significant correlation the intrinsic cardiac nervous system, with the medulla between higher levels of performance and heart oblongata and intrinsic cardiac nervous system pro- rhythm coherence as well as lower levels of frustra- viding major neural integration centers. HRV can be tion. A study of recently returning soldiers from used as an index of the functional capacity of various Iraq who were diagnosed with PTSD, found that rela- regulatory systems and assessment of regulatory tively brief periods of HRV coherence training com- capacity may offer an alternative to autonomic bal- bined with practicing the Quick Coherence Technique ance models. Since the HRV LF band primarily reflects resulted in significant improvements in the ability to the vagally mediated transmission between the heart self-regulate along with a wide range of cognitive func- and medulla, resting measurements should not be tions. The degree of improvement correlated with used as markers of sympathetic activity. Based on increased cardiac coherence. Other studies have 24-hour monitoring, ULF and VLF rhythms are more shown increases in parasympathetic activity (vagal strongly associated with overall health status than HF tone), reductions in cortisol and increases in rhythms. New perspectives on mechanisms underly- DHEA, lowered BP and stress measures in hyperten- ing the VLF rhythm suggest that the primary source of 124,126 123 sive populations, reduced healthcare costs, this rhythm is within the heart itself. Recent findings and significant improvements in functional capacity demonstrate the importance of the intrinsic cardiac in patients with congestive heart failure. In addi- nervous system and cardiac afferents in generating the tion, a study of correctional officers showed reduc- heart rhythm and modulating the intervals between 58 Volume 4, Number 1 • January 2015 • www.gahmj.com Review hEART RATE VARIABILITY: NEw PERSPEcTIVES over nine decades. J Am Coll Cardiol. 1998;31(3):593-601. heartbeats. Vagally-mediated HRV appears to repre- 19. Dekker JM, Schouten EG, Klootwijk P, Pool J, Swenne CA, Kromhout D. sent an index of psychological self-regulatory control, Heart rate variability from short electrocardiographic recordings predicts such that individuals with greater resting HRV have mortality from all causes in middle-aged and elderly men. The Zutphen Study. Am J Epidemiol. 1997;145(10):899-908. performed better on tests of executive function. 20. Tsuji H, Venditti FJ Jr, Manders ES, et al. Reduced heart rate variability and In addition to assessing regulatory capacity, HRV mortality risk in an elderly cohort. The Framingham Heart Study. can also be used in the context of real-time feedback to Circulation. 1994;90(2):878-83. 21. Huikuri HV, Jokinen V, Syvänne M, et al. Heart rate variability and progres- help restore regulatory capacity. Heart rhythm coher- sion of coronary atherosclerosis. Arterioscler Thromb Vasc Biol. ence approaches train clients to produce auto-coher- 1999;19(8):1979-85. 22. Sajadieh A, Nielsen OW, Rasmussen V, Hein HO, Abedini S, Hansen JF. ent heart rhythms with a single peak in the LF region Increased heart rate and reduced heart-rate variability are associated with (typically around 0.1 Hz) with no significant peaks in subclinical inflammation in middle-aged and elderly subjects with no the VLF and HF regions. Emotional self-regulation apparent heart disease. Eur Heart J. 2004;25(5):363-70. 23. 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Publisher: Pubmed Central
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ISSN: 2164-957X
eISSN: 2164-9561
DOI: 10.7453/gahmj.2014.073
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Abstract

GLOBAL ADVANCES IN HEALTH AND MEDICINE rEVIEW Heart rate Variability: new perspectives on physiological Mechanisms, assessment of self-regulatory Capacity, and Health risk 心率变异性：关于生理机制、自律能力和健康风险评估的新观点 Variabilidad de frecuencia cardiaca: Nuevas perspectivas sobre mecanismos fisiológicos, valoración de la capacidad autorreguladora y riesgo de la salud Rollin McCraty, PhD; United States; Fred Shaffer, PhD, BCB, United States author affiliations aBstraCt 摘要 ofrece nuevas perspectivas sobre Institute of HeartMath, Heart rate variability, the change in 心率变异性 (HRC)（在相邻心跳之 los mecanismos subyacentes al Boulder Creek, the time intervals between adjacent 间的时间间隔的变化）是相互依存 ritmo de muy baja frecuencia de la California, (Dr McCraty); Center for Applied heartbeats, is an emergent property of 的调节系统的一种紧急特性，在不 variabilidad de la frecuencia cardia- Psychophysiology, interdependent regulatory systems 同时段内发生，以适应环境和心理 ca. Se analiza la interpretación de Truman State University, that operates on different time scales 挑战。这篇文章简要回顾了心脏的 los ritmos de la variabilidad de la Kirksville, Missouri, to adapt to environmental and psy- 神经调节，在心率变异性的极低频 frecuencia cardiaca en el contexto (Dr Shaffer). chological challenges. This article 率节奏机制方面，提供了一些新的 del riesgo para la salud y la valor- Correspondence briefly reviews neural regulation of 观点。在健康风险和生理及心理自 ación de la capacidad autorregula- Rollin McCraty, PhD the heart and offers some new per- 我调节能力评估讨论的背景下解读 toria fisiológica y psicológica. Los [email protected] spectives on mechanisms underlying HRV 节律。伴有心血管系统输入功 centros reguladores cardiovascula- Citation the very low frequency rhythm of 能的更高级的大脑中枢集成输入的 res de la médula espinal y del bulbo Global Adv Health Med. heart rate variability. Interpretation of 脊髓和延髓心血管监管中心，通过 raquídeo integran entradas de cen- 2015;4(1):46-61. DOI: heart rate variability rhythms in the 交感和副交感神经传出通路调节心 tros cerebrales superiores con 10.7453/gahmj.2014.073 context of health risk and physiologi- 率和血压。我们还讨论了先天性心 entradas de sistemas cardiovascula- Key Words cal and psychological self-regulatory 脏神经系统和心脏大脑连接通路， res aferentes para ajustar la fre- Heart rate variability, capacity assessment is discussed. The 借以传入信息并可以影响皮质下 cuencia cardiaca y la tensión arte- physiological mecha- cardiovascular regulatory centers in 区，皮质前区和运动皮质区的活 rial por vías eferentes simpáticas y nisms, self-regulatory capacity, health risk the spinal cord and medulla integrate 动。此外，审查了使用实时的 HRV parasimpáticas. También hablamos inputs from higher brain centers with 反馈以提高自我调节能力。我们的 sobre el sistema cardiaco nervioso disclosures afferent cardiovascular system inputs 结论是，心脏节律的特征在于在更 intrínseco y las vías de conexión The authors completed the ICMJE Form for to adjust heart rate and blood pressure 长的时段上既有复杂性又有稳定 corazón-cerebro, a través de las Disclosure of Potential via sympathetic and parasympathetic 性，这反映出这些内部自我调节系 cuales la información aferente Conflicts of Interest. efferent pathways. We also discuss the 统的生理和心理功能状态。 puede influir sobre la actividad en Dr McCraty disclosed intrinsic cardiac nervous system and las áreas subcortical, frontocortical that he is employed by the Institute of the heart-brain connection pathways, y de la corteza motora. Además, se HeartMath, which sells sInOpsIs through which afferent information revisa el uso de retroalimentación one of the several heart can influence activity in the subcor- La variabilidad de la frecuencia car- de variabilidad de la frecuencia car- rate variability feedback diaca, o modificación de los inter- devices that are men- tical, frontocortical, and motor cor- diaca a tiempo real para aumentar tioned in the article. tex areas. In addition, the use of real- valos de tiempo entre los latidos la capacidad autorreguladora. Dr Shaffer had no consecutivos del corazón, es una time HRV feedback to increase self- Concluimos que los ritmos cardia- conflicts to disclose. regulatory capacity is reviewed. We propiedad emergente de los siste- cos se caracterizan tanto por su mas reguladores interdependientes conclude that the heart’s rhythms are complejidad como por su estabili- characterized by both complexity and que opera sobre diferentes escalas dad sobre escalas temporales más temporales para adaptarse a los stability over longer time scales that largas que reflejan los estados fun- reflect both physiological and psycho- retos ambientales y psicológicos. cionales tanto fisiológicos como Este artículo revisa brevemente la logical functional status of these inter- psicológicos de estos sistemas nal self-regulatory systems. regulación nerviosa del corazón y internos autorreguladores. IntrOduCtIOn condition. However, with the introduction of signal Since Walter Cannon introduced the concept of processing technologies that can acquire continuous homeostasis, the study of physiology has been based time series data from physiological processes such as on the principle that all cells, tissues, and organs heart rate (HR), blood pressure (BP), and nerve activi- strive to maintain a static or constant “steady-state” ty, it has become abundantly apparent that biological 46 Volume 4, Number 1 • January 2015 • www.gahmj.com Review hEART RATE VARIABILITY: NEw PERSPEcTIVES processes vary in complex and nonlinear ways, even anxiety, depression, asthma, and sudden infant 23-26 during so called “steady-state” conditions. These death. Reduced HRV may correlate with disease observations have led to the understanding that and mortality because it reflects reduced regulatory healthy, optimal function is a result of continuous, capacity and ability to adaptively respond to physio- dynamic, bi-directional interactions among multiple logical challenges such as exercise. For example, in the neural, hormonal, and mechanical control systems at Chicago Health, Aging, and Social Relations Study, both local and central levels. In concert, these physi- separate metrics for the assessment of autonomic bal- ological and psychological regulatory systems are ance and overall cardiac autonomic regulation were never truly at rest and are certainly never static. For developed and tested in a sample of 229 participants. example, we now know that the normal resting In this study, overall regulatory capacity was a signifi- rhythm of the heart is highly variable rather than cant predictor of overall health status, but autonomic being monotonously regular, which was the wide- balance was not. In addition, cardiac regulatory capac- spread notion for many years. ity was negatively associated with the prior incidence of myocardial infarction. The authors suggest that HEart ratE VarIaBILIty cardiac regulatory capacity reflects a physiological The investigation of the heart’s complex rhythms state that is more relevant to health than the indepen- or what is now called heart rate variability (HRV) dent sympathetic or parasympathetic controls or the began with the emergence of modern signal processing autonomic balance between these controls as indexed in the 1960s and 1970s, and has rapidly expanded in by different measures of HRV. more recent times. The irregular behavior of the heart- When speaking of autonomic balance, it should beat is readily apparent when HR is examined on a be kept in mind that a healthy system is constantly and beat-to-beat basis, but is overlooked when a mean value dynamically changing. Therefore, an important indica- over time is calculated. These fluctuations in HR result tor of the health status of the regulatory systems is the from complex, nonlinear interactions among a number capacity to respond to and adjust the relative auto- of different physiological systems. HRV is thus consid- nomic balance (eg, HR) to the appropriate state for the ered a measure of neurocardiac function that reflects context the person is engaged in at any given moment. heart–brain interactions and autonomic nervous sys- In other words, does the HR dynamically respond? Is it 3,4 tem (ANS) dynamics. higher during the daytime or when someone is dealing An optimal level of HRV within an organism with challenging tasks and lower when at rest or dur- reflects healthy function and an inherent self-regulatory ing sleep? The inability of the physiological self-regula- 4-10 capacity, adaptability, or resilience. Too much insta- tory systems to adapt to the current context and situa- bility, such as arrhythmias or nervous system chaos, is tion is associated with numerous clinical conditions. detrimental to efficient physiological functioning and Also distinct, altered, circadian patterns in 24-hour energy utilization. However, too little variation indi- heart rates are associated with different and specific 29,30 cates age-related system depletion, chronic stress, psychiatric disorders, particularly during sleep. pathology, or inadequate functioning in various levels HR estimated at any given time represents the net 2,11,12 of self-regulatory control systems. effect of the neural output of the parasympathetic The importance of HRV as an index of the func- (vagus) nerves, which slow HR, and the sympathetic tional status of physiological control systems was nerves, which accelerate it. In a denervated human noted as far back as 1965 when it was found that fetal heart where there are no connections from the ANS to distress is preceded by reductions in HRV before any the heart following its transplantation, the intrinsic changes occur in HR itself. In the 1970s, reduced rate generated by the pacemaker (SA node) is about 100 HRV was shown to predict autonomic neuropathy in beats per minute (bpm). Parasympathetic activity 14-16 diabetic patients before the onset of symptoms. predominates when HR is below this intrinsic rate dur- Reduced HRV was also found to be a greater risk factor ing normal daily activities and when at rest or sleep. of death post–myocardial infarction than other known When HR is above about 100 bpm, the relative balance risk factors. It has clearly been shown that HRV shifts and sympathetic activity predominates. declines with age and age-adjusted values should be Therefore, HR best reflects the relative balance between used in the context of risk prediction. Age-adjusted the sympathetic and parasympathetic systems. The HRV that is low has been confirmed as a strong, inde- average 24-hour HR in healthy people is approximately pendent predictor of future health problems in both 73 bpm. Higher HRs are independent markers of mor- healthy people. Age-adjusted HRV correlates with all- tality in a wide spectrum of conditions. 19,20 cause mortality. In prospective studies reduced It is important to note the natural relationship HRV has been the strongest independent predictor of between HR and amount of HRV. As HR increases the progression of coronary atherosclerosis. A num- there is less time between heartbeats for variability to ber of studies have shown that reduced HRV is associ- occur, thus HRV decreases. At lower HRs there is more ated with measures of inflammation in subjects with time between heartbeats and variability naturally no apparent heart disease. Reduced HRV is also increases. This is called cycle length dependence, and observed in patients with autonomic dysfunction, it persists in the healthy elderly to a variable degree, Review www.gahmj.com • January 2015 • Volume 4, Number 1 47 GLOBAL ADVANCES IN HEALTH AND MEDICINE even at a very advanced age. However, elderly patients in direct contrast to vagal stimulation, which is almost with ischemic heart disease or other pathologies instantaneous. Thus, any sudden change in HR, up or develop less variability at increasingly lower HRs and down or between one beat and the next, is primarily 33,34 ultimately lose the relationship between HR and vari- parasympathetically mediated. ability, to the point that variability does not increase Patient age may mediate the relationship between with reductions in HR. Even in healthy subjects, the reduced HRV and regulatory capacity of physiological effects of cycle length dependence should be taken control systems. Age-related reductions in HRV may into account when assessing HRV. HR values should reflect the loss of neurons in the brain and spinal cord, also always be reported, especially when HRs are resulting in degraded signal transmission and reduced increased due to factors like stress reactions, medica- regulatory capacity. Reduced physiological regulato- tions, and physical activity. ry capacity may contribute to functional gastrointes- 35,36 Efferent (descending) sympathetic nerves target tinal disorders, inflammation, and hypertension. the SA node via the intrinsic cardiac nervous system and the bulk of the myocardium. Action potentials HEart ratE VarIaBILIty anaLysIs MEtHOds conducted by these motor neurons trigger norepineph- HRV can be assessed with various analytical rine and epinephrine release, which increases HR and approaches, although the most commonly used are strengthens the contractility of the atria and ventricles. frequency domain (power spectral density) analysis Following the onset of sympathetic stimulation, there and time domain analysis. The interactions between is a delay of up to 5 seconds before the stimulation autonomic neural activity, BP, respiration, and higher induces a progressive increase in HR, which reaches a level control systems produce both short and longer 4,12,37 steady level in 20 to 30 seconds if the stimulus is con- term rhythms in HRV measurements. The most tinuous. Even a brief sympathetic stimulus can affect common form for observing these changes is the HR the HR and the HRV rhythm for 5 to 10 seconds. The tachogram, a plot of the sequence of time intervals relatively slow response to sympathetic stimulation is between heartbeats (Figure 1). High stress: public speaking High energy expenditure: exercise Figure 1 An example of the heart rate (HR) tachogram, a plot of the sequence of time intervals between heartbeats over an 8-hour period in ambulatory recording taken from a 36-year-old male. Each of the traces is 1 hour long, with the starting time of the hour on the left hand side of the figure. The time between each vertical line is 5 minutes. The vertical axis within each of the hourly tracings is the time between heartbeats (inter-beat-intervals) ranging between 400 and 1200 milliseconds (label shown on second row). The hours beginning at 10:45 through 12:45 were during a time when he was in a low-stress classroom setting. His overall HR increased, and the range of the HRV is considerably less during the hour starting at 13:45 (public speaking), when he was presenting to the class. In this case, the relative autonomic nervous system balance is shifted to sympathetic predominance due to the emotional stress around presenting to a group of his peers. Once the presentation completed near the end of the hour, his HR dropped and normal HRV was restored. In the following hours, he was listening to others present and providing feedback. In the hour starting at 17:45, he was engaged in physical exercise (walking up a long steep hill) starting about 20 minutes into the hour where his HR is increased and the HRV is reduced due to cycle-length dependence effects. 48 Volume 4, Number 1 • January 2015 • www.gahmj.com Review hEART RATE VARIABILITY: NEw PERSPEcTIVES HEart ratE VarIaBILIty FrEQuEnCy Bands and Low-frequency Band pHysIOLOGICaL MECHanIsMs The LF range is between 0.04 Hz and 0.15 Hz, The European Society of Cardiology and the North which equates to rhythms or modulations with periods American Society of Pacing and Electrophysiology Task that occur between 7 and 25 seconds. This region was Force Report on HRV divided heart rhythm oscillations previously called the “baroreceptor range” or “mid-fre- into 4 primary frequency bands: high-frequency (HF), quency band” by many researchers, since it primarily low-frequency (LF), very-low-frequency (VLF), and reflects baroreceptor activity while at rest. ultra-low-frequency (ULF). Most HRV analysis is done Baroreceptors are stretch-sensitive mechanoreceptors in 5-minute segments (of a 24-hour recording), although located in the chambers of the heart and vena cavae, other recording periods are often used. When other carotid sinuses (which contain the most sensitive recording lengths are analyzed, the length of the record- mechanoreceptors), and the aortic arch. As discussed ing should be reported since this has large effects on previously, the vagus nerves are a major conduit both HRV frequency and time domain values. though which afferent (ascending) neurological sig- nals from the heart are relayed to the brain, including High-frequency Band baroreflex signals. Baroreflex gain is commonly calcu- The HF range is from 0.15 Hz to 0.4 Hz, which lated as the beat-to-beat change in HR per unit of equates to rhythms with periods that occur between change in systolic BP. Decreased baroreflex gain is 2.5 and 7 seconds. This band reflects parasympathetic related to aging and impaired regulatory capacity. or vagal activity and is frequently called the respiratory The cardiovascular system resonance frequency band because it corresponds to the HR variations relat- is a distinctive high-amplitude peak in the HRV ed to the respiratory cycle known as respiratory sinus power spectrum around 0.1 Hz. It has long been estab- arrhythmia. The mechanisms linking the variability of lished that it is caused by a delay in the feedback loops HR to respiration are complex and involve both central within the baroreflex system between the heart and 38 48,49 and reflex interactions. During inhalation, the cardio- brain. In humans and many other mammals, the respiratory center inhibits vagal outflow resulting in resonance frequency of the system is approximately accelerating the HR. Conversely, during exhalation, 0.1 Hz, which is also characteristic of the coherent vagal outflow is restored resulting in slowing the HR. state described later. Although the magnitude of the oscillation is variable, The sympathetic nervous system does not appear in healthy people it can be increased by slow, deep to have much influence in rhythms above 0.1 Hz, while breathing. In younger healthy individuals, it is not the parasympathetic system can be observed to affect uncommon to see an obvious increase in the HF band heart rhythms down to 0.05 Hz (20-sec rhythm). 40,41 at night with a decrease during the day. Therefore, during periods of slow respiration rates, In terms of psychological regulation, reduced vagal activity can easily generate oscillations in the 50-52 vagally mediated HRV has been linked to reduced self- heart rhythms that cross over into the LF band. regulatory capacity and cognitive functions that Therefore, respiratory-related efferent vagally mediat- involve the executive centers of the prefrontal cortex. ed influences are particularly present in the LF band This is consistent with the finding that lower HF power when respiration rates are below 8.5 breaths per min- is associated with stress, panic, anxiety, or worry. ute (approximately 1 breath every 7 seconds) or when 52,53 Lowered parasympathetic activity, rather than reduced an individual sighs or takes a deep breath. sympathetic functioning, appears to account for the In ambulatory 24-hour HRV recordings, it has reduced HRV in aging. been suggested that the LF band reflects sympathetic A number of studies have shown that total vagal activity and the LF/HF ratio has been controversially blockade essentially eliminates HF oscillations and used to assess the balance between sympathetic and 42,43 54-56 reduces power in the LF range. Some investigators parasympathetic activity. A number of research- have used pharmacological blockade (eg, atropine) ers have challenged this perspective and have persua- and found greatly reduced HRV, including the LF and sively argued that in resting conditions, the LF band VLF bands. As a result, they have concluded that all reflects baroreflex activity and not cardiac sympa- 39,57-61 HRV is produced by parasympathetic mechanisms (eg, thetic innervation. 44,45 breathing) However, these investigations did not take into account that atropine and related agents Very-low-frequency Band have much broader effects than only blocking para- The VLF is the power in the range between 0.0033 sympathetic activity. These substances also target the and 0.04 Hz, which equates to rhythms or modulations intrinsic cardiac nervous system, especially the local with periods that occur between 25 and 300 seconds. circuit neurons, which are critical in cardiac control, Although all 24-hour clinical measures of HRV reflect- afferent communication, and the generation of HRV. ing low HRV are linked with increased risk of adverse It has been shown that atropine and similar substanc- outcomes, the VLF band has stronger associations with 46 20,62-64 es also affect sympathetic neurons, so it would be all-cause mortality than the LF and HF bands. expected that these blockades would affect HRV across Low VLF power has been shown to be associated with all frequency bands. arrhythmic death and posttraumatic stress disorder Review www.gahmj.com • January 2015 • Volume 4, Number 1 49 GLOBAL ADVANCES IN HEALTH AND MEDICINE (PTSD). Additionally, low power in this band has been Following up on these results, Armour and col- 67,68 associated with high inflammation and has been leagues developed methods to obtain long-term single- correlated with low levels of testosterone. In contrast, neuron recordings from a beating heart, and simultane- other biochemical markers, such as those mediated by ously, from extrinsic cardiac neurons. Figure 2 shows the hypothalamic-pituitary-adrenal (HPA) axis axis (eg, the VLF rhythm obtained from an afferent neuron cortisol), did not. Longer time periods using 24-hour located in the intrinsic cardiac nervous system in a dog HRV recordings should be obtained to provide compre- heart. In this case, the VLF rhythm is generated from hensive assessment of VLF and ULF fluctuations. intrinsic sources and cannot be explained by sources Historically, the physiological explanation and such as movement. The black bar at the bottom of the mechanisms involved in the generation of the VLF figure labeled “rapid ventricular pacing” shows the component have not been as well defined as the LF and time period where efferent spinal neurons were stimu- HF components. This region has been largely ignored lated. The resulting increase in efferent sympathetic even though it is the most predictive of adverse out- activity clearly elevates the amplitude of the afferent comes. Long-term regulatory mechanisms and ANS neuron’s intrinsic VLF rhythm (top row). activity related to thermoregulation, the renin-angio- Work by Armour and other investigators imply tensin system, and other hormonal factors appear to that the VLF rhythm is generated by the stimulation of 71,72 contribute to this band. afferent sensory neurons in the heart, which in turn Recent work by Armour has shed new light on the activate various levels of the feedback and feed-forward primary mechanisms underlying the VLF rhythm. This loops in the heart’s intrinsic cardiac nervous system, line of research began after some surprising results neurons in the extrinsic cardiac ganglia, and spinal 57,76 from a study looking at HRV in auto-transplanted column. Thus, the VLF rhythm appears to be pro- hearts in dogs. In auto-transplants, the heart is removed duced by the heart itself and may be an intrinsic and placed back in the same animal so there is no need rhythm that is fundamental to health and wellbeing. for anti-rejection medications. The primary purpose of This cardiac origin of the VLF rhythm is also supported the study was to determine if the autonomic nerves re- by studies showing that sympathetic blockade does not innervated the heart posttransplant. Monthly 24-hour affect VLF power. Furthermore, VLF activity remains in HRV recordings were done over a 1-year period on all quadriplegics, whose sympathetic innervation of the the dogs with auto-transplanted hearts as well as the heart and lungs is disrupted. control dogs. The nerves did re-innervate but in a way Thus, experimental evidence suggests that the that was not accurately reflected in HRV. It showed that VLF rhythm is intrinsically generated by the heart the intrinsic cardiac nervous system has neuroplasticity and that the amplitude and frequency of these oscilla- and re-structured its neural connections. The truly sur- tions are modulated by efferent sympathetic activity. prising result was that these de-innervated hearts had Normal VLF power appears to indicate healthy func- higher levels of HRV, including HRV that is typically tion, and increases in resting VLF power and or shift- associated with respiration, than control dogs immedi- ing of their frequency can reflect efferent sympathetic ately posttransplant. These levels were sustained over a activity. The modulation of the frequency of this 73 78 1-year period. This was unexpected as there is very rhythm due to physical activity, stress responses, little HRV in human transplant recipients. and other factors that increase efferent sympathetic Average: 90-sec rhythm Range: 75-100 sec (0.013 - 0.1 Hz) Neuronal Activity 20 /5 sec Activated neurons LV IMP (mmHg) Rapid ventricular pacing 0 50 100 150 200 250 300 350 400 450 500 550 600 650 700 750 800 850 900 950 Figure 2 Long-term single-neuron recordings from an afferent neuron in the intrinsic cardiac nervous system in a beating dog heart. The top row shows neural activity. The second row is the actual neural recording. The third row is the left ventricular pressure. This intrinsic rhythm has an average period of 90 seconds with a range between 75 to 100 seconds (0.013 Hz - 0.01 Hz), which falls within the VLF band. Used with permission from Dr J. Andrew Armour. 50 Volume 4, Number 1 • January 2015 • www.gahmj.com Review hEART RATE VARIABILITY: NEw PERSPEcTIVES activation can cause it to cross over into the lower easily detected in healthy individuals. region of the LF band during ambulatory monitoring Circadian rhythms, core body temperature, or during short-term recordings when there is a sig- metabolism, hormones, and intrinsic rhythms gener- nificant emotional stressor. ated by the heart all contribute to lower frequency rhythms (eg, VLF and ULF) that extend below 0.04 Hz. ultra-low-frequency Band In healthy individuals, there is an increase in VLF The ultra-low-frequency band (ULF) falls below power that occurs during the night and peaks before 79,80 0.0033 Hz (333 seconds or 5.6 minutes). Oscillations or waking. This increase in autonomic activity events in the heart rhythm with a period of 5 minutes or appears to correlate with the morning cortisol peak. greater are reflected in this band and it can only be assessed with 24-hour and longer recordings. The cir- power spectral analysis cadian oscillation in HR is the primary source of the Power spectral analysis is used to separate the ULF power, although other very slow-acting regulatory complex HRV waveform into its component rhythms processes, such as core body temperature regulation, that operates within different frequency ranges (Figure metabolism, and the renin-angiotensin system likely 3). Spectral analysis provides information regarding add to the power in this band. The Task Force Report how power is distributed (the variance and amplitude on HRV suggests that 24-hour recordings should be of a given rhythm) as a function of frequency (the time divided into 5-minute segments and that HRV analysis period of a given rhythm). The main advantages of should be performed on the individual segments prior spectral analysis are that it supplies both frequency to the calculation of mean values. This effectively filters and amplitude information on the specific rhythms out any oscillations with periods longer than 5 minutes. that exist in the HRV waveform, providing a means to However, when spectral analysis is applied to entire quantify these oscillations over any given period. The 24-hour records, several lower frequency rhythms are values are expressed as the power spectral density, Original VLF LF HF 4:29 AM 4:34 AM 4:39 AM 4:44 AM 50% 25 40% 30% 20% 10% 0% 0.00 0.05 0.10 0.15 0.20 0.25 0.30 0.35 0.40 VLF LF HF Frequency (Hz) Figure 3 A typical heart rate variability (HRV) recording over a 15-minute period during resting conditions in a healthy individual. The top tracing shows the original HRV waveform. Filtering techniques were used to separate the original waveform into VLF, LF, and HF bands as shown in the lower traces. The bottom of the figure shows the power spectra (left) and the percentage of power (right) in each band. abbreviations: HF, high frequency; LF, low frequency; PSD: power spectral density; VLF, very low frequency. Review www.gahmj.com • January 2015 • Volume 4, Number 1 51 Heart Rate Power Spectral Density (ms /Hz) Normalized Power GLOBAL ADVANCES IN HEALTH AND MEDICINE which is the area under the curve (peak) in a given seconds. This measure reflects the ebb and flow of all the bandwidth of the spectrum. The power or height of the factors that contribute to HRV. In 24-hour recordings, peak at any given frequency indicates the amplitude the SDNN is highly correlated with ULF and total and stability of the rhythm. The frequency reflects the power. In short-term resting recordings, the primary period of time over which the rhythm occurs. For source of the variation is parasympathetically mediated, example, a 0.1 Hz frequency has a period of 10 seconds. especially with slow, deep breathing protocols. However, in ambulatory and longer term recordings the SDNN autonomic Balance and the Low-frequency:High- values are highly correlated with lower frequency frequency ratio rhythms. Thus, low age-adjusted values predict morbid- The autonomic balance hypothesis assumes that ity and mortality. For example, patients with moderate the sympathetic and parasympathetic competitively SDNN values (50-100 milliseconds) have a 400% lower regulate HR (accentuated antagonism), where risk of mortality than those with low values (0-50 milli- 81,82 increased sympathetic activity is paired with seconds) in 24-hour recordings. decreased parasympathetic activity. While some orthostatic challenges can produce reciprocal chang- standard deviation of the normal-to-normal Index es in sympathetic activation and vagal withdrawal, The SDNN index is the mean of the standard devia- psychological stressors can also result in independent tions of all the NN intervals for each 5-minute segment. changes in sympathetic or parasympathetic activity. Therefore, this measurement only estimates variability It is now generally accepted that both branches of the due to the factors affecting HRV within a 5-minute ANS are simultaneously active. period. In 24-hour HRV recordings, it is calculated by The ratio of LF to HF power is controversial due to first dividing the 24-hour record into 288 five-minute the issues regarding the LF band described above. It is segments and then calculating the standard deviation often assumed that a low LF:HF ratio reflects greater of all NN intervals contained within each segment. The parasympathetic activity relative to sympathetic activ- SDNN index is the average of these 288 values. The ity. However, this ratio is often shifted due to reduc- SDNN index is believed to primarily measure auto- tions in LF power. Therefore, the LF:HR ratio should be nomic influence on HRV. This measure tends to corre- interpreted with caution and the mean values of HF late with VLF power over a 24-hour period. and LF power taken into consideration. In contrast, a high LF:HF ratio may indicate higher sympathetic the root Mean square of successive differences activity relative to parasympathetic activity as can be The RMSSD is the root mean square of successive observed when people engage in meeting a challenge differences between normal heartbeats. This value is that requires effort and increased sympathetic activa- obtained by first calculating each successive time dif- tion. Alternatively, it can indicate increased parasym- ference between heartbeats in milliseconds. Each of the pathetic activity as occurs during slow breathing. values is then squared and the result is averaged before Again, the same cautions must be taken into consider- the square root of the total is obtained. The RMSSD ation, especially in short-term recordings. reflects the beat-to-beat variance in HR and is the pri- mary time domain measure used to estimate the vagal- tIME dOMaIn MEasurEMEnts OF HEart ratE ly mediated changes reflected in HRV. The RMSSD is VarIaBILIty correlated with HF power and therefore also reflects Time domain measures are the simplest to calcu- self-regulatory capacity as discussed earlier. late. Time domain measures do not provide a means to adequately quantify autonomic dynamics or determine nEurOBIOLOGy OF sELF-rEGuLatIOn the rhythmic or oscillatory activity generated by the dif- Considerable evidence from clinical, physiologi- ferent physiological control systems. However, since cal, and anatomical research has identified cortical, they are always calculated the same way, data collected subcortical and medulla oblongata structures by different researchers are comparable but only if the involved in self-regulation. Oppenheimer and recordings are exactly the same length of time and the Hopkins mapped a detailed hierarchy of cardiac con- data are collected under the same conditions. Time trol structures among the cortex, amygdala and other domain indices quantify the amount of variance in the subcortical structures, all of which can modify cardio- inter-beat-intervals (IBI) using statistical measures. The vascular-related neurons in the lower levels of the three most important and commonly reported time neuraxis (Figure 4). They suggest that the amygdala domain measures are the standard deviation of normal- is involved with refined integration of emotional con- to-normal (SDNN), the SDNN index, and the root mean tent in higher centers to produce cardiovascular square of successive differences (RMSSD) are the most responses that are appropriate for the emotional commonly reported metrics. aspects of the current circumstances. The insular cortex and other centers such as the the standard deviation of the normal-to-normal orbitofrontal cortex and cingulate gyrus can overcome The SDNN is the standard deviation of the normal- (self-regulate) emotionally entrained responses by to-normal (NN) sinus-initiated IBIs measured in milli- inhibiting or enhancing them. They also point out that 52 Volume 4, Number 1 • January 2015 • www.gahmj.com Review hEART RATE VARIABILITY: NEw PERSPEcTIVES Insular and Prefrontal Cortex Bed Nucleus Central Nucleus Lateral Paraventricular Stria Terminals Hypothalamus Amygdala Hypothalamus Periaqueductal Gray Dorsal Vagal Rostral Ventrolateral Complex Medulla Figure 4 Schematic diagram showing the relationship of the principal descending neural pathways from the insular and prefrontal cortex to subcortical structures and the medulla oblongata as outlined by Oppenheimer and Hopkins. The insular and prefrontal cortexes are key sites involved in modulating the heart’s rhythm, particularly during emotionally charged circumstances. These structures alone with other centers such as the orbitofrontal cortex and cingulate gyrus can inhibit or enhance emotional responses. The amygdala is involved with refined integration of emotional content in higher centers to produce cardiovascular responses that are appropriate for the emotional aspects of the current circumstances. Imbalances between the neurons in the insula, amygdala and hypothalamus may initiate cardiac rhythm disturbances and arrhythmias. The structures in the medulla represent an interface between incoming afferent informa- tion from the heart, lungs and other body systems and outgoing efferent neuronal activity. imbalances between the neurons in the insula, amyg- uals are stressed or threatened and prolonged prefron- dala and hypothalamus may initiate cardiac rhythm tal inactivity can lead to hypervigilance, defensive- disturbances and arrhythmias. The data suggest that ness, and social isolation. the insular and medial prefrontal cortexes are key sites involved in modulating the heart’s rhythm, particular- Vagal Control system ly during emotionally charged circumstances. The cardiovascular control system is highly dis- Thayer and Lane have also have described the tributed throughout the central nervous system and same set of neural structures which they call the cen- interacts both widely and reciprocally with many tral autonomic network (CAN). The CAN is involved other neural control systems, especially with the respi- in cognitive, affective, and autonomic regulation. The ratory system. The final common output pathways for CAN is related to HRV and linked to cognitive perfor- the cardiorespiratory control system are located in the mance. In their model, the CAN links the nucleus of medulla oblongata. The medulla contains many neu- tractus solitarius (NTS) in the medulla with the ante- rons that act as interneurons and premotor neurons as rior cingulate, insula, prefrontal cortex, amygdala, and well as separate neuronal populations for respiratory hypothalamus through a series of feedback and feed- and cardiovascular regulation. The cell groups forming forward loops. They also propose that this network is the cardiorespiratory control system have an intimate an integrated system for internal self-regulation by relationship, which allows for a highly integrated regu- which the brain controls the heart, other visceromotor lation of motor output. The medulla represents an organs, and neuroendocrine and behavioral responses interface between incoming afferent information and that are critical for goal-directed behavior, adaptabili- outgoing efferent neuronal activity. An important ty, and sustained health. They suggest that these function of the cardiorespiratory control system is the dynamic connections explain why vagally mediated respiratory modulation of both sympathetic and para- HRV is linked to higher-level executive functions and sympathetic outflow that is present in the activity pat- reflects the functional capacity of the brain structures terns of spinal preganglionic neurons. that support working memory and emotional and The NTS of the medulla oblongata integrates affer- physiological self-regulation. They have shown that ent sensory information from proprioceptors (body vagally mediated HRV is correlated with prefrontal position), chemoreceptors (blood chemistry), and cortical performance and the ability to inhibit unwant- mechanoreceptors (also called baroreceptors) from the ed memories and intrusive thoughts. Furthermore, the heart, lungs, and face. The NTS connects to the dorsal prefrontal cortex can be taken “offline” when individ- motor nucleus of the vagus nerve and the nucleus Review www.gahmj.com • January 2015 • Volume 4, Number 1 53 GLOBAL ADVANCES IN HEALTH AND MEDICINE ambiguous (NA). Neurocardiology research indicates variability in HR and BP. The medulla oblongata is the that the efferent vagal fibers that innervate the heart major structure integrating incoming afferent informa- are primarily A-fibers, the largest and fastest conduct- tion from the heart, lungs and face with inputs from ing axons that originate from somata located primarily cortical and subcortical structures and is the source of in the NA. The NA also receives and integrates informa- the respiratory modulation of the activity patterns in tion from the cortical and subcortical systems. Thus, sympathetic and parasympathetic outflow. The intrin- the vagal regulatory centers respond to peripheral sen- sic cardiac nervous system integrates mechanosensi- sory (afferent) inputs and higher brain center inputs to tive and chemosensitive neuron inputs with efferent adjust efferent neuronal outflows, which results in the information from both the sympathetic and parasym- vagally mediated beat-to-beat changes in HR. pathetic inputs from the brain. As a complete system, it Since BP regulation is a central role of the cardio- affects HRV, vasoconstriction, venoconstriction, and vascular system, the factors that alter BP also affect cardiac contractility in order to regulate HR and BP. beat-to-beat fluctuations and therefore, the heart rhythms. Intrinsic cardiac afferent sensory neurons afferent Modulation of Cardiac and Brain activity transduce and distribute mechanical and chemical The field of neurocardiology has extensively information regarding the heart to the intrinsic car- explored the anatomy and functions of the intrinsic diac nervous system. The afferent impulses from the cardiac nervous system along with its connections 75,86 intrinsic cardiac neurons travel via the vagal nerves to with the brain. While efferent regulation of the the nodose ganglia and then to the NTS. The NTS has heart by the vagus nerves is generally well known, the connections with the NA and spinal cord resulting in majority of fibers in the vagus nerves are afferent in modulation of activity patterns in both parasympa- nature. Furthermore, more vagal fibers are related to thetic and sympathetic outflow to the heart and the cardiovascular pathways than other organs. Complex blood vessels. There is controversy regarding any patterns of cardiovascular afferent nerve activity occur inhibitory role of parasympathetic efferent pregangli- across time scales from milliseconds to minutes. The onic neurons in the dorsal motor vagal (DMV) com- intrinsic cardiac nervous system has both short-term plex of the medulla as a number of anatomical studies and long-term memory functions, which can influence suggest that virtually all efferent projections from the HRV and afferent activity related to BP, rhythm, rate, 83 70,88,89 DMV are to subdiaphragmatic structures. and hormonal factors. The intrinsic cardiac neu- The vagus nerves innervate the intrinsic cardiac rons (sensory, interconnecting, afferent, and motor) nervous system. A few of these connections synapse on can operate independently of central neuronal com- motor neurons in the intrinsic cardiac nervous system mand, and their network is sufficiently extensive to be that project directly to the SA node (and other tissues in characterized as its own “little brain” in the heart 84,90 the heart) where they trigger acetylcholine release to (Figure 5). The afferent nerves play a critical role in slow HR. However, the majority of the efferent pre- physiological regulation and affect the heart’s rhythm ganglionic vagal neurons (~80%) connect to local cir- and HRV. Efferent sympathetic and parasympathetic cuitry neurons in the intrinsic cardiac nervous system activity is integrated in the heart’s intrinsic nervous where motor information is integrated with inputs system, with the signals arising from the mechanosen- from mechanosensitive and chemosensory neurons in sory and chemosensory neurons in the heart (Figure 6). the heart. Thus, efferent sympathetic and parasympa- The neural output of the intrinsic cardiac nervous sys- thetic activity is integrated in and with the activity tem then travel to the brain via afferent pathways in occurring in the heart’s intrinsic nervous system. This the spinal column and vagus nerve. Intrinsic cardiac includes the input signals from the mechanosensitive afferent neurons project to nodose and dorsal root gan- and chemosensory neurons within the heart, all of glia, the spinal cord, brainstem, hypothalamus, thala- 4,46,91 which ultimately contribute to beat-to-beat cardiac mus, or amygdala and then to the cerebral cortex. functional changes. John and Beatrice Lacey were the first to suggest a The response time of a single efferent vagal causal role of the heart in modulating cognitive func- impulse on the sinus node is very short and results in tions such as sensory-motor and perceptual perfor- 92-94 an immediate response that typically occurs within the mance. They suggested that cortical functions are cardiac cycle in which it occurs and affects only 1 or 2 modulated via afferent input from pressure sensitive 33 93 heartbeats after its onset. After cessation of vagal neurons in the heart, carotid arteries, and aortic arch. stimulation, HR rapidly increases to its previous level. Their research focused on activity occurring within a An increase in HR can also be achieved by reduced single cardiac cycle, and they confirmed that cardio- vagal activity (vagal withdrawal). Thus, any sudden vascular activity influences perception and cognitive change in HR, up or down, or between 1 beat and the performance. Research by Velden and Wölk later dem- 33,34 next, are primarily parasympathetically mediated. onstrated that cognitive performance fluctuated at a In summary, the cardiorespiratory control system rhythm around 10 Hz and showed that the modula- is complex, and information from many inputs is inte- tion of cortical function via the heart’s influence was grated at multiple levels of the system, all of which are due to afferent inputs on the neurons in the thalamus, 95,96 important for the generation of normal beat-to-beat which globally synchronizes cortical activity. An 54 Volume 4, Number 1 • January 2015 • www.gahmj.com Review hEART RATE VARIABILITY: NEw PERSPEcTIVES Figure 5 Microscopic image of interconnected intrinsic cardiac ganglia in the human heart. The thin, light blue structures are multiple axons that connect the ganglia. Used with permission from Dr J. Andrew Armour. important aspect of their work was the finding that it tems, it can pull the other systems into increased syn- is the “pattern and stability” (of the rhythm) of the chronization and more efficient function. For example, heart’s afferent inputs, rather than the number of neu- frequency pulling and entrainment can easily be seen ral bursts within the cardiac cycle, that are important between the heart, respiratory, and BP rhythms as well in modulating thalamic activity, which in turn has as between very-low-frequency brain rhythms, cranio- global effects on brain function. sacral rhythms, and electrical potentials measured 52,102 There has since been a growing body of research across the skin. indicating that afferent information processed by the We (McCraty and colleagues) introduced the term intrinsic cardiac nervous system can influence activi- physiological coherence to describe the degree of order, 4,97,98 58 ty in the frontocortical areas and motor cortex, harmony, and stability in the various rhythmic activi- affecting psychological factors such as attention level, ties within living systems over any given time period. 99 100 motivation, perceptual sensitivity, and emotion- This harmonious order signifies a coherent system that al processing. has an efficient or optimal function directly related to the ease and flow in life processes. By contrast, an COHErEnCE erratic, discordant pattern of activity denotes an inco- The various concepts and measurements embraced herent system whose function reflects stress and inef- under the term coherence have become central to fields ficient utilization of energy in life processes. as diverse as quantum physics, cosmology, physiology, Specifically, heart coherence (also referred to as cardiac and brain and consciousness research. Coherence coherence or resonance) can be measured by HRV always implies connectedness, correlations, stability analysis wherein a person’s heart rhythm pattern and efficient energy utilization. For example, we refer to becomes more ordered and sine-wave like at a frequen- people’s speech or thoughts as coherent if the words fit cy of around 0.1 Hz (10 seconds). A coherent heart together well and incoherent if they are uttering mean- rhythm is defined as a relatively harmonic, sine wave– ingless nonsense or ideas that make no sense as a whole. like, signal with a very narrow, high-amplitude peak in In physics and physiology, the term coherence is used to the LF region of the HRV power spectrum with no describe the degree of synchronization between differ- major peaks in the VLF or HF regions. Coherence is ent oscillating systems. This type of coherence is called assessed by identifying the maximum peak in the 0.04 cross-coherence which occurs when two or more of the Hz to 0.26 Hz range of the HRV power spectrum, calcu- body’s oscillatory systems, such as respiration and heart lating the integral in a window 0.030 Hz wide, centered rhythms, become entrained and operate at the same on the highest peak in that region, and then calculating frequency. The term auto-coherence describes coherent the total power of the entire spectrum. The coherence activity within a single oscillatory system. An example ratio is formulated as: (Peak Power/[Total Power – Peak is a system that exhibits sine wave like oscillations; the Power]). Physiological coherence includes specific more stable the frequency, amplitude and shape, the approaches for quantifying the various types of coher- higher the degree of coherence. When coherence is ence measures, such as cross-coherence (frequency increased in a system that is coupled with other sys- entrainment between respiration, BP, and heart Review www.gahmj.com • January 2015 • Volume 4, Number 1 55 GLOBAL ADVANCES IN HEALTH AND MEDICINE Figure 6 The neural communication pathways interacting between the heart and the brain are responsible for the generation of heart rate variability. The intrinsic cardiac nervous system integrates information from the extrinsic nervous system and from the sensory neu- rites within the heart. The extrinsic cardiac ganglia located in the thoracic cavity have connections to the lungs and esophagus and are indirectly connected via the spinal cord to many other organs such as the skin and arteries. The vagus nerve primarily consists of afferent fibers that connect to the medulla after passing through the nodose ganglion. Used with permission from the Institute of HeartMath, Boulder Creek, California. rhythms), synchronization among systems (eg, syn- information is encoded in the dynamic patterns of chronization between various electro-encephalogra- physiological activity. The afferent pathways from the phy [EEG] rhythms and the cardiac cycle), auto-coher- heart and blood vessels are given more relevance in ence (stability of a single waveform such as respiration this model due to the significant degree of afferent or HRV patterns), and system resonance. cardiovascular input to the brain and the consistent Interestingly, we have found that positive emo- generation of dynamic patterns generated by the heart. tions such as appreciation and compassion, as opposed It is our thesis that positive emotions in general, as to negative emotions such as anxiety, anger, and fear, well as self-induced positive emotions, shift the sys- are reflected in a heart rhythm pattern that is more tem as a whole into a more globally coherent and har- 4,5,103 coherent. The coherent state has been correlated monious physiological mode associated with with a general sense of wellbeing, and improvements improved system performance, ability to self-regulate, in cognitive, social, and physical performance. We and overall wellbeing. The psychophysiological coher- have observed this association between emotions and ence model predicts that different emotions are reflect- heart rhythm patterns in studies conducted in both ed in state-specific patterns in the heart’s rhythms laboratory and natural settings and for both spontane- independent of the amount of HRV or HR. Recent 52,102 ous and intentionally generated emotions. independent work has verified this by demonstrating We introduced the Heart Rhythm Coherence a 75% accuracy in detection of discrete emotional Hypothesis, which states that the pattern and stability states from the HRV signal using a neural network of beat-to-beat HR activity encodes information over approach for pattern recognition. Several studies in “macroscopic time scales” (ie, over many seconds to healthy subjects, which helped inform the model, minutes rather than only within a single cardiac cycle) show that during the experience of positive emotions, that can impact cognitive performance and emotional a sine wave–like pattern naturally emerges in the 4,8 experience. The coherence model takes a dynamic heart’s rhythms without any conscious changes in 52,103 systems approach that focuses on increasing individu- breathing. This is likely due to more organized als’ self-regulatory capacity through self-management outputs of the subcortical structures involved in pro- techniques that induce a physiological shift reflected cessing emotional information described by Pribram, 60 83 11 in the heart’s rhythms. We suggest that rhythmic Porges, Oppenheimer and Hopkins, and Thayer, activity in living systems reflects the regulation of in which the subcortical structures influence the oscil- interconnected biological, social, and environmental latory output of the cardiorespiratory control system networks and that important biologically relevant in the medulla oblongata. 56 Volume 4, Number 1 • January 2015 • www.gahmj.com Review hEART RATE VARIABILITY: NEw PERSPEcTIVES Heart rate Variability Coherence Increases Vagal opment of emotional experience and the social engage- afferent traffic ment system. As human beings, we are not limited to One of the properties of sensory neurons is that fight, flight, or freeze responses. We can self-regulate they are most responsive to increases in rate of change and initiate pro-social behaviors when we encounter in the function to which they are tuned to detect (eg, challenges, disagreements, or stressors. Porges sug- HR, BP). During periods of increased cardiac coher- gests that the healthy function of the social engage- ence, there is typically an increased range of variabili- ment system depends upon the proper functioning of ty in both BP and HR, which is detected as increases in the vagus nerves, which act as a “vagal brake,” and that the rate of change by the sensory neurons, resulting in measurements of vagal activity could serve as a mark- increased firing rates that increase vagal afferent traf- er for one’s ability to self-regulate. His theory also sug- fic. There is also a more ordered pattern of activity. A gests that the evolution and healthy function of the recent study using heartbeat-evoked potentials ANS determines the boundaries for the range of one’s showed that using paced breathing at a 10-second emotional expression, quality of communication, and rhythm increased both the range of HRV and the the ability to self-regulate emotions and behaviors. coherence in the rhythms as expected and also increased the N200 amplitude potential in the EEG self-regulation techniques that Increase Cardiac heartbeat–evoked potentials, which indicates Coherence increased afferent input. There is a paradigm shift occurring in the treat- Anatomical and stimulation studies have shown ment of diverse disorders like depression, epilepsy, that the thalamic pain pathways in the spinal cord are and pain by using vagal nerve stimulation, which 128-130 inhibited by increases in vagal afferent nerve traffic stimulates afferent neural pathways. New per- 105-107 over normal intrinsic levels. Several studies have spectives are emerging on behavioral intervention demonstrated that teaching patients self-regulation approaches that teach people self-regulation strategies techniques that increase HRV coherence is associated that include a physiological aspect such as HRV bio- with reduced pain and physical activity limita- feedback and that naturally increase vagal traffic. For 108,109 tions. In a study of patients with severe brain example, there are many studies showing that the injury, it was found that emotion–self-regulation train- practice of breathing at 6 breaths per minute, sup- ing resulted in significantly higher coherence ratios ported by HRV biofeedback, induces the coherence 111,131-136 and higher attention scores. Ratings of participants’ rhythm and has a wide range of benefits. emotional control correlated with improved HRV In addition to clinical applications, HRV coher- coherence measures. Regular practice of HRV bio- ence feedback training is often used to support self- feedback results in lasting improvements in baroreflex regulation skill acquisition in educational, corporate, gain, independent of cardiovascular and respiratory law enforcement, and military settings. Several sys- effects. This indicates neuroplasticity within the baro- tems that assess the degree of coherence in the user’s reflex system, likely within the intrinsic cardiac ner- heart rhythms are available. The majority of these vous system. Thus, repeated sessions of heart coher- systems—such as the emWavePro, or Inner Balance ence practice can reset the baroreflex system resulting for iOS devices (HeartMath, Inc, Boulder Creek, in increased afferent nerve activity noninvasively. California), Relaxing Rhythms (Wild Divine, Boulder City, Nevada), and the Stress Resilience Training resilience and self-regulatory Capacity System (Ease Interactive, San Diego, California)—use HRV also indicates psychological resiliency and a noninvasive earlobe or finger pulse sensor and dis- behavioral flexibility, reflecting an individual’s capac- play the user’s heart rhythm to provide feedback on ity to self-regulate and effectively adapt to changing their level of coherence. 27,112 social or environmental demands. A growing Emotional self-regulation strategies may contrib- number of studies have specifically linked vagally ute to improved health and performance. Alone or in 9,10,113 mediated HRV to self-regulatory capacity, emo- combination with HRV coherence biofeedback train- 114,115 7,116 tional regulation, social interactions, one’s ing, these strategies have been shown to increase resil- sense of coherence, the personality character traits ience and accelerate recovery from stressors or trau- 118 119 5,8,136,137 of self-directedness, and coping styles. ma. Self-induced positive emotions can initi- More recently, several studies have shown an ate a shift to increased cardiac coherence without any association between higher levels of vagally-mediated conscious intention to change the breathing 52,103 resting HRV and performance on cognitive perfor- rhythm. Typically, when people are able to self- mance tasks requiring the use of executive func- activate a positive or calming feeling rather than tions. HRV coherence can be increased in order to remaining focused on their breathing, they enjoy the 4,120-122 improve cognitive function as well as a wide shift in feeling and are able to sustain high levels of range of clinical outcomes that have been shown to coherence for much longer time periods. 5,51,123-127 reduce healthcare costs. Heart-focused self-regulation techniques and Porges suggests that the evolution of the ANS, assistive technologies that provide real-time HRV specifically the vagus nerves, was central to the devel- coherence feedback provide a systematic process for Review www.gahmj.com • January 2015 • Volume 4, Number 1 57 GLOBAL ADVANCES IN HEALTH AND MEDICINE self-regulating thoughts, emotions, and behaviors and tions in systolic and diastolic BP, total cholesterol, increasing physiological coherence. Many of these fasting glucose, overall stress, anger, fatigue and hostil- techniques (eg, Heart-Focused Breathing, Freeze ity. Similar results were obtained in several studies 139 138,142 Frame, Quick Coherence ) are designed to enable with police officers. people to intervene in the moment they start to experi- In addition to the emotional self-regulation tech- ence stress reactions or unproductive thoughts or niques, there are other approaches that also increase emotions. With practice, one is able to use one of the HRV coherence. For example, a study of Zen monks techniques to shift into a more coherent physiological found that monks with greater experience in medita- state before, during, and after challenging or adverse tion tended to have more coherent heart rhythms dur- situations, thus optimizing mental clarity, emotional ing their resting recording, while the ones who had composure, and stability. been monks for less than 2 years did not. A study of The first step in most of the techniques developed autogenic training also showed increased HRV coher- by the Institute of HeartMath is called Heart-Focused ence and found that cardiac coherence was strongly Breathing, which includes putting one’s attention in correlated with EEG alpha activity. The authors sug- the center of the chest (area of the heart) and imagin- gested that cardiac coherence could be a general mark- ing the breath is flowing in and out of the chest area er for the meditative state. However, this does not while breathing a little slower and deeper than usual. suggest that all meditation or prayer styles increase Conscious regulation of one’s respiration at a 10-sec- coherence, unless the coherence state is driven by a ond rhythm (0.1Hz) increases cardiac coherence and focus on breathing at a 10-second rhythm or the acti- 145-148 starts the process of shifting into a more coherent vation of a positive emotion. For example, a 4,124 state. With conscious control over breathing, an study examining HRV while reciting rosary or bead individual can slow the rate and increase the depth of prayers and yoga mantras found that a coherent the breathing rhythm. This takes advantage of physi- rhythm was produced by rhythmically breathing but ological mechanisms to modulate efferent vagal activ- not by random verbalization or breathing. The authors ity and thus the heart rhythm. This increases vagal ascribed the mechanisms for this finding to a breath- afferent nerve traffic and increases the coherence (sta- ing pattern of 6-cycles per minute. In a study of the bility) in the patterns of vagal afferent nerve traffic. In effects of five different types of prayer on HRV, it was turn, this influences the neural systems involved in found that all types of prayer elicited increased cardiac regulating sympathetic outflow, informing emotional coherence. However, prayers of gratefulness and heart- experience, and synchronizing neural structures felt love resulted in definitively higher coherence lev- 4 148 underlying cognitive processes. els. It has also been shown that tensing the large Several studies using various combinations of muscles in the legs in a rhythmical manner at a 10-sec- these self-regulation techniques have found signifi- ond rhythm can induce a coherent heart rhythm. cant correlations between HRV coherence and improvements in cognitive function and self-regulato- COnCLusIOn ry capacity. For example, a study of middle school HRV is an emergent property of interdependent students with attention deficit hyperactivity disorder regulatory systems that operate on different time showed a wide range of significant improvements in scales to adapt to environmental and psychological short and long-term memory, ability to focus, and sig- challenges. The physiological mechanisms that con- nificant improvements in behaviors both at home and tribute to HRV are complex and involve the neuraxis in school. A study of 41 fighter pilots engaging in that spans from the prefrontal and insular cortex to flight simulator tasks found a significant correlation the intrinsic cardiac nervous system, with the medulla between higher levels of performance and heart oblongata and intrinsic cardiac nervous system pro- rhythm coherence as well as lower levels of frustra- viding major neural integration centers. HRV can be tion. A study of recently returning soldiers from used as an index of the functional capacity of various Iraq who were diagnosed with PTSD, found that rela- regulatory systems and assessment of regulatory tively brief periods of HRV coherence training com- capacity may offer an alternative to autonomic bal- bined with practicing the Quick Coherence Technique ance models. Since the HRV LF band primarily reflects resulted in significant improvements in the ability to the vagally mediated transmission between the heart self-regulate along with a wide range of cognitive func- and medulla, resting measurements should not be tions. The degree of improvement correlated with used as markers of sympathetic activity. Based on increased cardiac coherence. Other studies have 24-hour monitoring, ULF and VLF rhythms are more shown increases in parasympathetic activity (vagal strongly associated with overall health status than HF tone), reductions in cortisol and increases in rhythms. New perspectives on mechanisms underly- DHEA, lowered BP and stress measures in hyperten- ing the VLF rhythm suggest that the primary source of 124,126 123 sive populations, reduced healthcare costs, this rhythm is within the heart itself. Recent findings and significant improvements in functional capacity demonstrate the importance of the intrinsic cardiac in patients with congestive heart failure. In addi- nervous system and cardiac afferents in generating the tion, a study of correctional officers showed reduc- heart rhythm and modulating the intervals between 58 Volume 4, Number 1 • January 2015 • www.gahmj.com Review hEART RATE VARIABILITY: NEw PERSPEcTIVES over nine decades. J Am Coll Cardiol. 1998;31(3):593-601. heartbeats. Vagally-mediated HRV appears to repre- 19. Dekker JM, Schouten EG, Klootwijk P, Pool J, Swenne CA, Kromhout D. sent an index of psychological self-regulatory control, Heart rate variability from short electrocardiographic recordings predicts such that individuals with greater resting HRV have mortality from all causes in middle-aged and elderly men. The Zutphen Study. Am J Epidemiol. 1997;145(10):899-908. performed better on tests of executive function. 20. Tsuji H, Venditti FJ Jr, Manders ES, et al. Reduced heart rate variability and In addition to assessing regulatory capacity, HRV mortality risk in an elderly cohort. The Framingham Heart Study. can also be used in the context of real-time feedback to Circulation. 1994;90(2):878-83. 21. Huikuri HV, Jokinen V, Syvänne M, et al. Heart rate variability and progres- help restore regulatory capacity. Heart rhythm coher- sion of coronary atherosclerosis. Arterioscler Thromb Vasc Biol. ence approaches train clients to produce auto-coher- 1999;19(8):1979-85. 22. Sajadieh A, Nielsen OW, Rasmussen V, Hein HO, Abedini S, Hansen JF. ent heart rhythms with a single peak in the LF region Increased heart rate and reduced heart-rate variability are associated with (typically around 0.1 Hz) with no significant peaks in subclinical inflammation in middle-aged and elderly subjects with no the VLF and HF regions. Emotional self-regulation apparent heart disease. Eur Heart J. 2004;25(5):363-70. 23. 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Heart Rate Variability: New Perspectives on Physiological Mechanisms, Assessment of Self-regulatory Capacity, and Health risk

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Heart Rate Variability: New Perspectives on Physiological Mechanisms, Assessment of Self-regulatory Capacity, and Health risk

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