Relationships between trait and respiratory parameters during quiet breathing in normal subjects

Relationships between trait and respiratory parameters during quiet breathing in normal subjects J Physiol Sci (2018) 68:369–376 https://doi.org/10.1007/s12576-017-0539-7 ORIGINAL PAPER Relationships between trait and respiratory parameters during quiet breathing in normal subjects 1 1 1 • • Akae Kato Koki Takahashi Ikuo Homma Received: 29 September 2016 / Accepted: 11 April 2017 / Published online: 2 May 2017 The Author(s) 2017. This article is an open access publication Abstract Respiratory patterns are influenced and altered Introduction by various emotional changes. In the present study, we investigated how respiratory patterns differ from individual It is well known that the main function of breathing is to to individual during quiet breathing. We examined the inhale oxygen and expire carbon dioxide for maintaining State-Trait Anxiety Inventory and various respiratory life. The breathing of this function is called metabolic parameters in 16 healthy male subjects. Tidal volume was breathing and is generated in the respiratory center located significantly larger and respiratory rate (RR) was signifi- in the brainstem, particularly in the medulla and pons. cantly higher in both the higher trait (HT) and higher state However, in addition to metabolic breathing, the so-called (HS) anxiety groups compared to the lower trait and lower behavioral breathing is generated in the upper center in the state anxiety groups. Inspiratory (T ) and expiratory time brain. Behavioral breathing is generated by various internal (T ) was significantly shorter in both the HT and HS or external environmental changes. A subtype of behav- anxiety groups. There was no significant difference in ioral breathing, which is influenced by various emotions, minute ventilation between these two groups. End-tidal has recently been investigated and has been termed, ‘‘emotional breathing’’ [1]. Therefore, autonomic breathing CO %, heart rate, and oxygen uptake (VO =W) also 2 2 output generated by the combination of tidal activity and showed no significant differences. V showed a negative respiratory rhythm is not only controlled by metabolic correlation and RR showed a positive correlation with trait demands but also controlled by constantly responding scores. T and T showed a negative correlation with trait I E changes of emotions, such as fear, anxiety, sadness, and anxiety scores. However, no other respiratory parameter happiness. It is interesting that maintenance of both showed any correlation. These results suggest that the homeostasis and emotions coexist in the breathing pattern. respiratory rhythm reflected by RR is affected by the The center for emotional breathing may be in the limbic activity generated in the higher center in accordance with system, especially in the amygdala, which is well known as the level of trait anxiety during quiet breathing in awake the primary center for emotions [2, 3]. It has been shown in humans. an animal experiment that spontaneous burst activities recorded in the amygdala are functionally coupled to Keywords STAI  Respiratory rate  Trait anxiety  Quiet medullary respiratory rhythm in the limbic-brainstem- breathing spinal cord preparation of a newborn rat. Electrical stim- ulation applied to the amygdala induces an inspiratory burst in the root of the phrenic nerve [4]. Spontaneous respiratory rhythmic activities are increased by the local & Ikuo Homma application of CRF (corticotrophin releasing factor) in the hommai@tau.ac.jp preparation [5]. CRF is well known to integrate the global mammalian stress response [6, 7]. The relationship of Department of Judo Therapy, Tokyo Ariake University of respiratory activity and emotion has been shown in a study Medical and Health Sciences, 2-9-1 Ariake Koto-ku, on anticipatory anxiety [8]; the subject’s respiratory rate Tokyo 135-0063, Japan 123 370 J Physiol Sci (2018) 68:369–376 increased during the feeling of anticipatory anxiety. In an quiet for 3 min, respiratory rate per minute (RR), minute earlier study, the changes in respiratory rate were found to _ ventilation (V ), tidal volume (V ), inspiratory time (T ), E T I be positively correlated with individual trait anxiety scores, expiratory time (T ), end-tidal CO % (FetCO ) and oxygen E 2 2 and the amygdala was examined to determine the source consumption per weight (VO =W) was measured breath by generating the activity using a neuroimaging method dur- breath for 5 min. All respiratory data with heart rate (HR) ing a time of anticipatory anxiety experienced by the were stored on a laptop computer. The room temperature subject [9]. was maintained at 22.5 ± 1 C. Concomitant changes in breathing patterns and emotions have been shown in studies of odor stimulation and in the Psychological measurements performance of Ikebana, the Japanese traditional art of flower arrangement. Unpleasant odor stimulation increased The anxiety level of each subject was accessed using the respiratory rate and state anxiety scores, whereas they Spielberger’s State-Trait Anxiety Inventory (STAI) [15]. were decreased by pleasant odor stimulation [10]. Subjects The instrument comprises two scales, one for measuring showed a decrease in the state anxiety score and respiratory Trait, and one for measuring State anxiety level. Each scale rate after performing Ikebana. The effects were more sig- has 20 statements and anxiety levels for subjects are indi- nificant in subjects with a high trait anxiety [11]. Several cated by scores rating from 20 to 80. The trait anxiety score previous studies have examined breathing patterns not only evaluates how people feel generally, while the state anxiety in normal subjects but also in subjects with anxiety disor- score evaluates how people feel ‘right now’ in various situ- ders and found that the breathing patterns were linked to ations. Trait score is generally stable, while state score psychosomatic complains [12, 13]. changes depending on the situation [15]. Trait scores of more A previous study of Masaoka and Homma (1997) than 44 indicate a high trait anxiety, and scores of less than 43 showed that mental stimulation decreases expiratory time reflect normal or low trait anxiety in men. State scores of and increases minute ventilation. They also found a nega- more than 41 indicate high state anxiety, and scores of less tive correlation between expiratory time and anxiety scores than 40 reflect normal or low trait anxiety in men. In this during the mental stimulation [14]. study, subjects were asked to assess their anxiety level using It is interesting to consider whether these two parame- STAI before the start of physiological measurements. ters, breathing pattern and anxiety scores, have a close Subjects were divided into two groups based on trait relationship and also whether that relationship is different anxiety according to Spielberger’s State-Trait Anxiety in different individuals during quiet breathing. The present Inventory (STAI): higher trait anxiety (HT) group and study measured and compared breathing patterns and trait lower trait anxiety (LT) group. Trait anxiety score of the anxiety scores during quiet breathing in normal young HT subjects was greater than 44 and the score in the LT adult males. subjects was less than 43. Subjects were also divided into two groups according to state anxiety: higher state anxiety (HS) group (more than 41) and lower state anxiety (LS) Methods group (less than 40). Subjects Data analysis Sixteen healthy male subjects aged from 19 to 23 years All statistical analyses were performed with commercially (20.8 ± 1.1 mean ± SD) participated in this study. No available statistical package (JMP Pro13.0.0; SAS Institute subjects had a psychiatric, neurological or pulmonary dis- order. All subjects provided written informed consent, and Inc., Cary, NC, USA). Comparisons of all respiratory parameters with HR between HT and LT groups and the study was approved by the Ethics Committee of Tokyo Ariake University of Medical and Health Sciences. between HS and LS were analyzed using unpaired t test and non-parametric unpaired Mann–Whitney test. As the Procedure and measurements results were similar, the latter results are presented. Continuous valuables of the trait and state anxiety Subjects sat on a chair wearing a facemask with a trans- scores, which were not normally distributed, are shown as median and interquartile ranges. A p value of \0.05 was ducer connected to a respiratory monitor (AE-100i, Minato considered statistically significant. Spearman’s nonpara- Medical Co., Ltd., Osaka) for measuring respiratory pattern metric correlation coefficients (q) were used to evaluate and metabolism in a quiet room. Heart rate was also whether the trait or state anxiety score was correlated with measured by a pulse oximeter (BSM-2401, NIHON KOHDEN Co., Ltd., Tokyo). After the subjects remained any of the various respiratory parameters. 123 J Physiol Sci (2018) 68:369–376 371 correlated with trait anxiety scores (Fig. 4a, c). There was Results no significant correlation between trait anxiety scores and STAI (Trait and State Anxiety) HR or VO =W (Fig. 5a, c). V and T were negatively 2 T E and RR was positively correlated with state anxiety scores Trait and state anxiety scores with the age of each subject _ (Table 2). Correlations between HR or VO =W and state is shown in Table 1. Trait anxiety scores varied from 31 to anxiety scores were also examined. Neither parameter 63 and the median score and interquartile range was 48.0 showed a significant correlation with state anxiety scores (35.0–54.8) (median, 25th–75th percentiles). State anxiety (Table 2). scores also varied from 31 to 65 and the median score was 38.5 (34.0–43.8). Scores of the trait and state anxiety score were relatively similar for each subject and a positive Comparisons of respiratory parameters, HR correlation was observed between trait and state anxiety _ and VO =W in HT, LT and HS, LS groups scores (p \ 0.01) (Fig. 1a). The median of the state scores was 44.0 (41.0–52.0) and 34.0 (33.0–36.0) in HT and LT, The median of FetCO (%) was 5.11 (5.01–5.39) in HT and respectively (Fig. 1b). The state scores were significantly 5.36 (5.22–5.42) in LT (Fig. 2d). There was no significant higher in HT subjects (p = 0.019). difference in FetCO (%) (p = 0.397). The mean of V was 2 E Relationships between respiratory parameters, HR and 9.3 (8.81–9.88) L/min in HT and 8.39 (7.41–9.32) L/min in VO =W with trait and state anxiety 2 _ LT (Fig. 2b). There was no significant difference in V The relationships between the various respiratory (p = 0.081). The median of V was 536.95 (493.78– _ _ parameters, FetCO , V , V , RR, T , T ,or VO =W and E 2 2 T I E 584.15) ml in HT and 699.15 (585.68–803.07) ml in LT STAI scores were examined. There was no significant subjects (Fig. 3b). The V was significantly larger in LT correlation between FetCO (%) and trait anxiety scores 2 subjects (p = 0.011). The median RR was 16.92 (Fig. 2c). There was no significant correlation between V E (16.25–18.75) n/min in HT and 12.06 (8.23–16.09) n/min in and trait anxiety scores (Fig. 2a). V is determined by the LT subjects (Fig. 3d). The RR was significantly higher in HT combination of RR and V . V was negatively and RR subjects (p = 0.005). The median of T and T were I E T T was positively correlated with trait anxiety scores 1.38 (1.29–1.59) and 2.15 (1.82–2.27) s in HT and 2.23 (1.59–3.02) and 2.71 (2.22-4.54) s in LT subjects, respec- (Fig. 3a, c). RR is based on inspiratory time (T ) and expiratory time (T ). T and T were also negatively tively (Fig. 4b, d). T and T were significantly shorter in HT E I E I E subjects (p = 0.008 for T and p = 0.015 for T ). The I E median of VO =W was 3.82 (3.41–4.16) ml/W in HT and Table 1 STAI scores with the age of each subject 3.61 (3.28–4.19) ml/W in LT subjects (Fig. 5b). There was Subject (No.) Age (year) STAI no significant difference in VO =W (p = 0.459). The med- Trait State ian of HR was 67.71 (60.00–83.75) beat/min in HT and 73.10 (62.77–78.54) beat/min in LT subjects (Fig. 5d). There was 120 63 65 also no significant difference in HR between the two groups 221 54 52 (p = 1.000). There were also no significant differences in 323 35 34 _ _ V , FetCO (%), VO =W and HR in higher state anxiety (HS) E 2 2 422 59 44 and lower state anxiety (LS) groups (Table 2). 520 55 43 621 51 41 721 32 34 Discussion 821 45 33 921 52 41 Trait and state anxiety scores were distributed from low to 10 20 60 34 high among subjects. Trait anxiety score is generally 11 20 41 31 unchangeable, but state anxiety score is changeable. As 12 23 35 34 state anxiety is measured according to how the subject feels 13 21 35 39 ‘right now’ in various situations, it is affected by various 14 20 53 49 environments and mental factors. On the other hand, trait 15 20 40 33 anxiety represents the subjective feeling in general [15]. 16 19 31 38 However, both anxiety scores were closely related and the 20.8 ± 1.1 48.0 (35.0–54.8) 38.5 (34.0–43.8) median state anxiety score of the HT group was signifi- Mean ± SD Median (25th–75th percentiles) cantly higher than that of the LT group in this study. A 123 372 J Physiol Sci (2018) 68:369–376 Fig. 1 The relationship between state and trait anxieties. a Linear in LT (*p \ 0.05). Median state anxiety in HT and LT were indicated plot of state and trait scores in normal subjects. A significant positive with horizontal bars. The vertical bars indicate the range and the correlation was observed (q = 0.580, p \ 0.01). b Comparison of horizontal boundaries of the boxes represent the first and third state scores in the high trait anxiety group (HT) and in the low trait quartiles anxiety group (LT). State scores were significantly higher in HT than Fig. 2 The relationships between minute ventilation (V ), end-tidal CO % (FetCO ), E 2 2 and trait anxiety. a Linear plot of V and trait scores. No significant correlation was observed (q = 0.384). b Comparison of V in HT and in LT. No significant difference was observed in V . c Linear plot of FetCO and trait scores. No significant correlation was observed (q =-0.038). d Comparison of FetCO in HT and in LT. No significant difference was observed in FetCO . Median V and FetCO 2 E 2 in HT and LT were indicated with horizontal bars. The vertical bars indicate the range and the horizontal boundaries of the boxes represent the first and third quartiles positive correlation was also obtained between trait and change. HR and VO =W are also changed by metabolic state anxiety scores. _ demands. There were no differences in V , HR and VO =W between the higher and lower trait anxiety groups Relationships between respiratory parameters (HT and LT) and between the higher state and lower state and STAI anxiety groups (HS and LS) (Figs. 2b, 5b, d; Table 2). There were also no significant correlations between these It is generally agreed that breathing patterns are generated parameters and trait or state anxiety scores. This indicates in the brainstem under metabolic demands. Minute venti- that parameters changing with metabolic demands are lation (V ) reflects the volume demand from the metabolic independent of trait or state anxiety. Contrary to the so- 123 J Physiol Sci (2018) 68:369–376 373 Fig. 3 The relationships between tidal volume (V ), respiratory rate (RR) and trait anxiety. a Linear plot of V and trait scores. A significant negative correlation was observed (q =-0.687, p \ 0.01). b Comparison of V in HT and in LT. V in LT was significantly larger than in HT (*p \ 0.05). c Linear plot of RR and trait scores. A significant positive correlation was observed in RR (q = 0.749, p \ 0.05). d Comparison of RR in HT and in LT. RR in HT was significantly higher than in LT (**p \ 0.01). Median V and RR in HT and LT were indicated with horizontal bars. The vertical bars indicate the range and the horizontal boundaries of the boxes represent the first and third quartiles Fig. 4 The relationship between inspiratory time (T ), expiratory time (T ), and trait anxiety. a Linear plot of T and trait scores. A significant negative correlation was observed in T (q =-0.622, p \ 0.05). b Comparison of T in HT and in LT. T in HT was significantly shorter than in LT (**p \ 0.01). c Linear plot of T and trait scores. A significant negative correlation was observed (q =-0.631, p \ 0.05). d Comparison of T in HT and in LT. T in HT was significantly shorter than in LT (*p \ 0.05). Median T and T I E in HT and LT were indicated with horizontal bars. The vertical bars indicate the range and the horizontal boundaries of the boxes represent the first and third quartiles 123 374 J Physiol Sci (2018) 68:369–376 Fig. 5 The relationship between oxygen uptake (VO =W), heart rate (HR), and trait anxiety. a Linear plot of VO =W and trait scores. No significant correlation was observed (q = 0.209). b Comparison of VO =W in HT and in LT. No significant difference was observed in VO =W. c Linear plots of HR and trait scores. No significant correlation was observed (q =-0.047). d Comparison of HR in HT and in LT. No significant difference was observed in HR. Median VO =W and HR in HT and LT were indicated with horizontal bars. The vertical bars indicate the range and the horizontal boundaries of the boxes represent the first and third quartiles called ‘‘metabolic breathing’’, we have so-called ‘‘behav- respiratory rate and the values of trait anxiety score ioral breathing’’ in which our breathing is influenced by (Fig. 3c). State anxiety showed significant correlations internal or external environmental changes. Autonomic with V , RR, and T . However, these correlation coeffi- T E breathing is not only controlled by metabolic breathing, but cients were smaller than those in trait anxiety. This indi- also responds to changes in emotions, such as anxiety, fear, cated that these respiratory parameters are more strongly and pleasantness. More rapid breathing, shown during an correlated with trait. arousal state and during various negative emotional chan- Anxiety and other emotions are primarily generated in ges, indicates the relationships between emotions and res- the amygdala [2, 3]. Previous studies, using functional piration [14, 16–18]. Masaoka and Homma (2001) showed, neuroimaging methods, have shown the neuroanatomical in a study of anticipatory anxiety, that respiratory rate correlates of negative emotions of fear and anxiety and increases during anticipatory anxiety and that the response have revealed that the amygdala plays a crucial role in the is not related to changes in metabolic demand [8]. They processing of these emotions. Recently, respiratory rhyth- also showed that increased respiratory rate during antici- mic neural activities were recorded from the piriform patory anxiety shows a linear positive correlation with trait cortex and amygdala using a limbic brainstem-spinal cord anxiety scores. It is well known that subjects with idio- preparation in newborn rats [4]. The activity was syn- pathic hyperventilation or panic disorder have high trait chronized with the burst activities recorded from the spinal anxiety and increase their ventilation, which induces sus- root for the phrenic nerve and was functionally coupled to tained arterial and alveolar hypocapnia [12, 19]. There was medullary respiratory rhythm. It is generally believed that no hyperventilation observed in the present healthy sub- basic respiratory rhythm is generated in the brainstem. The jects, even in those who had higher trait anxiety during respiratory central pattern generator (RCPG) has been quiet breathing. Irregular breathing, such as that described shown to be located in the brainstem [21]. A neuroimaging in subjects with anxiety or panic disorder [12, 20], was not study using fMRI in awake humans showed that the lim- apparent in these subjects. In the present study, we showed bic/paralimbic-bulbar circuitry plays a significant role in that the respiratory rate during quiet breathing is influenced emotional modulation of spontaneous breathing [22]. The by trait anxiety. Subjects who have a higher trait anxiety recent work study of Kim et al. (2013) showed that stim- showed a higher respiratory rate and those with a lower ulation of the bed nucleus of the stria terminals (BNST), trait anxiety showed a lower respiratory rate (Fig. 3d). We which is known to influence physiological manifestations also found a positive correlation between individual of anxiety, increases the respiratory rate in mice [23]. In 123 J Physiol Sci (2018) 68:369–376 375 Table 2 Correlation of A. Trait respiratory parameters with trail (A) and (B) Circulation Differences q P HT LT P _ 0.384 NS 9.3 (8.9–9.9) 8.4 (7.4–9.3) NS V (I) FetCO (%) -0.038 NS 5.1 (5.0–5.4) 5.4 (5.2–5.4) NS V (ml) -0.687 \0.01 537.0 (493.8–584.1) 699.2 (585.7–803.21) \0.05 RR (n/min) 0.749 \0.001 16.9 (6.3–18..8) 12.1 (8.2–16.1) \0.01 T (s) -0.622 \0.05 1.4 (1.3–1.6) 2.2 (1.6–3.0) \0.01 T (s) -0.631 \0.01 2.2 (1.8–2.3) 2.7 (2.2–4.5) \0.05 0.209 NS 3.8 (3.4–4.2) 3.6 (3.3–4.2) NS VO =W (ml/min/ kg) HR (beat/min) -0.047 NS 67.7 (60.0–83.8) 73.1 (62.8–78.5) NS B. State Circulation Differences q P HS LS P _ 0.349 NS 9.3 (8.6–9.7) 8.47 (7.6–9.7) NS V (I) FetCO (%) -0.319 NS 5.1 (5.0–5.4) 5.4 (7.6–9.7) NS V (ml) -0.558 \0.05 498.9 (490.1–572.1) 655.2 (587.3–777.1) \0.01 RR (n/min) 0.582 \0.05 17.2 (16.5–19.5) 15.0 (10.1–16.2) \0.01 T (s) -0.404 NS 1.4 (1.3–1.5) 1.7 (1.5–2.7) \0.05 T (s) -0.623 \0.01 2.1 (1.8–2.2) 2.6 (2.3–3.7) \0.01 0.212 NS 3.8 (3.6–4.3) 3.6 (3.2–4.1) NS VO =W (ml/min/kg) HR (beat/min) -0.245 NS 65.8 (58.8–76.6) 76.4 (65.2–83.3) NS Differences of respiratory parameters between high (HT) and low (LT) trail and high (HS) and low (LS) state Compliance with ethical standards humans, dipoles obtained during the anticipatory anxiety were synchronized with respiration and were found to be Conflict of Interest The authors declare that they have no conflict of located in the amygdala [9]. interests. Human and animal experiments on limbic and paral- imbic areas suggested that emotional impact is not only Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creative associated in neural activities in the brainstem, but also in commons.org/licenses/by/4.0/), which permits unrestricted use, distri- the limbic and paralimbic regions particularly in amygdala bution, and reproduction in any medium, provided you give appropriate in the limbic system [1]. credit to the original author(s) and the source, provide a link to the The strong close relationship between respiratory Creative Commons license, and indicate if changes were made. rhythm and trait anxiety was also shown here in the rela- tionship between inspiratory time (T ) and expiratory time References (T ). T may contribute to the determination of RR and E E indeed T has been shown to have no correlation with trait 1. Homma I, Masaoka Y (2008) Breathing rhythms and emotions. anxiety during mental stimulation even though T was Exp Physiol 93(9):1011–1021 correlated with trait anxiety [14]. However, in this study 2. Adolph R, Tranel D, Damasio H, Damasio AR (1994) Impaired significant correlations between T or T and trait anxiety E I recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature 72:669–672 were shown with a correlation between RR and trait anx- 3. Morris J, Friston KJ, Buechel C, Frith CD, Young AW, Calder iety during quiet breathing. The respiratory rate, indepen- AJ, Dolan RJ (1998) A neuromodulatory role for the human dent of metabolic breathing demands, may be affected by amygdala in processing emotional facial expressions. Brain trait anxiety during quiet breathing in humans. 121:47–57 4. Onimaru H, Homma I (2007) Spontaneous oscillatory burst These basic research data obtained from normal subjects activity in the piriform-amygdala region and its relation to would be useful for explication of the clinical condition of in vitro respiratory activity in newborn rats. Neurosci the hyperventilation syndrome and anxiety disorders. 144:387–394 123 376 J Physiol Sci (2018) 68:369–376 5. Fujii T, Onimaru H, Homma I (2011) Effects of corticotrophin 15. Spielberger CD (1983) Manual for the State-Trait Anxiety releasing factor on spontaneous burst activity in the piriform- Inventory. Consulting Psychologists, Palo Alto amygdala complex of in vitro brain preparations from new-born 16. Nyklicek I, Thayer JF, Van Doorner LJP (1997) Cardiorespira- rats. Neurosci Res 71:134–139 tory differentiation of musically-induced emotions. J Psy- 6. Owens MJ, Nemeroff CB (1991) Physiology and pharmacology chophysiol 11:304–321 of corticotropin-releasing factor. Pharmacol Rev 43(4):425–473 17. Boiten FA (1998) The effects of emotional behavior on compo- 7. Skelton KH, Nemeroff CB, Knight DL, Owens MJ (2000) nents of the respiratory cycle. Biol Psychol 49:29–51 Chronic administration of the triazolobenzodiazepine alprazolam 18. Gomez P, Danuser B (2004) Affective and physiological produces opposite effects on corticotrophin-releasing factor and responses to environmental noise and music. Int J Psychophysiol urocortin neuronal systems. J Neurosci 20(3):1240–1248 53:91–103 8. Masaoka Y, Homma I (2001) The effect of anticipatory anxiety 19. Masaoka Y, Jack S, Warburton C, Homma I (2004) Breathing on breathing and metabolism in humans. Respir Physiol patterns associated with trait anxiety and breathlessness in 128:171–177 humans. Jpn J Physiol 54:465–470 9. Masaoka Y, Homma I (2000) The source generator of respira- 20. Yeragani VK, Radhakrishna RK, Tancer M, Uhde T (2002) tory-related anxiety potential in the human brain. Neurosci Lett Nonlinear measures of respiration:respiratory irregularity and 283:21–24 increased chaos of respiration in patients with panic disorder. 10. Masaoka Y, Koiwa N, Homma I (2005) Inspiratory phase-locked Neuropsychobiology 46(3):111–120 alpha oscillation in human olfaction: source generators estimated 21. Smith JC, Abdala AP, Koizumi H, Rybak IA, Paton JF (2007) by a dipole tracing method. J Physiol 566:979–997 Spatial and functional architecture of the mammalian brain stem 11. Homma I, Oizumi R, Masaoka Y (2015) Effects of practicing respiratory network: a hierarchy of three oscillatory mechanisms. Ikebana on anxiety and respiration. J Depression Anxiety J Neurophysiol 98:3370–3387 4(3):187 22. Evans KC, Dougherty DD, Xchmid AM, Scannell E, McCallister 12. Han JN, Stegen K, Schepers R, Van Den Bergh O, Van De A, Benson H, Dusek JA, Lazar SW (2009) Modulation of spon- Woestijne KP (1998) Subjective symptoms and breathing pattern taneous breathing via limbic/paralimbic-bulbar circuitry: an event at rest and following hyperventilation in anxiety and somatoform related fMRI study. Neuroimage 47(3):961–971 disorders. J Psychosomatic Res 45(6):519–532 23. Kim SY, Adhikari A, Lee SY, Marshel JH, Kim CK, Mallory CS, 13. Han JN, Schepers R, Stegen K, Van den Bergh O, Van de Lo M, Pak S, Mattis J, Lim BK, Malenka RC, Warden MR, Neve Woestijne KP (2000) Psychosomatic symptoms and breathing R, Tye KM (2013) Diverging neural pathways assemble a pattern. J Psychosomatic Res 49:319–333 behavioral state from separable features in anxiety. Nature 14. Masaoka Y, Homma I (1997) Anxiety and respiratory pattern: 496:219–223 their relationship during mental stress and physical load. Int J Psychophysiol 27:153–159 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png The Journal of Physiological Sciences Springer Journals

Relationships between trait and respiratory parameters during quiet breathing in normal subjects

Free
8 pages
Loading next page...
 
/lp/springer_journal/relationships-between-trait-and-respiratory-parameters-during-quiet-x2bxinml06
Publisher
Springer Japan
Copyright
Copyright © 2017 by The Author(s)
Subject
Biomedicine; Human Physiology; Neurosciences; Animal Biochemistry; Animal Physiology; Cell Physiology; Neurobiology
ISSN
1880-6546
eISSN
1880-6562
D.O.I.
10.1007/s12576-017-0539-7
Publisher site
See Article on Publisher Site

Abstract

J Physiol Sci (2018) 68:369–376 https://doi.org/10.1007/s12576-017-0539-7 ORIGINAL PAPER Relationships between trait and respiratory parameters during quiet breathing in normal subjects 1 1 1 • • Akae Kato Koki Takahashi Ikuo Homma Received: 29 September 2016 / Accepted: 11 April 2017 / Published online: 2 May 2017 The Author(s) 2017. This article is an open access publication Abstract Respiratory patterns are influenced and altered Introduction by various emotional changes. In the present study, we investigated how respiratory patterns differ from individual It is well known that the main function of breathing is to to individual during quiet breathing. We examined the inhale oxygen and expire carbon dioxide for maintaining State-Trait Anxiety Inventory and various respiratory life. The breathing of this function is called metabolic parameters in 16 healthy male subjects. Tidal volume was breathing and is generated in the respiratory center located significantly larger and respiratory rate (RR) was signifi- in the brainstem, particularly in the medulla and pons. cantly higher in both the higher trait (HT) and higher state However, in addition to metabolic breathing, the so-called (HS) anxiety groups compared to the lower trait and lower behavioral breathing is generated in the upper center in the state anxiety groups. Inspiratory (T ) and expiratory time brain. Behavioral breathing is generated by various internal (T ) was significantly shorter in both the HT and HS or external environmental changes. A subtype of behav- anxiety groups. There was no significant difference in ioral breathing, which is influenced by various emotions, minute ventilation between these two groups. End-tidal has recently been investigated and has been termed, ‘‘emotional breathing’’ [1]. Therefore, autonomic breathing CO %, heart rate, and oxygen uptake (VO =W) also 2 2 output generated by the combination of tidal activity and showed no significant differences. V showed a negative respiratory rhythm is not only controlled by metabolic correlation and RR showed a positive correlation with trait demands but also controlled by constantly responding scores. T and T showed a negative correlation with trait I E changes of emotions, such as fear, anxiety, sadness, and anxiety scores. However, no other respiratory parameter happiness. It is interesting that maintenance of both showed any correlation. These results suggest that the homeostasis and emotions coexist in the breathing pattern. respiratory rhythm reflected by RR is affected by the The center for emotional breathing may be in the limbic activity generated in the higher center in accordance with system, especially in the amygdala, which is well known as the level of trait anxiety during quiet breathing in awake the primary center for emotions [2, 3]. It has been shown in humans. an animal experiment that spontaneous burst activities recorded in the amygdala are functionally coupled to Keywords STAI  Respiratory rate  Trait anxiety  Quiet medullary respiratory rhythm in the limbic-brainstem- breathing spinal cord preparation of a newborn rat. Electrical stim- ulation applied to the amygdala induces an inspiratory burst in the root of the phrenic nerve [4]. Spontaneous respiratory rhythmic activities are increased by the local & Ikuo Homma application of CRF (corticotrophin releasing factor) in the hommai@tau.ac.jp preparation [5]. CRF is well known to integrate the global mammalian stress response [6, 7]. The relationship of Department of Judo Therapy, Tokyo Ariake University of respiratory activity and emotion has been shown in a study Medical and Health Sciences, 2-9-1 Ariake Koto-ku, on anticipatory anxiety [8]; the subject’s respiratory rate Tokyo 135-0063, Japan 123 370 J Physiol Sci (2018) 68:369–376 increased during the feeling of anticipatory anxiety. In an quiet for 3 min, respiratory rate per minute (RR), minute earlier study, the changes in respiratory rate were found to _ ventilation (V ), tidal volume (V ), inspiratory time (T ), E T I be positively correlated with individual trait anxiety scores, expiratory time (T ), end-tidal CO % (FetCO ) and oxygen E 2 2 and the amygdala was examined to determine the source consumption per weight (VO =W) was measured breath by generating the activity using a neuroimaging method dur- breath for 5 min. All respiratory data with heart rate (HR) ing a time of anticipatory anxiety experienced by the were stored on a laptop computer. The room temperature subject [9]. was maintained at 22.5 ± 1 C. Concomitant changes in breathing patterns and emotions have been shown in studies of odor stimulation and in the Psychological measurements performance of Ikebana, the Japanese traditional art of flower arrangement. Unpleasant odor stimulation increased The anxiety level of each subject was accessed using the respiratory rate and state anxiety scores, whereas they Spielberger’s State-Trait Anxiety Inventory (STAI) [15]. were decreased by pleasant odor stimulation [10]. Subjects The instrument comprises two scales, one for measuring showed a decrease in the state anxiety score and respiratory Trait, and one for measuring State anxiety level. Each scale rate after performing Ikebana. The effects were more sig- has 20 statements and anxiety levels for subjects are indi- nificant in subjects with a high trait anxiety [11]. Several cated by scores rating from 20 to 80. The trait anxiety score previous studies have examined breathing patterns not only evaluates how people feel generally, while the state anxiety in normal subjects but also in subjects with anxiety disor- score evaluates how people feel ‘right now’ in various situ- ders and found that the breathing patterns were linked to ations. Trait score is generally stable, while state score psychosomatic complains [12, 13]. changes depending on the situation [15]. Trait scores of more A previous study of Masaoka and Homma (1997) than 44 indicate a high trait anxiety, and scores of less than 43 showed that mental stimulation decreases expiratory time reflect normal or low trait anxiety in men. State scores of and increases minute ventilation. They also found a nega- more than 41 indicate high state anxiety, and scores of less tive correlation between expiratory time and anxiety scores than 40 reflect normal or low trait anxiety in men. In this during the mental stimulation [14]. study, subjects were asked to assess their anxiety level using It is interesting to consider whether these two parame- STAI before the start of physiological measurements. ters, breathing pattern and anxiety scores, have a close Subjects were divided into two groups based on trait relationship and also whether that relationship is different anxiety according to Spielberger’s State-Trait Anxiety in different individuals during quiet breathing. The present Inventory (STAI): higher trait anxiety (HT) group and study measured and compared breathing patterns and trait lower trait anxiety (LT) group. Trait anxiety score of the anxiety scores during quiet breathing in normal young HT subjects was greater than 44 and the score in the LT adult males. subjects was less than 43. Subjects were also divided into two groups according to state anxiety: higher state anxiety (HS) group (more than 41) and lower state anxiety (LS) Methods group (less than 40). Subjects Data analysis Sixteen healthy male subjects aged from 19 to 23 years All statistical analyses were performed with commercially (20.8 ± 1.1 mean ± SD) participated in this study. No available statistical package (JMP Pro13.0.0; SAS Institute subjects had a psychiatric, neurological or pulmonary dis- order. All subjects provided written informed consent, and Inc., Cary, NC, USA). Comparisons of all respiratory parameters with HR between HT and LT groups and the study was approved by the Ethics Committee of Tokyo Ariake University of Medical and Health Sciences. between HS and LS were analyzed using unpaired t test and non-parametric unpaired Mann–Whitney test. As the Procedure and measurements results were similar, the latter results are presented. Continuous valuables of the trait and state anxiety Subjects sat on a chair wearing a facemask with a trans- scores, which were not normally distributed, are shown as median and interquartile ranges. A p value of \0.05 was ducer connected to a respiratory monitor (AE-100i, Minato considered statistically significant. Spearman’s nonpara- Medical Co., Ltd., Osaka) for measuring respiratory pattern metric correlation coefficients (q) were used to evaluate and metabolism in a quiet room. Heart rate was also whether the trait or state anxiety score was correlated with measured by a pulse oximeter (BSM-2401, NIHON KOHDEN Co., Ltd., Tokyo). After the subjects remained any of the various respiratory parameters. 123 J Physiol Sci (2018) 68:369–376 371 correlated with trait anxiety scores (Fig. 4a, c). There was Results no significant correlation between trait anxiety scores and STAI (Trait and State Anxiety) HR or VO =W (Fig. 5a, c). V and T were negatively 2 T E and RR was positively correlated with state anxiety scores Trait and state anxiety scores with the age of each subject _ (Table 2). Correlations between HR or VO =W and state is shown in Table 1. Trait anxiety scores varied from 31 to anxiety scores were also examined. Neither parameter 63 and the median score and interquartile range was 48.0 showed a significant correlation with state anxiety scores (35.0–54.8) (median, 25th–75th percentiles). State anxiety (Table 2). scores also varied from 31 to 65 and the median score was 38.5 (34.0–43.8). Scores of the trait and state anxiety score were relatively similar for each subject and a positive Comparisons of respiratory parameters, HR correlation was observed between trait and state anxiety _ and VO =W in HT, LT and HS, LS groups scores (p \ 0.01) (Fig. 1a). The median of the state scores was 44.0 (41.0–52.0) and 34.0 (33.0–36.0) in HT and LT, The median of FetCO (%) was 5.11 (5.01–5.39) in HT and respectively (Fig. 1b). The state scores were significantly 5.36 (5.22–5.42) in LT (Fig. 2d). There was no significant higher in HT subjects (p = 0.019). difference in FetCO (%) (p = 0.397). The mean of V was 2 E Relationships between respiratory parameters, HR and 9.3 (8.81–9.88) L/min in HT and 8.39 (7.41–9.32) L/min in VO =W with trait and state anxiety 2 _ LT (Fig. 2b). There was no significant difference in V The relationships between the various respiratory (p = 0.081). The median of V was 536.95 (493.78– _ _ parameters, FetCO , V , V , RR, T , T ,or VO =W and E 2 2 T I E 584.15) ml in HT and 699.15 (585.68–803.07) ml in LT STAI scores were examined. There was no significant subjects (Fig. 3b). The V was significantly larger in LT correlation between FetCO (%) and trait anxiety scores 2 subjects (p = 0.011). The median RR was 16.92 (Fig. 2c). There was no significant correlation between V E (16.25–18.75) n/min in HT and 12.06 (8.23–16.09) n/min in and trait anxiety scores (Fig. 2a). V is determined by the LT subjects (Fig. 3d). The RR was significantly higher in HT combination of RR and V . V was negatively and RR subjects (p = 0.005). The median of T and T were I E T T was positively correlated with trait anxiety scores 1.38 (1.29–1.59) and 2.15 (1.82–2.27) s in HT and 2.23 (1.59–3.02) and 2.71 (2.22-4.54) s in LT subjects, respec- (Fig. 3a, c). RR is based on inspiratory time (T ) and expiratory time (T ). T and T were also negatively tively (Fig. 4b, d). T and T were significantly shorter in HT E I E I E subjects (p = 0.008 for T and p = 0.015 for T ). The I E median of VO =W was 3.82 (3.41–4.16) ml/W in HT and Table 1 STAI scores with the age of each subject 3.61 (3.28–4.19) ml/W in LT subjects (Fig. 5b). There was Subject (No.) Age (year) STAI no significant difference in VO =W (p = 0.459). The med- Trait State ian of HR was 67.71 (60.00–83.75) beat/min in HT and 73.10 (62.77–78.54) beat/min in LT subjects (Fig. 5d). There was 120 63 65 also no significant difference in HR between the two groups 221 54 52 (p = 1.000). There were also no significant differences in 323 35 34 _ _ V , FetCO (%), VO =W and HR in higher state anxiety (HS) E 2 2 422 59 44 and lower state anxiety (LS) groups (Table 2). 520 55 43 621 51 41 721 32 34 Discussion 821 45 33 921 52 41 Trait and state anxiety scores were distributed from low to 10 20 60 34 high among subjects. Trait anxiety score is generally 11 20 41 31 unchangeable, but state anxiety score is changeable. As 12 23 35 34 state anxiety is measured according to how the subject feels 13 21 35 39 ‘right now’ in various situations, it is affected by various 14 20 53 49 environments and mental factors. On the other hand, trait 15 20 40 33 anxiety represents the subjective feeling in general [15]. 16 19 31 38 However, both anxiety scores were closely related and the 20.8 ± 1.1 48.0 (35.0–54.8) 38.5 (34.0–43.8) median state anxiety score of the HT group was signifi- Mean ± SD Median (25th–75th percentiles) cantly higher than that of the LT group in this study. A 123 372 J Physiol Sci (2018) 68:369–376 Fig. 1 The relationship between state and trait anxieties. a Linear in LT (*p \ 0.05). Median state anxiety in HT and LT were indicated plot of state and trait scores in normal subjects. A significant positive with horizontal bars. The vertical bars indicate the range and the correlation was observed (q = 0.580, p \ 0.01). b Comparison of horizontal boundaries of the boxes represent the first and third state scores in the high trait anxiety group (HT) and in the low trait quartiles anxiety group (LT). State scores were significantly higher in HT than Fig. 2 The relationships between minute ventilation (V ), end-tidal CO % (FetCO ), E 2 2 and trait anxiety. a Linear plot of V and trait scores. No significant correlation was observed (q = 0.384). b Comparison of V in HT and in LT. No significant difference was observed in V . c Linear plot of FetCO and trait scores. No significant correlation was observed (q =-0.038). d Comparison of FetCO in HT and in LT. No significant difference was observed in FetCO . Median V and FetCO 2 E 2 in HT and LT were indicated with horizontal bars. The vertical bars indicate the range and the horizontal boundaries of the boxes represent the first and third quartiles positive correlation was also obtained between trait and change. HR and VO =W are also changed by metabolic state anxiety scores. _ demands. There were no differences in V , HR and VO =W between the higher and lower trait anxiety groups Relationships between respiratory parameters (HT and LT) and between the higher state and lower state and STAI anxiety groups (HS and LS) (Figs. 2b, 5b, d; Table 2). There were also no significant correlations between these It is generally agreed that breathing patterns are generated parameters and trait or state anxiety scores. This indicates in the brainstem under metabolic demands. Minute venti- that parameters changing with metabolic demands are lation (V ) reflects the volume demand from the metabolic independent of trait or state anxiety. Contrary to the so- 123 J Physiol Sci (2018) 68:369–376 373 Fig. 3 The relationships between tidal volume (V ), respiratory rate (RR) and trait anxiety. a Linear plot of V and trait scores. A significant negative correlation was observed (q =-0.687, p \ 0.01). b Comparison of V in HT and in LT. V in LT was significantly larger than in HT (*p \ 0.05). c Linear plot of RR and trait scores. A significant positive correlation was observed in RR (q = 0.749, p \ 0.05). d Comparison of RR in HT and in LT. RR in HT was significantly higher than in LT (**p \ 0.01). Median V and RR in HT and LT were indicated with horizontal bars. The vertical bars indicate the range and the horizontal boundaries of the boxes represent the first and third quartiles Fig. 4 The relationship between inspiratory time (T ), expiratory time (T ), and trait anxiety. a Linear plot of T and trait scores. A significant negative correlation was observed in T (q =-0.622, p \ 0.05). b Comparison of T in HT and in LT. T in HT was significantly shorter than in LT (**p \ 0.01). c Linear plot of T and trait scores. A significant negative correlation was observed (q =-0.631, p \ 0.05). d Comparison of T in HT and in LT. T in HT was significantly shorter than in LT (*p \ 0.05). Median T and T I E in HT and LT were indicated with horizontal bars. The vertical bars indicate the range and the horizontal boundaries of the boxes represent the first and third quartiles 123 374 J Physiol Sci (2018) 68:369–376 Fig. 5 The relationship between oxygen uptake (VO =W), heart rate (HR), and trait anxiety. a Linear plot of VO =W and trait scores. No significant correlation was observed (q = 0.209). b Comparison of VO =W in HT and in LT. No significant difference was observed in VO =W. c Linear plots of HR and trait scores. No significant correlation was observed (q =-0.047). d Comparison of HR in HT and in LT. No significant difference was observed in HR. Median VO =W and HR in HT and LT were indicated with horizontal bars. The vertical bars indicate the range and the horizontal boundaries of the boxes represent the first and third quartiles called ‘‘metabolic breathing’’, we have so-called ‘‘behav- respiratory rate and the values of trait anxiety score ioral breathing’’ in which our breathing is influenced by (Fig. 3c). State anxiety showed significant correlations internal or external environmental changes. Autonomic with V , RR, and T . However, these correlation coeffi- T E breathing is not only controlled by metabolic breathing, but cients were smaller than those in trait anxiety. This indi- also responds to changes in emotions, such as anxiety, fear, cated that these respiratory parameters are more strongly and pleasantness. More rapid breathing, shown during an correlated with trait. arousal state and during various negative emotional chan- Anxiety and other emotions are primarily generated in ges, indicates the relationships between emotions and res- the amygdala [2, 3]. Previous studies, using functional piration [14, 16–18]. Masaoka and Homma (2001) showed, neuroimaging methods, have shown the neuroanatomical in a study of anticipatory anxiety, that respiratory rate correlates of negative emotions of fear and anxiety and increases during anticipatory anxiety and that the response have revealed that the amygdala plays a crucial role in the is not related to changes in metabolic demand [8]. They processing of these emotions. Recently, respiratory rhyth- also showed that increased respiratory rate during antici- mic neural activities were recorded from the piriform patory anxiety shows a linear positive correlation with trait cortex and amygdala using a limbic brainstem-spinal cord anxiety scores. It is well known that subjects with idio- preparation in newborn rats [4]. The activity was syn- pathic hyperventilation or panic disorder have high trait chronized with the burst activities recorded from the spinal anxiety and increase their ventilation, which induces sus- root for the phrenic nerve and was functionally coupled to tained arterial and alveolar hypocapnia [12, 19]. There was medullary respiratory rhythm. It is generally believed that no hyperventilation observed in the present healthy sub- basic respiratory rhythm is generated in the brainstem. The jects, even in those who had higher trait anxiety during respiratory central pattern generator (RCPG) has been quiet breathing. Irregular breathing, such as that described shown to be located in the brainstem [21]. A neuroimaging in subjects with anxiety or panic disorder [12, 20], was not study using fMRI in awake humans showed that the lim- apparent in these subjects. In the present study, we showed bic/paralimbic-bulbar circuitry plays a significant role in that the respiratory rate during quiet breathing is influenced emotional modulation of spontaneous breathing [22]. The by trait anxiety. Subjects who have a higher trait anxiety recent work study of Kim et al. (2013) showed that stim- showed a higher respiratory rate and those with a lower ulation of the bed nucleus of the stria terminals (BNST), trait anxiety showed a lower respiratory rate (Fig. 3d). We which is known to influence physiological manifestations also found a positive correlation between individual of anxiety, increases the respiratory rate in mice [23]. In 123 J Physiol Sci (2018) 68:369–376 375 Table 2 Correlation of A. Trait respiratory parameters with trail (A) and (B) Circulation Differences q P HT LT P _ 0.384 NS 9.3 (8.9–9.9) 8.4 (7.4–9.3) NS V (I) FetCO (%) -0.038 NS 5.1 (5.0–5.4) 5.4 (5.2–5.4) NS V (ml) -0.687 \0.01 537.0 (493.8–584.1) 699.2 (585.7–803.21) \0.05 RR (n/min) 0.749 \0.001 16.9 (6.3–18..8) 12.1 (8.2–16.1) \0.01 T (s) -0.622 \0.05 1.4 (1.3–1.6) 2.2 (1.6–3.0) \0.01 T (s) -0.631 \0.01 2.2 (1.8–2.3) 2.7 (2.2–4.5) \0.05 0.209 NS 3.8 (3.4–4.2) 3.6 (3.3–4.2) NS VO =W (ml/min/ kg) HR (beat/min) -0.047 NS 67.7 (60.0–83.8) 73.1 (62.8–78.5) NS B. State Circulation Differences q P HS LS P _ 0.349 NS 9.3 (8.6–9.7) 8.47 (7.6–9.7) NS V (I) FetCO (%) -0.319 NS 5.1 (5.0–5.4) 5.4 (7.6–9.7) NS V (ml) -0.558 \0.05 498.9 (490.1–572.1) 655.2 (587.3–777.1) \0.01 RR (n/min) 0.582 \0.05 17.2 (16.5–19.5) 15.0 (10.1–16.2) \0.01 T (s) -0.404 NS 1.4 (1.3–1.5) 1.7 (1.5–2.7) \0.05 T (s) -0.623 \0.01 2.1 (1.8–2.2) 2.6 (2.3–3.7) \0.01 0.212 NS 3.8 (3.6–4.3) 3.6 (3.2–4.1) NS VO =W (ml/min/kg) HR (beat/min) -0.245 NS 65.8 (58.8–76.6) 76.4 (65.2–83.3) NS Differences of respiratory parameters between high (HT) and low (LT) trail and high (HS) and low (LS) state Compliance with ethical standards humans, dipoles obtained during the anticipatory anxiety were synchronized with respiration and were found to be Conflict of Interest The authors declare that they have no conflict of located in the amygdala [9]. interests. Human and animal experiments on limbic and paral- imbic areas suggested that emotional impact is not only Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creative associated in neural activities in the brainstem, but also in commons.org/licenses/by/4.0/), which permits unrestricted use, distri- the limbic and paralimbic regions particularly in amygdala bution, and reproduction in any medium, provided you give appropriate in the limbic system [1]. credit to the original author(s) and the source, provide a link to the The strong close relationship between respiratory Creative Commons license, and indicate if changes were made. rhythm and trait anxiety was also shown here in the rela- tionship between inspiratory time (T ) and expiratory time References (T ). T may contribute to the determination of RR and E E indeed T has been shown to have no correlation with trait 1. Homma I, Masaoka Y (2008) Breathing rhythms and emotions. anxiety during mental stimulation even though T was Exp Physiol 93(9):1011–1021 correlated with trait anxiety [14]. However, in this study 2. Adolph R, Tranel D, Damasio H, Damasio AR (1994) Impaired significant correlations between T or T and trait anxiety E I recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature 72:669–672 were shown with a correlation between RR and trait anx- 3. Morris J, Friston KJ, Buechel C, Frith CD, Young AW, Calder iety during quiet breathing. The respiratory rate, indepen- AJ, Dolan RJ (1998) A neuromodulatory role for the human dent of metabolic breathing demands, may be affected by amygdala in processing emotional facial expressions. Brain trait anxiety during quiet breathing in humans. 121:47–57 4. Onimaru H, Homma I (2007) Spontaneous oscillatory burst These basic research data obtained from normal subjects activity in the piriform-amygdala region and its relation to would be useful for explication of the clinical condition of in vitro respiratory activity in newborn rats. Neurosci the hyperventilation syndrome and anxiety disorders. 144:387–394 123 376 J Physiol Sci (2018) 68:369–376 5. Fujii T, Onimaru H, Homma I (2011) Effects of corticotrophin 15. Spielberger CD (1983) Manual for the State-Trait Anxiety releasing factor on spontaneous burst activity in the piriform- Inventory. Consulting Psychologists, Palo Alto amygdala complex of in vitro brain preparations from new-born 16. Nyklicek I, Thayer JF, Van Doorner LJP (1997) Cardiorespira- rats. Neurosci Res 71:134–139 tory differentiation of musically-induced emotions. J Psy- 6. Owens MJ, Nemeroff CB (1991) Physiology and pharmacology chophysiol 11:304–321 of corticotropin-releasing factor. Pharmacol Rev 43(4):425–473 17. Boiten FA (1998) The effects of emotional behavior on compo- 7. Skelton KH, Nemeroff CB, Knight DL, Owens MJ (2000) nents of the respiratory cycle. Biol Psychol 49:29–51 Chronic administration of the triazolobenzodiazepine alprazolam 18. Gomez P, Danuser B (2004) Affective and physiological produces opposite effects on corticotrophin-releasing factor and responses to environmental noise and music. Int J Psychophysiol urocortin neuronal systems. J Neurosci 20(3):1240–1248 53:91–103 8. Masaoka Y, Homma I (2001) The effect of anticipatory anxiety 19. Masaoka Y, Jack S, Warburton C, Homma I (2004) Breathing on breathing and metabolism in humans. Respir Physiol patterns associated with trait anxiety and breathlessness in 128:171–177 humans. Jpn J Physiol 54:465–470 9. Masaoka Y, Homma I (2000) The source generator of respira- 20. Yeragani VK, Radhakrishna RK, Tancer M, Uhde T (2002) tory-related anxiety potential in the human brain. Neurosci Lett Nonlinear measures of respiration:respiratory irregularity and 283:21–24 increased chaos of respiration in patients with panic disorder. 10. Masaoka Y, Koiwa N, Homma I (2005) Inspiratory phase-locked Neuropsychobiology 46(3):111–120 alpha oscillation in human olfaction: source generators estimated 21. Smith JC, Abdala AP, Koizumi H, Rybak IA, Paton JF (2007) by a dipole tracing method. J Physiol 566:979–997 Spatial and functional architecture of the mammalian brain stem 11. Homma I, Oizumi R, Masaoka Y (2015) Effects of practicing respiratory network: a hierarchy of three oscillatory mechanisms. Ikebana on anxiety and respiration. J Depression Anxiety J Neurophysiol 98:3370–3387 4(3):187 22. Evans KC, Dougherty DD, Xchmid AM, Scannell E, McCallister 12. Han JN, Stegen K, Schepers R, Van Den Bergh O, Van De A, Benson H, Dusek JA, Lazar SW (2009) Modulation of spon- Woestijne KP (1998) Subjective symptoms and breathing pattern taneous breathing via limbic/paralimbic-bulbar circuitry: an event at rest and following hyperventilation in anxiety and somatoform related fMRI study. Neuroimage 47(3):961–971 disorders. J Psychosomatic Res 45(6):519–532 23. Kim SY, Adhikari A, Lee SY, Marshel JH, Kim CK, Mallory CS, 13. Han JN, Schepers R, Stegen K, Van den Bergh O, Van de Lo M, Pak S, Mattis J, Lim BK, Malenka RC, Warden MR, Neve Woestijne KP (2000) Psychosomatic symptoms and breathing R, Tye KM (2013) Diverging neural pathways assemble a pattern. J Psychosomatic Res 49:319–333 behavioral state from separable features in anxiety. Nature 14. Masaoka Y, Homma I (1997) Anxiety and respiratory pattern: 496:219–223 their relationship during mental stress and physical load. Int J Psychophysiol 27:153–159

Journal

The Journal of Physiological SciencesSpringer Journals

Published: May 2, 2017

References

You’re reading a free preview. Subscribe to read the entire article.


DeepDyve is your
personal research library

It’s your single place to instantly
discover and read the research
that matters to you.

Enjoy affordable access to
over 18 million articles from more than
15,000 peer-reviewed journals.

All for just $49/month

Explore the DeepDyve Library

Search

Query the DeepDyve database, plus search all of PubMed and Google Scholar seamlessly

Organize

Save any article or search result from DeepDyve, PubMed, and Google Scholar... all in one place.

Access

Get unlimited, online access to over 18 million full-text articles from more than 15,000 scientific journals.

Your journals are on DeepDyve

Read from thousands of the leading scholarly journals from SpringerNature, Elsevier, Wiley-Blackwell, Oxford University Press and more.

All the latest content is available, no embargo periods.

See the journals in your area

DeepDyve

Freelancer

DeepDyve

Pro

Price

FREE

$49/month
$360/year

Save searches from
Google Scholar,
PubMed

Create lists to
organize your research

Export lists, citations

Read DeepDyve articles

Abstract access only

Unlimited access to over
18 million full-text articles

Print

20 pages / month

PDF Discount

20% off