Direct and indirect effects of age on interoceptive accuracy and awareness across the adult lifespan

Direct and indirect effects of age on interoceptive accuracy and awareness across the adult lifespan Psychon Bull Rev (2018) 25:1193–1202 DOI 10.3758/s13423-017-1339-z BRIEF REPORT Direct and indirect effects of age on interoceptive accuracy and awareness across the adult lifespan 1 2 2 2 Jennifer Murphy & Hayley Geary & Edward Millgate & Caroline Catmur & 1,3 Geoffrey Bird Published online: 6 July 2017 The Author(s) 2017. This article is an open access publication Abstract Various aspects of physical and mental health have reduced interoceptive accuracy. Such findings support and ex- been linked to an individual’s ability to perceive the physical tend previous research demonstrating interoceptive decline condition of their body (‘interoception’). In addition, numerous with advancing age, and highlight the importance of assessing studies have demonstrated a role for interoception in higher- whether decreasing interoceptive ability is responsible for some aspects of age-related ill-health and cognitive impairment. order cognitive abilities such as decision-making and emotion processing. The importance of interoception for health and typ- . . ical cognitive functioning has prompted interest in how Keywords Ageing Interoceptive accuracy Interoceptive interoception varies over the lifespan. However, few studies awareness have investigated interoception into older adulthood, and no studies account for the set of physiological changes that may influence task performance. The present study examined Introduction interoception from young to very late adulthood (until 90 years of age) utilising a self-report measure of interoception (Study Interoception is described as the perception of the physical One) and an objective measure of cardiac interoception (Study condition of the body (Craig, 2002), including numerous vis- Two). Across both studies, interoception decreased with age, ceral sensations such as hunger, itch, respiratory and cardiac and changes in interoceptive accuracy were observed which awareness (Khalsa & Lapidus, 2016). Whilst accurate percep- were not explained by accompanying physiological changes. tion of bodily sensations may be crucial for homeostasis, and In addition to a direct effect of age on interoception, an indirect therefore for maintaining physical health, in recent years there effect of ageing on cardiac interoceptive accuracy mediated by has been a growing interest in the relationship between body mass index (BMI) was found, such that ageing was asso- interoception and higher-order cognition. Indeed, ciated with increased BMI which was, in turn, associated with interoception has been related to various aspects of cognition, including emotional processing (Füstös, Gramann, Herbert, & Pollatos, 2013; Schandry, 1981; Terasawa, Fukushima, & Umeda, 2013; Wiens, Mezzacappa, & Katkin, 2000) and risky * Jennifer Murphy decision making (Dunn et al., 2010a; Sokol-Hessner, Hartley, Jennifer.Murphy@kcl.ac.uk Hamilton, & Phelps, 2015; Werner, Jung, Duschek, & Schandry, 2009), supporting theories of emotion and decision Social, Genetic and Developmental Psychiatry Centre (MRC), making that ascribe a fundamental role for the perception of Institute of Psychiatry, Psychology and Neuroscience - PO80, King’s bodily sensations (Critchley & Nagai, 2012; Damasio, 1994; College London, De Crespigny Park, Denmark Hill, London SE5 Garfinkel & Critchley, 2013; Gendron & Barrett, 2009; 8AF, UK 2 Schachter & Singer, 1962;Seth, 2013). Furthermore, evidence Institute of Psychiatry Psychology and Neuroscience, Department of supporting a role for interoception in higher-order cognition is Psychology, King’s College London, PO Box 78, 4 Windsor Walk, London SE5 8AF, UK consistent with both empirical evidence (e.g., (Ardizzi et al., 2016;Ehlers & Breuer, 1992; Gaigg, Cornell & Bird, 2016; Department of Experimental Psychology, University of Oxford, Oxford, UK Garfinkel, et al., 2016a; Herbert, Herbert, & Pollatos, 2011; 1194 Psychon Bull Rev (2018) 25:1193–1202 Herbert & Pollatos, 2014; Klabunde, Acheson, Boutelle, Examining cardiac interoception across the lifespan is com- Matthews, & Kaye, 2013; Mussgay, Klinkenberg, & Rüddel, plicated, however, by previous findings demonstrating that var- 1999; Pollatos et al., 2008; Shah, Hall, Catmur, & Bird, 2016) ious physiological and psychological factors influence task per- and theoretical models (Brewer, Happé, Cook, & Bird, 2015; formance, and have also been associated with ageing. For ex- Ehlers, 1993;Harshaw, 2015; Khalsa & Lapidus, 2016; ample, lower resting heartrate, reduced heartrate variability and Murphy, Brewer, Catmur, & Bird, 2017; Naqvi & Bechara, body composition (e.g., lower BMI/body fat) have all been as- 2010; Paulus & Stein, 2006;Quattrocki&Friston, 2014; sociated with better cardiac perception (Knapp-Kline & Kline, Verdejo-Garcia, Clark, & Dunn, 2012) linking aberrant 2005; Rouse, Jones, & Jones, 1988), while reduced systolic interoception (both atypically high and low interoception; blood pressure has been linked to worse cardiac perception see Murphy et al., 2017) to poor mental health in conditions (O’Brien, Reid, & Jones, 1998). Psychological factors such as such as panic and anxiety disorders, feeding and eating disor- participants’ beliefs regarding heartrate have also been shown to ders, substance abuse, autism, schizophrenia, somatic symp- strongly influence performance on objective tests of cardiac in- tom disorders and alexithymia. teroceptive accuracy (Ring, Brener, Knapp, & Mailloux, 2015; Given this body of evidence linking interoception to as- Ring & Brener, 1996; Windmann, Schonecke, Fröhlig, & pects of higher-order cognition and physical and mental health Maldener, 1999) and time perception has also been linked with (Brewer, Cook, & Bird, 2016; Khalsa & Lapidus, 2016; task performance (see Wittmann, 2013). Murphy et al., 2017), examining the stability of interoception It is therefore unclear whether ageing is associated with across an individual’s lifespan may be crucial. Notably, it has changes in interoceptive accuracy independent of its effects on been found that cardiac interoceptive accuracy declines with these psychological and physiological factors, or whether in fact age (Khalsa, Rudrauf, & Tranel, 2009), supporting earlier these factors mediate the effect of age on cardiac interoceptive work reporting that the perception of other interoceptive sig- accuracy (Franklin et al., 1997; St-Onge, 2005; Turgeon, Lustig, nals, including thirst (see Silver, 1990), taste (Stevens, Cruz, & Meck, 2016; Umetani, Singer, McCraty, & Atkinson, 1998; Hoffman, & Patterson, 1995), temperature (Clark & Mehl, Yashin et al., 2006). Examining whether changes in interoception 1971) and pain (see Gagliese, 2009), is less accurate in later across the lifespan are attributable directly to aging, or to factors life (but see Garfinkel et al., 2016b). However, although a co-varying with age, may be crucial for identifying the mecha- limited number of studies have therefore looked at develop- nism underlying interoceptive change with increased age. mental influences on the accuracy of interoception, to our Uncovering this mechanism is of interest given the relationship knowledge no study has examined age-related changes in between interoception and socio-cognitive abilities (Murphy self-reported awareness of interoceptive signals (known as et al., 2017), and the well-documented decline in these abilities interoceptive sensibility under the framework of Garfinkel, in later life (e.g., Ruffman, Henry, Livingstone, & Phillips, 2008; Sparrow & Spaniol, 2016). Furthermore, although a decline in Seth, Barrett, Suzuki, & Critchley, 2015), which is of interest as self-report measures of interoceptive awareness do not al- heartbeat discrimination performance with age has been demon- ways correlate with objective tests of interoceptive accuracy strated inparticipantsagedupto63yearsofage (Khalsaetal., (Garfinkel et al., 2015). Study One therefore aimed to examine 2009), whether cardiac interoceptive accuracy continues to de- interoceptive awareness across the lifespan. cline after this period into late, and very late, adulthood remains Alongside the investigation of whether interoceptive aware- an unanswered question, and is the focus of Study Two. ness declines over the lifespan, there is a need to improve our The present pair of studies therefore aimed to quantify in- understanding of changes in interoceptive accuracy. Studies ex- teroceptive awareness (Study One) and accuracy (Study Two) amining changes in interoceptive accuracy across the lifespan across the lifespan, from young adulthood to very late adult- typically use one of the two most commonly used measures of hood. Study One utilised self-report measures, whereas Study interoception: heartbeat tracking (Schandry, 1981)and discrim- Two utilised objective measures whilst also measuring psy- ination procedures (Brener & Kluvitse, 1988; Whitehead, chological and physiological factors which may mediate any Drescher, Heiman, & Blackwell, 1977), which both assess per- association between cardiac interoception and age. ception of cardiac signals. In the former, participants are asked to count their heartbeats over a series of intervals whilst their heart- beat is objectively measured. The difference between the objec- Study one tive and subjective measurements acts as a measure of intero- ceptive accuracy. In the latter, participants are asked to determine Methods whether a signal is in or out of sync with their heartbeat. In a study by Khalsa and colleagues (2009), age explained ~40% of Participants the variance in heartbeat discrimination performance in partici- pants aged up to 63 years of age, such that increasing age was A total of 1008 participants took part in an online survey with associated with poorer performance. a prize draw offered as incentive. Of these, 898 participants Psychon Bull Rev (2018) 25:1193–1202 1195 completed the survey as part of a larger study that included additional questionnaires, with the remainder (110 partici- pants) only completing the interoceptive awareness question- naire. Participants were recruited from pre-existing participant databases and via social media outlets. Of the 1008 partici- pants, 345 participants fully completed the survey, reported no pre-existing psychiatric conditions and had English as their first language and were therefore included in the study (M age =38.66, SD = 17.59, Age range 18–89 years, 95 males, 0 age other). Of the 345 participants, 235 completed the additional questionnaires. In line with the declaration of Helsinki, all participants gave informed consent and were debriefed upon task completion. Measures and procedure Fig. 1 A significant relationship between self-reported interoceptive awareness, as measured by the very short BPQ, and age was observed The online survey was conducted using Qualtrics such that increasing age was associated with poorer interoceptive Research Suite (Qualtrics, Provo, UT, USA). To quanti- awareness fy interoceptive awareness, the very short version of the Body Perception Questionnaire (BPQ; Porges, 1993; interoceptive awareness into very late adulthood would be Kolacz et al., in preparation) was used. In this 12-item accompanied by decreasing interoceptive accuracy as mea- questionnaire, participants are asked to indicate on a 5- sured by objective tests. To examine this question, Study point Likert scale (strongly disagree to strongly agree) Two utilised an objective measurement of interoceptive accu- whether they are aware of particular bodily sensations racy to quantify interoception across the lifespan. (e.g., their mouth being dry) during most situations. Prior to the questionnaire, demographic details were col- lected, including age (years) and sex (male, female, oth- er). Additionally, participants were asked to indicate Study two whether English was their first language and whether they had a diagnosis of any psychiatric conditions. Methods Results and discussion Participants BPQ scoresrangedfrom12to57(M =26.89, SD =10.12) A total of 140 participants took part in this study in ex- with high scores representing greater self-reported awareness change for a small honorarium. Participants were selected of interoceptive signals. A Spearman’s rank order correlation on the basis that they had no known psychiatric or neu- indicated a significant negative correlation between age rological conditions. To screen for cognitive impairment, (years) and BPQ scores, r(345) = –.337, p < .001 (two-tailed; all participants were administered the Mini Mental State Fig. 1). No sex differences were found, t(343) = .208, Examination test (MMSE; Folstein, Folstein, & McHugh, p >.250, d = .03, 95% CI for d (–0.211, 0.261). No differences 1975), with scores below 23 indicative of cognitive im- in BPQ scores were observed between participants completing pairment (Tombaugh & McIntyre, 1992). Four participants just the interoception questionnaire and those completing ad- were excluded (one scored below the typical threshold on ditional questionnaires when age was statistically controlled the MMSE; two disclosed existing psychiatric/neurological for, t(343) = 0.68, p > .250, d = .08, 95% CI for d (–.154, conditions post-testing; and one was excluded due to .317). equipment failure) resulting in 136 valid cases (M = age A significant negative association between age and self- 55.10, SD = 19.50; age range 20–90 years, 49 males). age reported interoceptive awareness was found. These results A minimum of 5 participants were present in each 5-year suggest that interoceptive awareness deteriorates across the age bracket. In line with the declaration of Helsinki, all lifespan and continues to decline into late, and very late, adult- participants gave informed consent and were debriefed up- hood. However, given previous findings of a dissociation be- on task completion. To minimise the effects of elevated tween subjective tests of interoceptive awareness and objec- heartrate on accuracy (Knapp-Kline & Kline, 2005), all tive tests of interoceptive accuracy (Garfinkel et al., 2015), it participants were asked to refrain from caffeine for 6 h remains unclear whether the continuing decline of prior to testing. 1196 Psychon Bull Rev (2018) 25:1193–1202 Interoception Scoring and data analysis The heartbeat tracking task (Schandry, 1981) was used to Interoceptive and timing accuracy quantify interoceptive accuracy with timing ability employed as a control task (Ainley, Brass, & Tsakiris, 2014;Shah etal., Interoceptive accuracy on the heartbeat tracking task was es- 2016). Objective heartbeat was measured using a pulse oxim- timated on a scale from 0 to 400: Σ[1 – (|Actual number of eter (Contec Systems, CMS-50Dþ; Qinhuangdao, China) at- heartbeats – participant’s estimate|/Actual number of heart- tached to the participant’s right index finger. Each participant beats)] × 100. Higher scores indicate better performance completed both the heartbeat tracking task and the timing task (Shah et al., 2016; see also Garfinkel et al., 2015). Timing over four durations. Two sets of durations were used (either scores were estimated similarly, Σ[1 – (|Actual number of 25, 35, 45, 100 s or 28, 38, 48, 103 s) and the duration sets seconds – participant’s estimate|/Actual number of seconds)] were counterbalanced across participants such that half of the × 100. Again, high scores indicate better performance. participants completed the longer durations for the timing task Average ratio scores (participants’ estimate/objective and half completed the longer intervals for the heartbeat task. measure) were also computed with scores above one Additionally, task order was fully counterbalanced, and the indicative of overestimation. Unsurprisingly, given the order of individual durations was counterbalanced according explicit task instructions (see Methods), >95% of partic- to a Latin-square across participants. Task order did not affect ipants underestimated the number of heartbeats and a performance in interoceptive accuracy, t(134) = 1.640, p >.05, similar pattern was observed for timing accuracy d =0.28, 95%CI for d (–0.057, 0.619) or timing accuracy, (>80%). This variable was therefore not considered t(134) = 1.364, p >.05, d =0.23,95%CIfor d (-0.104, 0.571). further. During the task, participants were seated with both feet flat on the floor and both hands on the table. Participants were Body composition instructed that they would be asked to silently count their heartbeats over a period without physically measuring their BMI was calculated using the following equation: mass(kg)/ heartbeat. With their eyes closed, they were asked to count 2 (height(m)) . their heartbeats from when the experimenter said Bstart^ until they heard a beep, at which point they should indicate the Beliefs regarding heartrate number they had counted. They were explicitly told to only count heartbeats they felt and not to count seconds or guess. The accuracy of participants’ beliefs was calculated as a con- They were also told that if they did not feel anything they tinuous variable calculated by taking the absolute difference should give zero as their answer. Participants were then given between participants’ estimates and the grand mean of resting 2 min to practice prior to the first heartrate trial; no feedback heartrate reported in large studies of human physiology was provided. The timing task was identical to the heartbeat (Agelink et al., 2001; Ramaekers, Ector, Aubert, Rubens, & task except participants were asked to count seconds rather Van de Werf, 1998; grand mean = 72.26 beats per minute; than their heartbeats. bpm). As this variable indicates how far participants’ esti- mates are from the grand mean, higher scores indicate more Anthropometrics inaccurate beliefs about the average person’sheartrate. For each participant body mass index (BMI) and blood pres- sure measurements were taken. Blood pressure was taken Heartrate physiology using an electronic upper arm monitor (Omron M2) whilst participants were seated. A proxy of heartrate variability was calculated from pulse-rate signals. This method has been shown to be reliable when Beliefs regarding heartrate participants are at rest (Schäfer & Vagedes, 2013). For each participant, the root mean squared of successive differences To quantify beliefs, participants were asked to estimate the (RMSSD) was calculated from the last 60 s of heartrate re- average person’s resting heartbeat. Specifically, participants cording for the longest interval examined (100 or 103 s). were asked ‘How many times do you think the average per- RMSSD was favoured over other measures of heartrate vari- son’s heartbeats, in 1 min when they are at rest?’ Note that ability due to evidence attesting to its better reliability over earlier studies sometimes required the participant to estimate short durations (Munoz et al., 2015). From this same 60-s their own heartrate (Ring, et al., 2015; Ring & Brener, 1996); interval, mean resting heartrate (average bpm) was taken. this was avoided in the present study to avoid any effect of the For three participants, the recording for the 100-s interval estimation on the heartbeat tracking task or vice versa. was corrupted, and a 60-s recording from one of the other Psychon Bull Rev (2018) 25:1193–1202 1197 intervals was used as a replacement which was comparable to p > .05 (one-tailed) were not significant, but the correlation the 100-s recordings. between age and timing performance approached significance r(136) = –.14, p = .05. When formally compared, the sizes of Analysis strategy the correlations between ageing and interoceptive accuracy, and ageing and the timing control task, were not significantly Zero-order correlations revealed the associations between age- different (z =0.6, p =.55). ing and cardiac interoceptive accuracy, and ageing and the Age was positively associated with BMI, r(136) = .25, timing control task. The size of these correlations were com- p = .002 (one-tailed). A negative relationship between age pared using Steiger’s Z-test (Steiger, 1980) using the quantpsy and heartrate variability was also observed, r(136) = –.16, web implementation (Lee & Preacher, 2013). Correlations p = .036 (one-tailed). In contrast, age was not associated with were then used to examine the association between age and resting heartrate, r(136) = –.01, p > .05 (one-tailed), systolic the possible psychological and physiological mediators of the blood pressure, r(136) = –.10, p > .05 (one-tailed), or beliefs effect of age on interoceptive accuracy, before similar analyses (r(136) = –.04, p >.05; two-tailed). compared the relationship between these potential mediators Negative associations were observed between interocep- and interoceptive accuracy. tive accuracy and BMI, r(136) = –.19, p = .015, and beliefs, The existence of direct and indirect effects of age on inter- r(136) = –.232, p = .003 (one-tailed). A positive association oceptive accuracy was investigated using a parallel mediation was observed between interoceptive accuracy and systolic model in which BMI, gender, systolic blood pressure, accura- blood pressure, r(136) = .21, p = .008 (one-tailed). No associ- cy of beliefs about average heartrate, heartrate variability, ation was observed between interoception and heartrate vari- mean heartrate, and timing accuracy were entered as potential ability, r(136) = .06, p > .05, or resting heartrate, r(136) = mediators of the effect of age on interoception. Mediation –.10, p > .05 (one-tailed). modelling was carried out using the SPSS macro-script The results of the mediation model are illustrated in Fig. 2. (Process) provided by Hayes (2013) and Preacher and Hayes As can be seen, there was a significant effect of age on BMI, (2008). For indirect effects, 90% (one-tailed) bias-corrected heartrate variability, and performance on the timing control bootstrapped confidence intervals were calculated using task (as outlined above; all one-tailed). All other predictors 5,000 repetitions. This method was selected over the Sobel were non-significant (all p > .10). There were also significant (1982) method as the former does not require the assumption effects of BMI (b = –.15, SE =.09, p = .04), gender (b = –.34, of a normal distribution and simulation studies indicate higher SE =.17, p = .02), beliefs regarding average heartrate (b = power whilst controlling for Type one error rates –.22, SE = .08, p = .004) and systolic blood pressure (b = (MacKinnon, Lockwood, Hoffman, West, & Sheets, 2002; .19, SE =.08, p = .01) on interoception (all one-tailed). All Mackinnon, Lockwood, & Williams, 2004). As outlined by other predictors were non-significant (all p > .10). Of impor- Preacher and Hayes (2004), an indirect effect is significant if tance was the finding that age exerted a direct (i.e. unmediat- the confidence intervals for the indirect effect do not include ed) effect on interoception (direct effect = –.15, SE =.09, t = zero. For all analyses where directional hypotheses are made, 1.69, p = .047; one-tailed) and a small indirect effect on one-tailed p values are reported. Standardized coefficients are interoception mediated by the effect of BMI (b = –.039, SE reported in the mediation analysis. =.03, CI (–.982, –.004); one-tailed) despite no total indirect effect (b = –.06, SE =.05, CI(–1.12, .25). All other indirect Results and discussion effects were non-significant (e.g., confidence intervals includ- ed zero). The indirect effect of BMI accounted for 0.18 (18%) A small amount of randomly-distributed data were missing of the total effect between age and interoception (ab/c;see (0.74%; three blood pressure measurements, two belief esti- Jose, 2013), indicating partial mediation. mates, and one measure of heartrate variability and resting heartrate) and these missing values were imputed using mul- tiple imputation in SPSS. The Mersenne–Twister algorithm General discussion with a starting point fixed to 2,000,000 was utilised for ran- dom number generation. All variables were entered into the This set of studies aimed to examine variation in interoceptive model, the automatic method was selected, and all variables awareness and accuracy across the lifespan. In Study One, a were used as predictors. No participant had more than one negative relationship between age and interoceptive aware- missing data point. ness was observed; older participants rated their interoceptive Simple zero-order correlations revealed a significant nega- awareness as reduced. Building on this, Study Two examined tive association between interoceptive accuracy and age, cardiac interoceptive accuracy across the adult lifespan using r(136) = –.21 p = .008 (one-tailed). Correlations between in- an objective performance measure, demonstrating a negative teroceptive accuracy and timing performance, r(136) = .12, relationship between age and interoceptive accuracy. These 1198 Psychon Bull Rev (2018) 25:1193–1202 Fig. 2 Depicts the results of the mediation analysis. Mediation analysis accuracy; Fig. 2 centre), in addition to an indirect path from age to indicated a significant path from age to BMI, heartrate variability and interoception via BMI. The indirect path via BMI thus partially time perception ability (a path; the individual relationships between the mediated the effect of age on interoception. *Denotes significance at IVand the mediators; e.g., from age to BMI; Fig. 2 left), whilst significant the p < .05 level (one-tailed). BMI Body Mass Index; Gender Male or paths to interoceptive accuracy from BMI, gender, heartrate variability Female (0 or 1); Heartrate Variability variation in the time interval beliefs and time perception ability were also observed (b path; the between heartbeats; Mean HR The average second-by-second heartbeat relationship between the mediators and the DV controlling for other recorded over 60 seconds; Beliefs the error of participants’ estimates mediators and keeping the IV constant; e.g., from BMI to interoceptive regarding the average heartrate; Time Perception Performance on the time accuracy; Fig. 2 right). Most importantly, a direct effect of age on estimation task; Systolic Blood Pressure Taken whilst seated and mea- interoceptive accuracy was observed (c’ path; the relationship between sured in millimetres of mercury the IVand the DV controlling for the mediators; from age to interoceptive data confirm previously reported evidence suggesting a de- awareness and interoceptive accuracy (Garfinkel et al., cline in interoceptive accuracy in older adulthood (Khalsa 2015) mean that care must be taken in interpreting reduced et al., 2009), and go further to suggest that this decline con- awareness of interceptive signals as underlying the direct ef- tinues into both late and very late adulthood. fect of age on interoceptive accuracy. The results from Study Two highlight that the poor perfor- The relationship between age and performance on the in- mance observed in late adulthood is due to both a direct effect teroceptive accuracy and timing control tasks is worthy of of age on interoceptive accuracy and an indirect effect medi- note. Whereas the zero-order correlations indicated a similar ated by BMI, whereby age was associated with increased magnitude of the effect of ageing on performance of these BMI, which in turn, predicted reduced interoceptive accuracy. tasks, the results of the mediation analysis demonstrate that Therefore, it appears that changes in BMI partially mediate the the effects of ageing on interoceptive accuracy were not a relationship between age and interoception. Other physiolog- product of reduced timing/counting ability (Turgeon et al., ical and psychological changes such as heartrate variability, 2016; Wittmann, 2013), and are also likely not due to general resting heartrate, and time perception, previously associated problems with motivation or attention. Thus, although similar both with interoceptive accuracy (Knapp-Kline & Kline, age-related declines were observed across these tasks, the ef- 2005;O’Brien et al., 1998; Rouse et al., 1988; Wittmann, fects of age were independent. 2013) and increasing age (Franklin et al., 1997; St-Onge, The finding that interoception declines throughout the 2005; Umetani et al., 1998; Yashin et al., 2006), were not lifespan raises important questions regarding the extent to significant mediators of the age–interoception relationship. which interoception is related to the decline in socio- The partial mediation of the effect of age on interoceptive emotional competence and altered cognition observed in late accuracy by BMI provides some indication as to the mecha- adulthood (Murphy et al., 2017). For example, a body of re- nism by which ageing negatively impacts interoceptive accu- search indicates poorer emotion recognition (Ruffman et al., racy. However, the existence of a direct effect of age indicates 2008) and changes in risky decision making with advancing at least one further mechanism to be identified. Although the age (Sparrow & Spaniol, 2016). Crucially, these same abilities results of Study One demonstrated reduced awareness of in- have been linked to interoceptive accuracy (Dunn et al., teroceptive information with increasing age, previous reports 2010b; Füstös et al., 2013; Schandry, 1981; Sokol-Hessner of a dissociation between self-reported interoceptive et al., 2015; Terasawa et al., 2013;Werneretal., 2009; Psychon Bull Rev (2018) 25:1193–1202 1199 Wiens et al., 2000). Given the interrelatedness of these factors, interoceptive metacognition—particularly those with inflated determining the extent to which age-related changes in these beliefs regarding their ability—may utilise unreliable intero- abilities is predicted by interoception is an important aim for ceptive cues for gauging interoceptive states, placing them at future research. Moreover, if interoception does underlie ad- a greater risk of adverse health outcomes (e.g., dehydration). verse age-related cognitive change, then such evidence may In conclusion, Study One demonstrated a negative relation- inform interventions, such as interoceptive training (e.g., ship between age and interoceptive awareness. Study Two dem- Canales-Johnson et al., 2015; Schaefer, Egloff, Gerlach, & onstrated that the decline in interoceptive accuracy across the Witthöft, 2014; Schandry & Weitkunat, 1990) designed to lifespan continues into late and very late adulthood. A decline ameliorate undesirable effects of ageing on cognition and in interoceptive awareness and accuracy with increasing age socio-emotional competence. highlights the importance of understanding the relationship be- In comparison to the only other study examining the impact tween age-related changes in interoceptive ability and age- of older age on cardiac interoceptive accuracy (Khalsa et al., related changes in cognition and physical and mental health. 2009), the variance explained by age in the present study was Acknowledgements JM was supported by a doctoral studentship from modest. The difference in the size of the observed age effect the Economic and Social Research Council [1599941; ES/J500057/1]. could be because the present study quantified interoceptive ac- GB was supported by the Baily Thomas Trust. We gratefully acknowl- curacy using the heartbeat tracking task (Schandry, 1981), edge the help of Raluca Prepelita in the early stages of data collection. whereas Khalsa et al. (2009) utilised the heartbeat discrimination Open Access This article is distributed under the terms of the Creative procedure (Brener & Kluvitse, 1988; Whitehead et al., 1977). Commons Attribution 4.0 International License (http:// Whilst small to moderate correlations have been observed be- creativecommons.org/licenses/by/4.0/), which permits unrestricted use, tween these two tasks (Garfinkel et al., 2015; Knoll & Hodapp, distribution, and reproduction in any medium, provided you give appro- 1992; but see Phillips, Jones, Rieger, & Snell, 1999), the extent priate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. to which task differences impact the accurate measurement of interoceptive accuracy remains unknown. 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Direct and indirect effects of age on interoceptive accuracy and awareness across the adult lifespan

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Psychon Bull Rev (2018) 25:1193–1202 DOI 10.3758/s13423-017-1339-z BRIEF REPORT Direct and indirect effects of age on interoceptive accuracy and awareness across the adult lifespan 1 2 2 2 Jennifer Murphy & Hayley Geary & Edward Millgate & Caroline Catmur & 1,3 Geoffrey Bird Published online: 6 July 2017 The Author(s) 2017. This article is an open access publication Abstract Various aspects of physical and mental health have reduced interoceptive accuracy. Such findings support and ex- been linked to an individual’s ability to perceive the physical tend previous research demonstrating interoceptive decline condition of their body (‘interoception’). In addition, numerous with advancing age, and highlight the importance of assessing studies have demonstrated a role for interoception in higher- whether decreasing interoceptive ability is responsible for some aspects of age-related ill-health and cognitive impairment. order cognitive abilities such as decision-making and emotion processing. The importance of interoception for health and typ- . . ical cognitive functioning has prompted interest in how Keywords Ageing Interoceptive accuracy Interoceptive interoception varies over the lifespan. However, few studies awareness have investigated interoception into older adulthood, and no studies account for the set of physiological changes that may influence task performance. The present study examined Introduction interoception from young to very late adulthood (until 90 years of age) utilising a self-report measure of interoception (Study Interoception is described as the perception of the physical One) and an objective measure of cardiac interoception (Study condition of the body (Craig, 2002), including numerous vis- Two). Across both studies, interoception decreased with age, ceral sensations such as hunger, itch, respiratory and cardiac and changes in interoceptive accuracy were observed which awareness (Khalsa & Lapidus, 2016). Whilst accurate percep- were not explained by accompanying physiological changes. tion of bodily sensations may be crucial for homeostasis, and In addition to a direct effect of age on interoception, an indirect therefore for maintaining physical health, in recent years there effect of ageing on cardiac interoceptive accuracy mediated by has been a growing interest in the relationship between body mass index (BMI) was found, such that ageing was asso- interoception and higher-order cognition. Indeed, ciated with increased BMI which was, in turn, associated with interoception has been related to various aspects of cognition, including emotional processing (Füstös, Gramann, Herbert, & Pollatos, 2013; Schandry, 1981; Terasawa, Fukushima, & Umeda, 2013; Wiens, Mezzacappa, & Katkin, 2000) and risky * Jennifer Murphy decision making (Dunn et al., 2010a; Sokol-Hessner, Hartley, Jennifer.Murphy@kcl.ac.uk Hamilton, & Phelps, 2015; Werner, Jung, Duschek, & Schandry, 2009), supporting theories of emotion and decision Social, Genetic and Developmental Psychiatry Centre (MRC), making that ascribe a fundamental role for the perception of Institute of Psychiatry, Psychology and Neuroscience - PO80, King’s bodily sensations (Critchley & Nagai, 2012; Damasio, 1994; College London, De Crespigny Park, Denmark Hill, London SE5 Garfinkel & Critchley, 2013; Gendron & Barrett, 2009; 8AF, UK 2 Schachter & Singer, 1962;Seth, 2013). Furthermore, evidence Institute of Psychiatry Psychology and Neuroscience, Department of supporting a role for interoception in higher-order cognition is Psychology, King’s College London, PO Box 78, 4 Windsor Walk, London SE5 8AF, UK consistent with both empirical evidence (e.g., (Ardizzi et al., 2016;Ehlers & Breuer, 1992; Gaigg, Cornell & Bird, 2016; Department of Experimental Psychology, University of Oxford, Oxford, UK Garfinkel, et al., 2016a; Herbert, Herbert, & Pollatos, 2011; 1194 Psychon Bull Rev (2018) 25:1193–1202 Herbert & Pollatos, 2014; Klabunde, Acheson, Boutelle, Examining cardiac interoception across the lifespan is com- Matthews, & Kaye, 2013; Mussgay, Klinkenberg, & Rüddel, plicated, however, by previous findings demonstrating that var- 1999; Pollatos et al., 2008; Shah, Hall, Catmur, & Bird, 2016) ious physiological and psychological factors influence task per- and theoretical models (Brewer, Happé, Cook, & Bird, 2015; formance, and have also been associated with ageing. For ex- Ehlers, 1993;Harshaw, 2015; Khalsa & Lapidus, 2016; ample, lower resting heartrate, reduced heartrate variability and Murphy, Brewer, Catmur, & Bird, 2017; Naqvi & Bechara, body composition (e.g., lower BMI/body fat) have all been as- 2010; Paulus & Stein, 2006;Quattrocki&Friston, 2014; sociated with better cardiac perception (Knapp-Kline & Kline, Verdejo-Garcia, Clark, & Dunn, 2012) linking aberrant 2005; Rouse, Jones, & Jones, 1988), while reduced systolic interoception (both atypically high and low interoception; blood pressure has been linked to worse cardiac perception see Murphy et al., 2017) to poor mental health in conditions (O’Brien, Reid, & Jones, 1998). Psychological factors such as such as panic and anxiety disorders, feeding and eating disor- participants’ beliefs regarding heartrate have also been shown to ders, substance abuse, autism, schizophrenia, somatic symp- strongly influence performance on objective tests of cardiac in- tom disorders and alexithymia. teroceptive accuracy (Ring, Brener, Knapp, & Mailloux, 2015; Given this body of evidence linking interoception to as- Ring & Brener, 1996; Windmann, Schonecke, Fröhlig, & pects of higher-order cognition and physical and mental health Maldener, 1999) and time perception has also been linked with (Brewer, Cook, & Bird, 2016; Khalsa & Lapidus, 2016; task performance (see Wittmann, 2013). Murphy et al., 2017), examining the stability of interoception It is therefore unclear whether ageing is associated with across an individual’s lifespan may be crucial. Notably, it has changes in interoceptive accuracy independent of its effects on been found that cardiac interoceptive accuracy declines with these psychological and physiological factors, or whether in fact age (Khalsa, Rudrauf, & Tranel, 2009), supporting earlier these factors mediate the effect of age on cardiac interoceptive work reporting that the perception of other interoceptive sig- accuracy (Franklin et al., 1997; St-Onge, 2005; Turgeon, Lustig, nals, including thirst (see Silver, 1990), taste (Stevens, Cruz, & Meck, 2016; Umetani, Singer, McCraty, & Atkinson, 1998; Hoffman, & Patterson, 1995), temperature (Clark & Mehl, Yashin et al., 2006). Examining whether changes in interoception 1971) and pain (see Gagliese, 2009), is less accurate in later across the lifespan are attributable directly to aging, or to factors life (but see Garfinkel et al., 2016b). However, although a co-varying with age, may be crucial for identifying the mecha- limited number of studies have therefore looked at develop- nism underlying interoceptive change with increased age. mental influences on the accuracy of interoception, to our Uncovering this mechanism is of interest given the relationship knowledge no study has examined age-related changes in between interoception and socio-cognitive abilities (Murphy self-reported awareness of interoceptive signals (known as et al., 2017), and the well-documented decline in these abilities interoceptive sensibility under the framework of Garfinkel, in later life (e.g., Ruffman, Henry, Livingstone, & Phillips, 2008; Sparrow & Spaniol, 2016). Furthermore, although a decline in Seth, Barrett, Suzuki, & Critchley, 2015), which is of interest as self-report measures of interoceptive awareness do not al- heartbeat discrimination performance with age has been demon- ways correlate with objective tests of interoceptive accuracy strated inparticipantsagedupto63yearsofage (Khalsaetal., (Garfinkel et al., 2015). Study One therefore aimed to examine 2009), whether cardiac interoceptive accuracy continues to de- interoceptive awareness across the lifespan. cline after this period into late, and very late, adulthood remains Alongside the investigation of whether interoceptive aware- an unanswered question, and is the focus of Study Two. ness declines over the lifespan, there is a need to improve our The present pair of studies therefore aimed to quantify in- understanding of changes in interoceptive accuracy. Studies ex- teroceptive awareness (Study One) and accuracy (Study Two) amining changes in interoceptive accuracy across the lifespan across the lifespan, from young adulthood to very late adult- typically use one of the two most commonly used measures of hood. Study One utilised self-report measures, whereas Study interoception: heartbeat tracking (Schandry, 1981)and discrim- Two utilised objective measures whilst also measuring psy- ination procedures (Brener & Kluvitse, 1988; Whitehead, chological and physiological factors which may mediate any Drescher, Heiman, & Blackwell, 1977), which both assess per- association between cardiac interoception and age. ception of cardiac signals. In the former, participants are asked to count their heartbeats over a series of intervals whilst their heart- beat is objectively measured. The difference between the objec- Study one tive and subjective measurements acts as a measure of intero- ceptive accuracy. In the latter, participants are asked to determine Methods whether a signal is in or out of sync with their heartbeat. In a study by Khalsa and colleagues (2009), age explained ~40% of Participants the variance in heartbeat discrimination performance in partici- pants aged up to 63 years of age, such that increasing age was A total of 1008 participants took part in an online survey with associated with poorer performance. a prize draw offered as incentive. Of these, 898 participants Psychon Bull Rev (2018) 25:1193–1202 1195 completed the survey as part of a larger study that included additional questionnaires, with the remainder (110 partici- pants) only completing the interoceptive awareness question- naire. Participants were recruited from pre-existing participant databases and via social media outlets. Of the 1008 partici- pants, 345 participants fully completed the survey, reported no pre-existing psychiatric conditions and had English as their first language and were therefore included in the study (M age =38.66, SD = 17.59, Age range 18–89 years, 95 males, 0 age other). Of the 345 participants, 235 completed the additional questionnaires. In line with the declaration of Helsinki, all participants gave informed consent and were debriefed upon task completion. Measures and procedure Fig. 1 A significant relationship between self-reported interoceptive awareness, as measured by the very short BPQ, and age was observed The online survey was conducted using Qualtrics such that increasing age was associated with poorer interoceptive Research Suite (Qualtrics, Provo, UT, USA). To quanti- awareness fy interoceptive awareness, the very short version of the Body Perception Questionnaire (BPQ; Porges, 1993; interoceptive awareness into very late adulthood would be Kolacz et al., in preparation) was used. In this 12-item accompanied by decreasing interoceptive accuracy as mea- questionnaire, participants are asked to indicate on a 5- sured by objective tests. To examine this question, Study point Likert scale (strongly disagree to strongly agree) Two utilised an objective measurement of interoceptive accu- whether they are aware of particular bodily sensations racy to quantify interoception across the lifespan. (e.g., their mouth being dry) during most situations. Prior to the questionnaire, demographic details were col- lected, including age (years) and sex (male, female, oth- er). Additionally, participants were asked to indicate Study two whether English was their first language and whether they had a diagnosis of any psychiatric conditions. Methods Results and discussion Participants BPQ scoresrangedfrom12to57(M =26.89, SD =10.12) A total of 140 participants took part in this study in ex- with high scores representing greater self-reported awareness change for a small honorarium. Participants were selected of interoceptive signals. A Spearman’s rank order correlation on the basis that they had no known psychiatric or neu- indicated a significant negative correlation between age rological conditions. To screen for cognitive impairment, (years) and BPQ scores, r(345) = –.337, p < .001 (two-tailed; all participants were administered the Mini Mental State Fig. 1). No sex differences were found, t(343) = .208, Examination test (MMSE; Folstein, Folstein, & McHugh, p >.250, d = .03, 95% CI for d (–0.211, 0.261). No differences 1975), with scores below 23 indicative of cognitive im- in BPQ scores were observed between participants completing pairment (Tombaugh & McIntyre, 1992). Four participants just the interoception questionnaire and those completing ad- were excluded (one scored below the typical threshold on ditional questionnaires when age was statistically controlled the MMSE; two disclosed existing psychiatric/neurological for, t(343) = 0.68, p > .250, d = .08, 95% CI for d (–.154, conditions post-testing; and one was excluded due to .317). equipment failure) resulting in 136 valid cases (M = age A significant negative association between age and self- 55.10, SD = 19.50; age range 20–90 years, 49 males). age reported interoceptive awareness was found. These results A minimum of 5 participants were present in each 5-year suggest that interoceptive awareness deteriorates across the age bracket. In line with the declaration of Helsinki, all lifespan and continues to decline into late, and very late, adult- participants gave informed consent and were debriefed up- hood. However, given previous findings of a dissociation be- on task completion. To minimise the effects of elevated tween subjective tests of interoceptive awareness and objec- heartrate on accuracy (Knapp-Kline & Kline, 2005), all tive tests of interoceptive accuracy (Garfinkel et al., 2015), it participants were asked to refrain from caffeine for 6 h remains unclear whether the continuing decline of prior to testing. 1196 Psychon Bull Rev (2018) 25:1193–1202 Interoception Scoring and data analysis The heartbeat tracking task (Schandry, 1981) was used to Interoceptive and timing accuracy quantify interoceptive accuracy with timing ability employed as a control task (Ainley, Brass, & Tsakiris, 2014;Shah etal., Interoceptive accuracy on the heartbeat tracking task was es- 2016). Objective heartbeat was measured using a pulse oxim- timated on a scale from 0 to 400: Σ[1 – (|Actual number of eter (Contec Systems, CMS-50Dþ; Qinhuangdao, China) at- heartbeats – participant’s estimate|/Actual number of heart- tached to the participant’s right index finger. Each participant beats)] × 100. Higher scores indicate better performance completed both the heartbeat tracking task and the timing task (Shah et al., 2016; see also Garfinkel et al., 2015). Timing over four durations. Two sets of durations were used (either scores were estimated similarly, Σ[1 – (|Actual number of 25, 35, 45, 100 s or 28, 38, 48, 103 s) and the duration sets seconds – participant’s estimate|/Actual number of seconds)] were counterbalanced across participants such that half of the × 100. Again, high scores indicate better performance. participants completed the longer durations for the timing task Average ratio scores (participants’ estimate/objective and half completed the longer intervals for the heartbeat task. measure) were also computed with scores above one Additionally, task order was fully counterbalanced, and the indicative of overestimation. Unsurprisingly, given the order of individual durations was counterbalanced according explicit task instructions (see Methods), >95% of partic- to a Latin-square across participants. Task order did not affect ipants underestimated the number of heartbeats and a performance in interoceptive accuracy, t(134) = 1.640, p >.05, similar pattern was observed for timing accuracy d =0.28, 95%CI for d (–0.057, 0.619) or timing accuracy, (>80%). This variable was therefore not considered t(134) = 1.364, p >.05, d =0.23,95%CIfor d (-0.104, 0.571). further. During the task, participants were seated with both feet flat on the floor and both hands on the table. Participants were Body composition instructed that they would be asked to silently count their heartbeats over a period without physically measuring their BMI was calculated using the following equation: mass(kg)/ heartbeat. With their eyes closed, they were asked to count 2 (height(m)) . their heartbeats from when the experimenter said Bstart^ until they heard a beep, at which point they should indicate the Beliefs regarding heartrate number they had counted. They were explicitly told to only count heartbeats they felt and not to count seconds or guess. The accuracy of participants’ beliefs was calculated as a con- They were also told that if they did not feel anything they tinuous variable calculated by taking the absolute difference should give zero as their answer. Participants were then given between participants’ estimates and the grand mean of resting 2 min to practice prior to the first heartrate trial; no feedback heartrate reported in large studies of human physiology was provided. The timing task was identical to the heartbeat (Agelink et al., 2001; Ramaekers, Ector, Aubert, Rubens, & task except participants were asked to count seconds rather Van de Werf, 1998; grand mean = 72.26 beats per minute; than their heartbeats. bpm). As this variable indicates how far participants’ esti- mates are from the grand mean, higher scores indicate more Anthropometrics inaccurate beliefs about the average person’sheartrate. For each participant body mass index (BMI) and blood pres- sure measurements were taken. Blood pressure was taken Heartrate physiology using an electronic upper arm monitor (Omron M2) whilst participants were seated. A proxy of heartrate variability was calculated from pulse-rate signals. This method has been shown to be reliable when Beliefs regarding heartrate participants are at rest (Schäfer & Vagedes, 2013). For each participant, the root mean squared of successive differences To quantify beliefs, participants were asked to estimate the (RMSSD) was calculated from the last 60 s of heartrate re- average person’s resting heartbeat. Specifically, participants cording for the longest interval examined (100 or 103 s). were asked ‘How many times do you think the average per- RMSSD was favoured over other measures of heartrate vari- son’s heartbeats, in 1 min when they are at rest?’ Note that ability due to evidence attesting to its better reliability over earlier studies sometimes required the participant to estimate short durations (Munoz et al., 2015). From this same 60-s their own heartrate (Ring, et al., 2015; Ring & Brener, 1996); interval, mean resting heartrate (average bpm) was taken. this was avoided in the present study to avoid any effect of the For three participants, the recording for the 100-s interval estimation on the heartbeat tracking task or vice versa. was corrupted, and a 60-s recording from one of the other Psychon Bull Rev (2018) 25:1193–1202 1197 intervals was used as a replacement which was comparable to p > .05 (one-tailed) were not significant, but the correlation the 100-s recordings. between age and timing performance approached significance r(136) = –.14, p = .05. When formally compared, the sizes of Analysis strategy the correlations between ageing and interoceptive accuracy, and ageing and the timing control task, were not significantly Zero-order correlations revealed the associations between age- different (z =0.6, p =.55). ing and cardiac interoceptive accuracy, and ageing and the Age was positively associated with BMI, r(136) = .25, timing control task. The size of these correlations were com- p = .002 (one-tailed). A negative relationship between age pared using Steiger’s Z-test (Steiger, 1980) using the quantpsy and heartrate variability was also observed, r(136) = –.16, web implementation (Lee & Preacher, 2013). Correlations p = .036 (one-tailed). In contrast, age was not associated with were then used to examine the association between age and resting heartrate, r(136) = –.01, p > .05 (one-tailed), systolic the possible psychological and physiological mediators of the blood pressure, r(136) = –.10, p > .05 (one-tailed), or beliefs effect of age on interoceptive accuracy, before similar analyses (r(136) = –.04, p >.05; two-tailed). compared the relationship between these potential mediators Negative associations were observed between interocep- and interoceptive accuracy. tive accuracy and BMI, r(136) = –.19, p = .015, and beliefs, The existence of direct and indirect effects of age on inter- r(136) = –.232, p = .003 (one-tailed). A positive association oceptive accuracy was investigated using a parallel mediation was observed between interoceptive accuracy and systolic model in which BMI, gender, systolic blood pressure, accura- blood pressure, r(136) = .21, p = .008 (one-tailed). No associ- cy of beliefs about average heartrate, heartrate variability, ation was observed between interoception and heartrate vari- mean heartrate, and timing accuracy were entered as potential ability, r(136) = .06, p > .05, or resting heartrate, r(136) = mediators of the effect of age on interoception. Mediation –.10, p > .05 (one-tailed). modelling was carried out using the SPSS macro-script The results of the mediation model are illustrated in Fig. 2. (Process) provided by Hayes (2013) and Preacher and Hayes As can be seen, there was a significant effect of age on BMI, (2008). For indirect effects, 90% (one-tailed) bias-corrected heartrate variability, and performance on the timing control bootstrapped confidence intervals were calculated using task (as outlined above; all one-tailed). All other predictors 5,000 repetitions. This method was selected over the Sobel were non-significant (all p > .10). There were also significant (1982) method as the former does not require the assumption effects of BMI (b = –.15, SE =.09, p = .04), gender (b = –.34, of a normal distribution and simulation studies indicate higher SE =.17, p = .02), beliefs regarding average heartrate (b = power whilst controlling for Type one error rates –.22, SE = .08, p = .004) and systolic blood pressure (b = (MacKinnon, Lockwood, Hoffman, West, & Sheets, 2002; .19, SE =.08, p = .01) on interoception (all one-tailed). All Mackinnon, Lockwood, & Williams, 2004). As outlined by other predictors were non-significant (all p > .10). Of impor- Preacher and Hayes (2004), an indirect effect is significant if tance was the finding that age exerted a direct (i.e. unmediat- the confidence intervals for the indirect effect do not include ed) effect on interoception (direct effect = –.15, SE =.09, t = zero. For all analyses where directional hypotheses are made, 1.69, p = .047; one-tailed) and a small indirect effect on one-tailed p values are reported. Standardized coefficients are interoception mediated by the effect of BMI (b = –.039, SE reported in the mediation analysis. =.03, CI (–.982, –.004); one-tailed) despite no total indirect effect (b = –.06, SE =.05, CI(–1.12, .25). All other indirect Results and discussion effects were non-significant (e.g., confidence intervals includ- ed zero). The indirect effect of BMI accounted for 0.18 (18%) A small amount of randomly-distributed data were missing of the total effect between age and interoception (ab/c;see (0.74%; three blood pressure measurements, two belief esti- Jose, 2013), indicating partial mediation. mates, and one measure of heartrate variability and resting heartrate) and these missing values were imputed using mul- tiple imputation in SPSS. The Mersenne–Twister algorithm General discussion with a starting point fixed to 2,000,000 was utilised for ran- dom number generation. All variables were entered into the This set of studies aimed to examine variation in interoceptive model, the automatic method was selected, and all variables awareness and accuracy across the lifespan. In Study One, a were used as predictors. No participant had more than one negative relationship between age and interoceptive aware- missing data point. ness was observed; older participants rated their interoceptive Simple zero-order correlations revealed a significant nega- awareness as reduced. Building on this, Study Two examined tive association between interoceptive accuracy and age, cardiac interoceptive accuracy across the adult lifespan using r(136) = –.21 p = .008 (one-tailed). Correlations between in- an objective performance measure, demonstrating a negative teroceptive accuracy and timing performance, r(136) = .12, relationship between age and interoceptive accuracy. These 1198 Psychon Bull Rev (2018) 25:1193–1202 Fig. 2 Depicts the results of the mediation analysis. Mediation analysis accuracy; Fig. 2 centre), in addition to an indirect path from age to indicated a significant path from age to BMI, heartrate variability and interoception via BMI. The indirect path via BMI thus partially time perception ability (a path; the individual relationships between the mediated the effect of age on interoception. *Denotes significance at IVand the mediators; e.g., from age to BMI; Fig. 2 left), whilst significant the p < .05 level (one-tailed). BMI Body Mass Index; Gender Male or paths to interoceptive accuracy from BMI, gender, heartrate variability Female (0 or 1); Heartrate Variability variation in the time interval beliefs and time perception ability were also observed (b path; the between heartbeats; Mean HR The average second-by-second heartbeat relationship between the mediators and the DV controlling for other recorded over 60 seconds; Beliefs the error of participants’ estimates mediators and keeping the IV constant; e.g., from BMI to interoceptive regarding the average heartrate; Time Perception Performance on the time accuracy; Fig. 2 right). Most importantly, a direct effect of age on estimation task; Systolic Blood Pressure Taken whilst seated and mea- interoceptive accuracy was observed (c’ path; the relationship between sured in millimetres of mercury the IVand the DV controlling for the mediators; from age to interoceptive data confirm previously reported evidence suggesting a de- awareness and interoceptive accuracy (Garfinkel et al., cline in interoceptive accuracy in older adulthood (Khalsa 2015) mean that care must be taken in interpreting reduced et al., 2009), and go further to suggest that this decline con- awareness of interceptive signals as underlying the direct ef- tinues into both late and very late adulthood. fect of age on interoceptive accuracy. The results from Study Two highlight that the poor perfor- The relationship between age and performance on the in- mance observed in late adulthood is due to both a direct effect teroceptive accuracy and timing control tasks is worthy of of age on interoceptive accuracy and an indirect effect medi- note. Whereas the zero-order correlations indicated a similar ated by BMI, whereby age was associated with increased magnitude of the effect of ageing on performance of these BMI, which in turn, predicted reduced interoceptive accuracy. tasks, the results of the mediation analysis demonstrate that Therefore, it appears that changes in BMI partially mediate the the effects of ageing on interoceptive accuracy were not a relationship between age and interoception. Other physiolog- product of reduced timing/counting ability (Turgeon et al., ical and psychological changes such as heartrate variability, 2016; Wittmann, 2013), and are also likely not due to general resting heartrate, and time perception, previously associated problems with motivation or attention. Thus, although similar both with interoceptive accuracy (Knapp-Kline & Kline, age-related declines were observed across these tasks, the ef- 2005;O’Brien et al., 1998; Rouse et al., 1988; Wittmann, fects of age were independent. 2013) and increasing age (Franklin et al., 1997; St-Onge, The finding that interoception declines throughout the 2005; Umetani et al., 1998; Yashin et al., 2006), were not lifespan raises important questions regarding the extent to significant mediators of the age–interoception relationship. which interoception is related to the decline in socio- The partial mediation of the effect of age on interoceptive emotional competence and altered cognition observed in late accuracy by BMI provides some indication as to the mecha- adulthood (Murphy et al., 2017). For example, a body of re- nism by which ageing negatively impacts interoceptive accu- search indicates poorer emotion recognition (Ruffman et al., racy. However, the existence of a direct effect of age indicates 2008) and changes in risky decision making with advancing at least one further mechanism to be identified. Although the age (Sparrow & Spaniol, 2016). Crucially, these same abilities results of Study One demonstrated reduced awareness of in- have been linked to interoceptive accuracy (Dunn et al., teroceptive information with increasing age, previous reports 2010b; Füstös et al., 2013; Schandry, 1981; Sokol-Hessner of a dissociation between self-reported interoceptive et al., 2015; Terasawa et al., 2013;Werneretal., 2009; Psychon Bull Rev (2018) 25:1193–1202 1199 Wiens et al., 2000). Given the interrelatedness of these factors, interoceptive metacognition—particularly those with inflated determining the extent to which age-related changes in these beliefs regarding their ability—may utilise unreliable intero- abilities is predicted by interoception is an important aim for ceptive cues for gauging interoceptive states, placing them at future research. Moreover, if interoception does underlie ad- a greater risk of adverse health outcomes (e.g., dehydration). verse age-related cognitive change, then such evidence may In conclusion, Study One demonstrated a negative relation- inform interventions, such as interoceptive training (e.g., ship between age and interoceptive awareness. Study Two dem- Canales-Johnson et al., 2015; Schaefer, Egloff, Gerlach, & onstrated that the decline in interoceptive accuracy across the Witthöft, 2014; Schandry & Weitkunat, 1990) designed to lifespan continues into late and very late adulthood. A decline ameliorate undesirable effects of ageing on cognition and in interoceptive awareness and accuracy with increasing age socio-emotional competence. highlights the importance of understanding the relationship be- In comparison to the only other study examining the impact tween age-related changes in interoceptive ability and age- of older age on cardiac interoceptive accuracy (Khalsa et al., related changes in cognition and physical and mental health. 2009), the variance explained by age in the present study was Acknowledgements JM was supported by a doctoral studentship from modest. The difference in the size of the observed age effect the Economic and Social Research Council [1599941; ES/J500057/1]. could be because the present study quantified interoceptive ac- GB was supported by the Baily Thomas Trust. We gratefully acknowl- curacy using the heartbeat tracking task (Schandry, 1981), edge the help of Raluca Prepelita in the early stages of data collection. whereas Khalsa et al. (2009) utilised the heartbeat discrimination Open Access This article is distributed under the terms of the Creative procedure (Brener & Kluvitse, 1988; Whitehead et al., 1977). Commons Attribution 4.0 International License (http:// Whilst small to moderate correlations have been observed be- creativecommons.org/licenses/by/4.0/), which permits unrestricted use, tween these two tasks (Garfinkel et al., 2015; Knoll & Hodapp, distribution, and reproduction in any medium, provided you give appro- 1992; but see Phillips, Jones, Rieger, & Snell, 1999), the extent priate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. to which task differences impact the accurate measurement of interoceptive accuracy remains unknown. 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Psychonomic Bulletin & ReviewSpringer Journals

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