- Email: [email protected]
Attenuated interoceptive sensitivity in overweight and obese individuals
Eating Behaviors 15 (2014) 445–448
Contents lists available at ScienceDirect
Eating Behaviors
Attenuated interoceptive sensitivity in overweight and obese individuals Beate M. Herbert ⁎, Olga Pollatos ⁎⁎ Health Psychology, Institute of Psychology, University of Ulm, Germany
a r t i c l e
i n f o
Article history: Received 28 January 2014 Received in revised form 7 May 2014 Accepted 9 June 2014 Available online 17 June 2014 Keywords: Overweight Obesity Interoception Interoceptive sensitivity Food intake Insula
a b s t r a c t Objective: Perceiving internal signals of hunger and satiety is related to the regulation of food intake. Recent data suggest that interoception (perception of bodily signals) and interoceptive sensitivity (sensitivity for internal signals) might be a crucial variable for the regulation of behavior associated with feelings of satiety. It is yet unclear whether interoceptive sensitivity is altered in overweight and obese participants. Design and methods: We therefore examined interoceptive sensitivity among 75 overweight and obese women and men using a heartbeat detection task and compared them to normal weight controls. We hypothesized that overweight and obesity would be related to attenuated interoceptive sensitivity. Results: Interoceptive sensitivity was higher in normal weight participants as compared to overweight and obese participants. Additionally, we found a negative correlation coefficient between the BMI and interoceptive sensitivity in the overweight and obese group only. Conclusions: In accordance with our hypotheses, we found evidence for reduced interoceptive sensitivity in overweight and obese individuals. Interoceptive sensitivity presumably interacts with the regulation of food intake in everyday life in part by facilitating the detection of bodily changes accompanying satiety. Overweight and obese individuals might experience greater difficulties in accurately detecting such signals due to reduced interoceptive sensitivity. © 2014 Elsevier Ltd. All rights reserved.
1. Introduction There is an increasing prevalence of overweight and obesity in Western civilizations. This nutritional disorder is associated with numerous health risks including hypertension, respiratory disease, and diabetes mellitus. Perceiving bodily signals and discriminating between the sensations of hunger and satiety are crucial abilities for the regulation of food intake. Fassino, Pierò, Gramaglia, and Abbate-Daga (2004) highlighted that interoceptive awareness assessed by questionnaire was significantly reduced in eating disorders and obesity, thereby suggesting that interoceptive processes might be disturbed both in eating and weight disorders. The generation and perception (interoception) of internal states of bodily arousal are central to many theoretical accounts of emotion (e.g. Damasio, 1999; James, 1884). William James and Carl Lange (James, 1884) presented an influential psychological theory linking
⁎ Correspondence to: B.M. Herbert, Health Psychology, Institute of Psychology and Education, University of Ulm, Albert-Einstein-Allee 41, 89069 Ulm, Germany. Tel.: +49 731 31732; fax: +49 731 31739. ⁎⁎ Correspondence to: O. Pollatos, Health Psychology, Institute of Psychology and Education, University of Ulm, Albert-Einstein-Allee 41, 89069 Ulm, Germany. Tel.: +49 731 31730; fax: +49 731 31739. E-mail addresses: [email protected] (B.M. Herbert), [email protected] (O. Pollatos).
http://dx.doi.org/10.1016/j.eatbeh.2014.06.002 1471-0153/© 2014 Elsevier Ltd. All rights reserved.
somatic and viscero-afferent feedback to subjective emotional experience (feelings). This model argues that an emotive stimulus automatically initiates visceral, vascular or somatic reactions, e.g. changes in blood pressure or heart rate; and it is the perception of these bodily reactions that crucially constitutes the emotional component of experience. Refinements of this model include the notion of somatic markers, which represent involuntary changes in internal bodily state signaling stimulus significance to guide both emotional and cognitive behaviors (e.g. decision making) (Damasio, 1999). Such peripheral models of emotion led to an interest in individual differences in the perception and sensitivity to changes in internal bodily state. Today, there is evidence that primates have a distinct cortical image of homeostatic afferent activity that reflects all components of the physiological conditions of all tissues of the body. This suggests that all feelings from the body are represented in a phylogenetically new system that evolved from the afferent limb of the evolutionarily ancient, hierarchical homeostatic system that maintains the integrity of the body (Craig, 2004). Neuroanatomic evidence underscores the relevance of an “interoceptive neural network” in the brain comprising the somatosensory and somatomotor cortices, the insular cortex, cingulate cortex (ACC), and prefrontal cortices (ventromedial prefrontal cortex, dorsolateral prefrontal cortex; see Pollatos, Schandry, Auer, & Kaufmann, 2007). These structures are relevant for monitoring the internal emotional and viscerosensory state (Critchley, Corfield, Chandler, Mathias, & Dolan, 2000; Critchley et al., 2003), for emotion
446
B.M. Herbert, O. Pollatos / Eating Behaviors 15 (2014) 445–448
processing and reactivity (Phan, Wager, Taylor, & Liberzon, 2002), and the self-regulation of feelings and behavior (Bechara & Naqvi, 2004). Research on interoception of the cardiovascular (Critchley, Wiens, Rotshtein, Ohman, & Dolan, 2004; Pollatos, Kirsch, & Schandry, 2005a; Pollatos, Schandry, Auer, & Kaufmann, 2007) and the gastrointestinal system (Pardo et al., 2003) underscores that there are significant interindividual differences in interoceptive sensitivity (IS). Basic research on IS has predominantly focused on heartbeat perception and the individual sensitivity for cardiac signals (“cardiac awareness”). This sensitivity has been most usually quantified by using validated and reliable heartbeat perception tasks (Jones, 1994; Jones, Leonberger, Rouse, Caldwell, & Jones, 1986; Wildman & Jones, 1982) such as “tracking” (Schandry, 1981) or “discrimination tasks” (Knapp, Ring, & Brener, 1997; Whitehead & Drescher, 1980). In these tasks participants are instructed to perceive their own heartbeats without feeling for their pulse. They allow calculating individual heartbeat perception scores that characterize the deviation of the subjectively felt cardiac signal from the objective cardiac signal. The individual degree of IS can be conceptualized as a trait-like sensitivity toward one's visceral signals. And, the perceptibility of visceral, cardiac signals can also be manipulated by procedures that evoke changes in autonomic cardiovascular activity (Herbert et al., 2012; Schandry, Bestler, & Montoya, 1993). Differences in IS are related with both reported emotional experience, and corresponding psychophysiological markers of emotion processing (Dunn et al., 2010; Pollatos, Gramann, & Schandry, 2007; Pollatos, Kirsch, & Schandry, 2005b). Moreover the strength of correspondence between cognitive–affective processing and bodily reactions depends on whether individuals can perceive bodily changes well — or not (Dunn et al., 2010). Two recent studies clearly link interoceptive sensitivity across different inner systems and highlight its importance for sensing signals of fullness and everyday eating behavior: Herbert, Muth, Pollatos, and Herbert (in press) demonstrated that participants with higher interoceptive sensitivity as assessed by heartbeat perception ingested significantly lower amount of water in a free drinking paradigm (waterload test) (Herbert et al., in press). This result indicates that interoceptive sensitivity as assessed by heartbeat perception is related to gastric sensitivity. In another recent work (Herbert, Blechert, Hautzinger, Matthias, & Herbert, 2013) it could also be demonstrated that eating primarily according to one's bodily cues – which reflects a major aspect of intuitive eating behavior – is significantly associated with interoceptive sensitivity. These findings suggest that in healthy persons there is a relevant overlap between gastric and cardiac sensitivities. While there is first evidence that interoceptive sensitivity is reduced in anorexia nervosa (Pollatos et al., 2008), there is to our knowledge no empirical study assessing interoceptive sensitivity in overweight and obese participants. Our objective was to examine interoceptive sensitivity among overweight and obese women and men using a heartbeat detection task. We hypothesized that overweight and obesity would be related to reduced interoceptive sensitivity. 2. Methods 2.1. Participants 55 overweight and obese (body mass index [BMI] N 25 kg/m2) female (mean age (M ± SD yrs) 25.1 ± 4.5) and 20 overweight and obese male students (mean age (M ± SD yrs) 25.6 ± 4.6) were recruited from introductory psychology and medicine courses and by advertising announcements at the universities of Potsdam and Tuebingen from 2010 to 2012. All participants were screened for health status using a questionnaire. Participants were excluded if they had a history of eating disorders, disturbed eating behavior, and any common psychiatric disorder, in particular anxiety disorders or depression (or any other axis 1 disorders) according to the Diagnostic and Statistical Manual of Mental
Disorders (American Psychiatric Association, 1994). Drug use (except contraceptives) was also an exclusion criterion. Weight and height were assessed. The mean BMI was 27.2 ± 2.0 kg/m2 (females 27.2 ± 1.9 kg/m2, males 27.4 ± 2.3 kg/m2). Normal weight (18.5 b [BMI] N 25 kg/m2) females (mean age (M ± SD yrs) 23.9 ± 4.6) and males (25.8 ± 5.1) were consecutively recruited and matched concerning age and sex for each of the overweight participants. Ethical approval from local ethic boards was obtained. All participants gave their written informed consent. Experiments were conducted in accordance with the Declaration of Helsinki. 2.2. Procedure outline Upon arrival at the laboratory rooms in the Department of Psychology either at the University of Potsdam or at the University of Tuebingen, equipment for heart rate (electrocardiography; ECG) was attached using a portable BIOPAC system (Biopac MP150, version 2.7.2.). Then, interoceptive sensitivity was assessed using four heartbeat counting phases (varying in length) in accordance with the Mental Tracking Method suggested by Schandry (see e.g. (Pollatos et al., 2008). Participants were asked to count their own heartbeats silently and to verbally report the number of counted heartbeats at the end of the counting phase. The beginning and the end of the counting intervals were signaled acoustically. Interoceptive sensitivity was estimated as the mean heartbeat perception score according to the following transformation: 1
. X 4
ð1−ðjrecorded heartbeats−counted heartbeatsjÞ=recorded heartbeatsÞ:
Heart rate during the heartbeat counting phase was assessed and averaged across a time interval of 5 min. 2.3. Data analyses We calculated ANOVAs with two levels of Group (overweight/normal weight) and two levels of Sex (females/males) focusing on group differences in interoceptive sensitivity and heart rate. In a second step, Pearson correlations were assessed between interoceptive sensitivity, BMI and heart rate in both groups. 3. Results 3.1. Interoceptive sensitivity contrasting overweight and normal weight groups Mean interoceptive sensitivity scores contrasting overweight and obese males and females and corresponding normal weight controls are depicted in Fig. 1. We observed a significant main effect of Group (F(1,146) = 10.25, p b .01, η2 = .07, ε = .89) indicating higher interoceptive sensitivity in normal weight participants (mean 0.72 ± 0.13) as compared to overweight and obese participants (mean 0.62 ± 0.19). No significant main effect of sex and no significant interaction of sex × group were observed. Scatter plots depict the Pearson correlation coefficients contrasting both groups (Fig. 2). While there was no significant correlation between the BMI and the interoceptive sensitivity score in the normal weight group (r = .09, p = .42), an inverse correlation was found in the overweight and obese group (r = −.43, p b .001). 3.2. Heart rate and interoceptive sensitivity contrasting overweight and normal weight groups The mean heart rate was 68.0 bpm (SD 10.3) in the overweight and obese group as compared to 65.8 (SD 13.6) in the normal weight
B.M. Herbert, O. Pollatos / Eating Behaviors 15 (2014) 445–448
447
1
*
Interoceptive Sensitivity
0,9
*
0,8
normal weight
0,7
overweight
0,6
0,5
0,4
females
males
Fig. 1. Mean interoceptive sensitivity scores for male and female normal weight and overweight/obese participants.
controls. There was no significant effect of Group (F(1,146) = 1.98, p = .16) indicating that the observed heart rate difference was not significant. We observed a significant effect of Sex (F(1,146) = 6.38, p b .05, η2 = .04, ε = .71): men had a lower heart rate (mean 62.9) as
compared to women (mean 68.4). No other significant main or interaction effect occurred. Additionally, we calculated Pearson correlation coefficients between heart rate and interoceptive sensitivity contrasting both groups. Concerning the normal weight group, we observed a non-significant correlation of r = − .09 (p = .43) between heart rate and BMI and a non-significant correlation of r = − .07 (p = .56) between heart rate and interoceptive sensitivity. The overweight and obese group did also exhibit no significant correlations between heart rate and BMI (r = .01, p = .98) as well as heart rate and interoceptive sensitivity (r = .09, p = .42). 4. Discussion
Fig. 2. Scatter plots depicting the relationship between interoceptive sensitivity and the BMI contrasting normal weight and overweight/obese participants.
In accordance with our hypotheses, we found evidence for reduced interoceptive sensitivity in overweight and obese individuals. These differences were accompanied by an inverse correlation between the BMI and the interoceptive sensitivity score in overweight and obese participants, while no such relationship was observed for normal weight range. The mean heart rate between both groups did not differ significantly, nor was there a significant relationship between heart rate and interoceptive sensitivity, ruling out the possibility that baseline differences in heart rate account for the observed group differences in interoceptive sensitivity. We interpret our findings as showing that individuals with overweight and obesity have poorer detection ability for internal signals, and that more pronounced overweight is associated with poorer interoceptive sensitivity. To our knowledge, this study is the first that could demonstrate that interoceptive sensitivity is reduced in overweight and obese participants, suggesting that interoceptive sensitivity should be taken into account as an important variable for the etiology or maintenance of weight problems. Favoring the idea that feelings of hunger and satiety respectively their conscious perception might be associated with the sensitivity for cardiac signals Herbert et al. (2013) reported a significant positive correlation between intuitive eating and interoceptive sensitivity as assessed by heartbeat perception. In accordance to this assumption there is empirical evidence showing that the conscious perception of one's internal signals referring to satiety cues – assessed by the construct of “intuitive eating” behavior as measured by self-report scales – is significantly associated with one's body weight/BMI ((Gast, Madanat, & Nielson, 2012; Herbert et al., 2013). Persons who report to eat according to their bodily sensations are less likely to overindulge in food in the absence of hunger and to allow emotional or situational cues guide their food intake (Birch, Fisher, & Davison, 2003).
448
B.M. Herbert, O. Pollatos / Eating Behaviors 15 (2014) 445–448
We therefore follow that interoceptive sensitivity interacts with the regulation of food intake in everyday life in part by facilitating the detection of bodily changes accompanying satiety or fullness. There is clear evidence that interoception of inputs from different organ systems like the cardiovascular system and the gastrointestinal system is interconnected (Herbert et al., in press; Whitehead & Drescher, 1980). In accordance to this we assume that overweight and obese individuals experience greater difficulties in accurately detecting such signals as they also show a reduced sensitivity for cardiac signals. 5. Conclusions Our study provides the first empirical evidence that interoceptive sensitivity and associated activation of interoceptive representations and meta-representations of bodily signals profoundly interact with overweight and obesity. Importantly, the overweight and obese group exhibited pronounced difficulties in detecting internal signals which has been shown for other clinical samples such as anorectic females (Pollatos et al., 2008), depressive (Dunn, Dalgleish, Ogilvie, & Lawrence, 2007) or somatoform patients (Pollatos et al., 2011). Reduced interoceptive sensitivity is assumedly associated with difficulties in the consolidation of somatic markers required for guiding individual behavior by signaling stimulus significance to the body as proposed in the somatic marker theory by Damasio, 1999. It could be hypothesized that a low level of interoceptive sensitivity hampers processes of emotional learning and emotional experience. Possible limitations of this study refer to the fact that a student sample was assessed, that the participants' number was rather small and that only the BMI was assessed. For this reason, assessing interoceptive sensitivity in greater samples might be a powerful approach to provide ideas for novel therapeutic interventions, e.g. based on interoceptive sensitivity training. Role of funding source The study was partly funded by University grants to OP. Contributors OP and BH participated in the study design and the sampling of the data. OP performed the statistical analysis. OP and BH drafted the manuscript. All authors read and approved the final manuscript. Conflict of interest No confict of interests exist. Acknowledgments We would like to thank Jennifer Meyer, Kevin Görsch, Alexander Dreyer and Julia Schneider for their support in data assessment and data processing.
References American Psychiatric Association (1994). Diagnostic and statistical manual for mental disorders (4th ed.). Washington: APA Press (DSM-IV). Bechara, A., & Naqvi, N. (2004). Listening to your heart: Interoceptive awareness as a gateway to feeling. Nature Neuroscience, 7, 102–103. Birch, L. L., Fisher, J. O., & Davison, K. K. (2003). Learning to overeat: Maternal use of restrictive feeding practices promotes girls' eating in the absence of hunger. The American Journal of Clinical Nutrition, 78, 215–220. Craig, A.D. (2004). Human feelings: Why are some more aware than others? Trends in Cognitive Science, 8, 239–241.
Critchley, H. D., Corfield, D. R., Chandler, M. P., Mathias, C. J., & Dolan, R. J. (2000). Cerebral correlates of autonomic cardiovascular arousal: A functional neuroimaging investigation in humans. The Journal of Physiology, 523, 259–270. Critchley, H. D., Mathias, C. J., Josephs, O., O'Doherty, J., Zanini, S., Dewar, B. K., et al. (2003). Human cingulate cortex and autonomic control: Converging neuroimaging and clinical evidence. Brain, 126, 2139–2152. Critchley, H. D., Wiens, S., Rotshtein, P., Ohman, A., & Dolan, R. J. (2004). Neural systems supporting interoceptive awareness. Nature Neuroscience, 7, 189–195. Damasio, A.R. (1999). The feeling of what happens: Body and emotion in the making of consciousness. New York: Harcourt Brace. Dunn, B.D., Dalgleish, T., Ogilvie, A.D., & Lawrence, A.D. (2007). Heartbeat perception in depression. Behaviour Research and Therapy, 45, 1921–1930. Dunn, B.D., Galton, H. C., Morgan, R., Evans, D., Oliver, C., Meyer, M., et al. (2010). Listening to your heart: How interoception shapes emotion experience and intuitive decision making. Psychological Science, 21, 1835–1844. Fassino, S., Pierò, A., Gramaglia, C., & Abbate-Daga, G. (2004). Clinical, psychopathological and personality correlates of interoceptive awareness in anorexia nervosa, bulimia nervosa and obesity. Psychopathology, 37, 168–174. Gast, J., Madanat, H., & Nielson, A.C. (2012). Are men more intuitive when it comes to eating and physical activity? American Journal of Men's Health, 6, 164–171. Herbert, B.M., Blechert, J., Hautzinger, M., Matthias, E., & Herbert, C. (2013). Intuitive eating is associated with interoceptive sensitivity. Effects on body mass index? Appetite, 70, 22–30. Herbert, B.M., Herbert, C., Pollatos, O., Weimer, K., Enck, P., Sauer, H., et al. (2012). Effects of short-term food deprivation on interoceptive awareness, feelings and autonomic cardiac activity. Biological Psychology, 89, 71–79. Herbert, B.M., Muth, E. R., Pollatos, O., & Herbert, C. (2012). Interoception across modalities: On the relationship between cardiac awareness and the sensitivity for gastric functions. PLoS ONE, 7, e36646. James, W. (1884). What is an emotion? Mind, 9, 188–205. Jones, G. E. (1994). Perception of visceral sensations: A review of recent findings, methodologies, and future directions. In J. R. Jennings, & P. K. Ackles (Eds.), Advances in psychophysiology, Vol. 5, London: Jessica Kingsley Publishers. Jones, G. E., Leonberger, T. F., Rouse, C. H., Caldwell, J. A., & Jones, K. R. (1986). Preliminary data exploring the presence of an evoked potential associated with cardiac visceral activity. Psychophysiology, 23. Knapp, K., Ring, C., & Brener, J. (1997). Sensitivity to mechanical stimuli and the role of general sensory and perceptual processes in heartbeat detection. Psychophysiology, 34, 467–473. Pardo, S. E., Faris, P. L., Hartman, B. K., Kim, S. W., Ivanov, E. H., Daughters, R. S., et al. (2003). Functional neuroimaging of gastric distention. Journal of General Psychology, 7, 740–749. Phan, K. L., Wager, T., Taylor, S. F., & Liberzon, I. (2002). Functional neuroanatomy of emotion: A meta-analysis of emotion activation studies in PET and fMRI. NeuroImage, 16, 331–348. Pollatos, O., Gramann, K., & Schandry, R. (2007). Neural systems connecting interoceptive awareness and feelings. Human Brain Mapping, 28, 9–18. Pollatos, O., Herbert, B.M., Wankner, S., Dietel, A., Wachsmuth, C., Henningsen, P., et al. (2011). Autonomic imbalance is associated with reduced facial recognition in somatoform disorders. Journal of Psychosomatic Research, 71, 232–239. Pollatos, O., Kirsch, W., & Schandry, R. (2005a). Brain structures involved in interoceptive awareness and cardioafferent signal processing: A dipole source localization study. Human Brain Mapping, 26, 54–64. Pollatos, O., Kirsch, W., & Schandry, R. (2005b). On the relationship between interoceptive awareness, emotional experience, and brain processes. Cognitive Brain Research, 25, 948–962. Pollatos, O., Kurz, A. L., Albrecht, J., Schreder, T., Kleemann, A.M., Schöpf, V., et al. (2008). Reduced perception of bodily signals in anorexia nervosa. Eating Behaviors, 9, 381–388. Pollatos, O., Schandry, R., Auer, D. P., & Kaufmann, C. (2007). Brain structures mediating cardiovascular arousal and interoceptive awareness. Brain Research, 1141, 178–187. Schandry, R. (1981). Heart beat perception and emotional experience. Psychophysiology, 18, 483–488. Schandry, R., Bestler, M., & Montoya, P. (1993). On the relation between cardiodynamics and heartbeat perception. Psychophysiology, 30, 467–474. Whitehead, W. E., & Drescher, V. M. (1980). Perception of gastric contractions and selfcontrol of gastric motility. Psychophysiology, 17, 552–558. Wildman, H. E., & Jones, G. E. (1982). Consistency of heartbeat discrimination scores on the Whitehead procedure in knowledge-of-results — Trained and untrained subjects. Psychophysiology, 19, 592.
Contents lists available at ScienceDirect
Eating Behaviors
Attenuated interoceptive sensitivity in overweight and obese individuals Beate M. Herbert ⁎, Olga Pollatos ⁎⁎ Health Psychology, Institute of Psychology, University of Ulm, Germany
a r t i c l e
i n f o
Article history: Received 28 January 2014 Received in revised form 7 May 2014 Accepted 9 June 2014 Available online 17 June 2014 Keywords: Overweight Obesity Interoception Interoceptive sensitivity Food intake Insula
a b s t r a c t Objective: Perceiving internal signals of hunger and satiety is related to the regulation of food intake. Recent data suggest that interoception (perception of bodily signals) and interoceptive sensitivity (sensitivity for internal signals) might be a crucial variable for the regulation of behavior associated with feelings of satiety. It is yet unclear whether interoceptive sensitivity is altered in overweight and obese participants. Design and methods: We therefore examined interoceptive sensitivity among 75 overweight and obese women and men using a heartbeat detection task and compared them to normal weight controls. We hypothesized that overweight and obesity would be related to attenuated interoceptive sensitivity. Results: Interoceptive sensitivity was higher in normal weight participants as compared to overweight and obese participants. Additionally, we found a negative correlation coefficient between the BMI and interoceptive sensitivity in the overweight and obese group only. Conclusions: In accordance with our hypotheses, we found evidence for reduced interoceptive sensitivity in overweight and obese individuals. Interoceptive sensitivity presumably interacts with the regulation of food intake in everyday life in part by facilitating the detection of bodily changes accompanying satiety. Overweight and obese individuals might experience greater difficulties in accurately detecting such signals due to reduced interoceptive sensitivity. © 2014 Elsevier Ltd. All rights reserved.
1. Introduction There is an increasing prevalence of overweight and obesity in Western civilizations. This nutritional disorder is associated with numerous health risks including hypertension, respiratory disease, and diabetes mellitus. Perceiving bodily signals and discriminating between the sensations of hunger and satiety are crucial abilities for the regulation of food intake. Fassino, Pierò, Gramaglia, and Abbate-Daga (2004) highlighted that interoceptive awareness assessed by questionnaire was significantly reduced in eating disorders and obesity, thereby suggesting that interoceptive processes might be disturbed both in eating and weight disorders. The generation and perception (interoception) of internal states of bodily arousal are central to many theoretical accounts of emotion (e.g. Damasio, 1999; James, 1884). William James and Carl Lange (James, 1884) presented an influential psychological theory linking
⁎ Correspondence to: B.M. Herbert, Health Psychology, Institute of Psychology and Education, University of Ulm, Albert-Einstein-Allee 41, 89069 Ulm, Germany. Tel.: +49 731 31732; fax: +49 731 31739. ⁎⁎ Correspondence to: O. Pollatos, Health Psychology, Institute of Psychology and Education, University of Ulm, Albert-Einstein-Allee 41, 89069 Ulm, Germany. Tel.: +49 731 31730; fax: +49 731 31739. E-mail addresses: [email protected] (B.M. Herbert), [email protected] (O. Pollatos).
http://dx.doi.org/10.1016/j.eatbeh.2014.06.002 1471-0153/© 2014 Elsevier Ltd. All rights reserved.
somatic and viscero-afferent feedback to subjective emotional experience (feelings). This model argues that an emotive stimulus automatically initiates visceral, vascular or somatic reactions, e.g. changes in blood pressure or heart rate; and it is the perception of these bodily reactions that crucially constitutes the emotional component of experience. Refinements of this model include the notion of somatic markers, which represent involuntary changes in internal bodily state signaling stimulus significance to guide both emotional and cognitive behaviors (e.g. decision making) (Damasio, 1999). Such peripheral models of emotion led to an interest in individual differences in the perception and sensitivity to changes in internal bodily state. Today, there is evidence that primates have a distinct cortical image of homeostatic afferent activity that reflects all components of the physiological conditions of all tissues of the body. This suggests that all feelings from the body are represented in a phylogenetically new system that evolved from the afferent limb of the evolutionarily ancient, hierarchical homeostatic system that maintains the integrity of the body (Craig, 2004). Neuroanatomic evidence underscores the relevance of an “interoceptive neural network” in the brain comprising the somatosensory and somatomotor cortices, the insular cortex, cingulate cortex (ACC), and prefrontal cortices (ventromedial prefrontal cortex, dorsolateral prefrontal cortex; see Pollatos, Schandry, Auer, & Kaufmann, 2007). These structures are relevant for monitoring the internal emotional and viscerosensory state (Critchley, Corfield, Chandler, Mathias, & Dolan, 2000; Critchley et al., 2003), for emotion
446
B.M. Herbert, O. Pollatos / Eating Behaviors 15 (2014) 445–448
processing and reactivity (Phan, Wager, Taylor, & Liberzon, 2002), and the self-regulation of feelings and behavior (Bechara & Naqvi, 2004). Research on interoception of the cardiovascular (Critchley, Wiens, Rotshtein, Ohman, & Dolan, 2004; Pollatos, Kirsch, & Schandry, 2005a; Pollatos, Schandry, Auer, & Kaufmann, 2007) and the gastrointestinal system (Pardo et al., 2003) underscores that there are significant interindividual differences in interoceptive sensitivity (IS). Basic research on IS has predominantly focused on heartbeat perception and the individual sensitivity for cardiac signals (“cardiac awareness”). This sensitivity has been most usually quantified by using validated and reliable heartbeat perception tasks (Jones, 1994; Jones, Leonberger, Rouse, Caldwell, & Jones, 1986; Wildman & Jones, 1982) such as “tracking” (Schandry, 1981) or “discrimination tasks” (Knapp, Ring, & Brener, 1997; Whitehead & Drescher, 1980). In these tasks participants are instructed to perceive their own heartbeats without feeling for their pulse. They allow calculating individual heartbeat perception scores that characterize the deviation of the subjectively felt cardiac signal from the objective cardiac signal. The individual degree of IS can be conceptualized as a trait-like sensitivity toward one's visceral signals. And, the perceptibility of visceral, cardiac signals can also be manipulated by procedures that evoke changes in autonomic cardiovascular activity (Herbert et al., 2012; Schandry, Bestler, & Montoya, 1993). Differences in IS are related with both reported emotional experience, and corresponding psychophysiological markers of emotion processing (Dunn et al., 2010; Pollatos, Gramann, & Schandry, 2007; Pollatos, Kirsch, & Schandry, 2005b). Moreover the strength of correspondence between cognitive–affective processing and bodily reactions depends on whether individuals can perceive bodily changes well — or not (Dunn et al., 2010). Two recent studies clearly link interoceptive sensitivity across different inner systems and highlight its importance for sensing signals of fullness and everyday eating behavior: Herbert, Muth, Pollatos, and Herbert (in press) demonstrated that participants with higher interoceptive sensitivity as assessed by heartbeat perception ingested significantly lower amount of water in a free drinking paradigm (waterload test) (Herbert et al., in press). This result indicates that interoceptive sensitivity as assessed by heartbeat perception is related to gastric sensitivity. In another recent work (Herbert, Blechert, Hautzinger, Matthias, & Herbert, 2013) it could also be demonstrated that eating primarily according to one's bodily cues – which reflects a major aspect of intuitive eating behavior – is significantly associated with interoceptive sensitivity. These findings suggest that in healthy persons there is a relevant overlap between gastric and cardiac sensitivities. While there is first evidence that interoceptive sensitivity is reduced in anorexia nervosa (Pollatos et al., 2008), there is to our knowledge no empirical study assessing interoceptive sensitivity in overweight and obese participants. Our objective was to examine interoceptive sensitivity among overweight and obese women and men using a heartbeat detection task. We hypothesized that overweight and obesity would be related to reduced interoceptive sensitivity. 2. Methods 2.1. Participants 55 overweight and obese (body mass index [BMI] N 25 kg/m2) female (mean age (M ± SD yrs) 25.1 ± 4.5) and 20 overweight and obese male students (mean age (M ± SD yrs) 25.6 ± 4.6) were recruited from introductory psychology and medicine courses and by advertising announcements at the universities of Potsdam and Tuebingen from 2010 to 2012. All participants were screened for health status using a questionnaire. Participants were excluded if they had a history of eating disorders, disturbed eating behavior, and any common psychiatric disorder, in particular anxiety disorders or depression (or any other axis 1 disorders) according to the Diagnostic and Statistical Manual of Mental
Disorders (American Psychiatric Association, 1994). Drug use (except contraceptives) was also an exclusion criterion. Weight and height were assessed. The mean BMI was 27.2 ± 2.0 kg/m2 (females 27.2 ± 1.9 kg/m2, males 27.4 ± 2.3 kg/m2). Normal weight (18.5 b [BMI] N 25 kg/m2) females (mean age (M ± SD yrs) 23.9 ± 4.6) and males (25.8 ± 5.1) were consecutively recruited and matched concerning age and sex for each of the overweight participants. Ethical approval from local ethic boards was obtained. All participants gave their written informed consent. Experiments were conducted in accordance with the Declaration of Helsinki. 2.2. Procedure outline Upon arrival at the laboratory rooms in the Department of Psychology either at the University of Potsdam or at the University of Tuebingen, equipment for heart rate (electrocardiography; ECG) was attached using a portable BIOPAC system (Biopac MP150, version 2.7.2.). Then, interoceptive sensitivity was assessed using four heartbeat counting phases (varying in length) in accordance with the Mental Tracking Method suggested by Schandry (see e.g. (Pollatos et al., 2008). Participants were asked to count their own heartbeats silently and to verbally report the number of counted heartbeats at the end of the counting phase. The beginning and the end of the counting intervals were signaled acoustically. Interoceptive sensitivity was estimated as the mean heartbeat perception score according to the following transformation: 1
. X 4
ð1−ðjrecorded heartbeats−counted heartbeatsjÞ=recorded heartbeatsÞ:
Heart rate during the heartbeat counting phase was assessed and averaged across a time interval of 5 min. 2.3. Data analyses We calculated ANOVAs with two levels of Group (overweight/normal weight) and two levels of Sex (females/males) focusing on group differences in interoceptive sensitivity and heart rate. In a second step, Pearson correlations were assessed between interoceptive sensitivity, BMI and heart rate in both groups. 3. Results 3.1. Interoceptive sensitivity contrasting overweight and normal weight groups Mean interoceptive sensitivity scores contrasting overweight and obese males and females and corresponding normal weight controls are depicted in Fig. 1. We observed a significant main effect of Group (F(1,146) = 10.25, p b .01, η2 = .07, ε = .89) indicating higher interoceptive sensitivity in normal weight participants (mean 0.72 ± 0.13) as compared to overweight and obese participants (mean 0.62 ± 0.19). No significant main effect of sex and no significant interaction of sex × group were observed. Scatter plots depict the Pearson correlation coefficients contrasting both groups (Fig. 2). While there was no significant correlation between the BMI and the interoceptive sensitivity score in the normal weight group (r = .09, p = .42), an inverse correlation was found in the overweight and obese group (r = −.43, p b .001). 3.2. Heart rate and interoceptive sensitivity contrasting overweight and normal weight groups The mean heart rate was 68.0 bpm (SD 10.3) in the overweight and obese group as compared to 65.8 (SD 13.6) in the normal weight
B.M. Herbert, O. Pollatos / Eating Behaviors 15 (2014) 445–448
447
1
*
Interoceptive Sensitivity
0,9
*
0,8
normal weight
0,7
overweight
0,6
0,5
0,4
females
males
Fig. 1. Mean interoceptive sensitivity scores for male and female normal weight and overweight/obese participants.
controls. There was no significant effect of Group (F(1,146) = 1.98, p = .16) indicating that the observed heart rate difference was not significant. We observed a significant effect of Sex (F(1,146) = 6.38, p b .05, η2 = .04, ε = .71): men had a lower heart rate (mean 62.9) as
compared to women (mean 68.4). No other significant main or interaction effect occurred. Additionally, we calculated Pearson correlation coefficients between heart rate and interoceptive sensitivity contrasting both groups. Concerning the normal weight group, we observed a non-significant correlation of r = − .09 (p = .43) between heart rate and BMI and a non-significant correlation of r = − .07 (p = .56) between heart rate and interoceptive sensitivity. The overweight and obese group did also exhibit no significant correlations between heart rate and BMI (r = .01, p = .98) as well as heart rate and interoceptive sensitivity (r = .09, p = .42). 4. Discussion
Fig. 2. Scatter plots depicting the relationship between interoceptive sensitivity and the BMI contrasting normal weight and overweight/obese participants.
In accordance with our hypotheses, we found evidence for reduced interoceptive sensitivity in overweight and obese individuals. These differences were accompanied by an inverse correlation between the BMI and the interoceptive sensitivity score in overweight and obese participants, while no such relationship was observed for normal weight range. The mean heart rate between both groups did not differ significantly, nor was there a significant relationship between heart rate and interoceptive sensitivity, ruling out the possibility that baseline differences in heart rate account for the observed group differences in interoceptive sensitivity. We interpret our findings as showing that individuals with overweight and obesity have poorer detection ability for internal signals, and that more pronounced overweight is associated with poorer interoceptive sensitivity. To our knowledge, this study is the first that could demonstrate that interoceptive sensitivity is reduced in overweight and obese participants, suggesting that interoceptive sensitivity should be taken into account as an important variable for the etiology or maintenance of weight problems. Favoring the idea that feelings of hunger and satiety respectively their conscious perception might be associated with the sensitivity for cardiac signals Herbert et al. (2013) reported a significant positive correlation between intuitive eating and interoceptive sensitivity as assessed by heartbeat perception. In accordance to this assumption there is empirical evidence showing that the conscious perception of one's internal signals referring to satiety cues – assessed by the construct of “intuitive eating” behavior as measured by self-report scales – is significantly associated with one's body weight/BMI ((Gast, Madanat, & Nielson, 2012; Herbert et al., 2013). Persons who report to eat according to their bodily sensations are less likely to overindulge in food in the absence of hunger and to allow emotional or situational cues guide their food intake (Birch, Fisher, & Davison, 2003).
448
B.M. Herbert, O. Pollatos / Eating Behaviors 15 (2014) 445–448
We therefore follow that interoceptive sensitivity interacts with the regulation of food intake in everyday life in part by facilitating the detection of bodily changes accompanying satiety or fullness. There is clear evidence that interoception of inputs from different organ systems like the cardiovascular system and the gastrointestinal system is interconnected (Herbert et al., in press; Whitehead & Drescher, 1980). In accordance to this we assume that overweight and obese individuals experience greater difficulties in accurately detecting such signals as they also show a reduced sensitivity for cardiac signals. 5. Conclusions Our study provides the first empirical evidence that interoceptive sensitivity and associated activation of interoceptive representations and meta-representations of bodily signals profoundly interact with overweight and obesity. Importantly, the overweight and obese group exhibited pronounced difficulties in detecting internal signals which has been shown for other clinical samples such as anorectic females (Pollatos et al., 2008), depressive (Dunn, Dalgleish, Ogilvie, & Lawrence, 2007) or somatoform patients (Pollatos et al., 2011). Reduced interoceptive sensitivity is assumedly associated with difficulties in the consolidation of somatic markers required for guiding individual behavior by signaling stimulus significance to the body as proposed in the somatic marker theory by Damasio, 1999. It could be hypothesized that a low level of interoceptive sensitivity hampers processes of emotional learning and emotional experience. Possible limitations of this study refer to the fact that a student sample was assessed, that the participants' number was rather small and that only the BMI was assessed. For this reason, assessing interoceptive sensitivity in greater samples might be a powerful approach to provide ideas for novel therapeutic interventions, e.g. based on interoceptive sensitivity training. Role of funding source The study was partly funded by University grants to OP. Contributors OP and BH participated in the study design and the sampling of the data. OP performed the statistical analysis. OP and BH drafted the manuscript. All authors read and approved the final manuscript. Conflict of interest No confict of interests exist. Acknowledgments We would like to thank Jennifer Meyer, Kevin Görsch, Alexander Dreyer and Julia Schneider for their support in data assessment and data processing.
References American Psychiatric Association (1994). Diagnostic and statistical manual for mental disorders (4th ed.). Washington: APA Press (DSM-IV). Bechara, A., & Naqvi, N. (2004). Listening to your heart: Interoceptive awareness as a gateway to feeling. Nature Neuroscience, 7, 102–103. Birch, L. L., Fisher, J. O., & Davison, K. K. (2003). Learning to overeat: Maternal use of restrictive feeding practices promotes girls' eating in the absence of hunger. The American Journal of Clinical Nutrition, 78, 215–220. Craig, A.D. (2004). Human feelings: Why are some more aware than others? Trends in Cognitive Science, 8, 239–241.
Critchley, H. D., Corfield, D. R., Chandler, M. P., Mathias, C. J., & Dolan, R. J. (2000). Cerebral correlates of autonomic cardiovascular arousal: A functional neuroimaging investigation in humans. The Journal of Physiology, 523, 259–270. Critchley, H. D., Mathias, C. J., Josephs, O., O'Doherty, J., Zanini, S., Dewar, B. K., et al. (2003). Human cingulate cortex and autonomic control: Converging neuroimaging and clinical evidence. Brain, 126, 2139–2152. Critchley, H. D., Wiens, S., Rotshtein, P., Ohman, A., & Dolan, R. J. (2004). Neural systems supporting interoceptive awareness. Nature Neuroscience, 7, 189–195. Damasio, A.R. (1999). The feeling of what happens: Body and emotion in the making of consciousness. New York: Harcourt Brace. Dunn, B.D., Dalgleish, T., Ogilvie, A.D., & Lawrence, A.D. (2007). Heartbeat perception in depression. Behaviour Research and Therapy, 45, 1921–1930. Dunn, B.D., Galton, H. C., Morgan, R., Evans, D., Oliver, C., Meyer, M., et al. (2010). Listening to your heart: How interoception shapes emotion experience and intuitive decision making. Psychological Science, 21, 1835–1844. Fassino, S., Pierò, A., Gramaglia, C., & Abbate-Daga, G. (2004). Clinical, psychopathological and personality correlates of interoceptive awareness in anorexia nervosa, bulimia nervosa and obesity. Psychopathology, 37, 168–174. Gast, J., Madanat, H., & Nielson, A.C. (2012). Are men more intuitive when it comes to eating and physical activity? American Journal of Men's Health, 6, 164–171. Herbert, B.M., Blechert, J., Hautzinger, M., Matthias, E., & Herbert, C. (2013). Intuitive eating is associated with interoceptive sensitivity. Effects on body mass index? Appetite, 70, 22–30. Herbert, B.M., Herbert, C., Pollatos, O., Weimer, K., Enck, P., Sauer, H., et al. (2012). Effects of short-term food deprivation on interoceptive awareness, feelings and autonomic cardiac activity. Biological Psychology, 89, 71–79. Herbert, B.M., Muth, E. R., Pollatos, O., & Herbert, C. (2012). Interoception across modalities: On the relationship between cardiac awareness and the sensitivity for gastric functions. PLoS ONE, 7, e36646. James, W. (1884). What is an emotion? Mind, 9, 188–205. Jones, G. E. (1994). Perception of visceral sensations: A review of recent findings, methodologies, and future directions. In J. R. Jennings, & P. K. Ackles (Eds.), Advances in psychophysiology, Vol. 5, London: Jessica Kingsley Publishers. Jones, G. E., Leonberger, T. F., Rouse, C. H., Caldwell, J. A., & Jones, K. R. (1986). Preliminary data exploring the presence of an evoked potential associated with cardiac visceral activity. Psychophysiology, 23. Knapp, K., Ring, C., & Brener, J. (1997). Sensitivity to mechanical stimuli and the role of general sensory and perceptual processes in heartbeat detection. Psychophysiology, 34, 467–473. Pardo, S. E., Faris, P. L., Hartman, B. K., Kim, S. W., Ivanov, E. H., Daughters, R. S., et al. (2003). Functional neuroimaging of gastric distention. Journal of General Psychology, 7, 740–749. Phan, K. L., Wager, T., Taylor, S. F., & Liberzon, I. (2002). Functional neuroanatomy of emotion: A meta-analysis of emotion activation studies in PET and fMRI. NeuroImage, 16, 331–348. Pollatos, O., Gramann, K., & Schandry, R. (2007). Neural systems connecting interoceptive awareness and feelings. Human Brain Mapping, 28, 9–18. Pollatos, O., Herbert, B.M., Wankner, S., Dietel, A., Wachsmuth, C., Henningsen, P., et al. (2011). Autonomic imbalance is associated with reduced facial recognition in somatoform disorders. Journal of Psychosomatic Research, 71, 232–239. Pollatos, O., Kirsch, W., & Schandry, R. (2005a). Brain structures involved in interoceptive awareness and cardioafferent signal processing: A dipole source localization study. Human Brain Mapping, 26, 54–64. Pollatos, O., Kirsch, W., & Schandry, R. (2005b). On the relationship between interoceptive awareness, emotional experience, and brain processes. Cognitive Brain Research, 25, 948–962. Pollatos, O., Kurz, A. L., Albrecht, J., Schreder, T., Kleemann, A.M., Schöpf, V., et al. (2008). Reduced perception of bodily signals in anorexia nervosa. Eating Behaviors, 9, 381–388. Pollatos, O., Schandry, R., Auer, D. P., & Kaufmann, C. (2007). Brain structures mediating cardiovascular arousal and interoceptive awareness. Brain Research, 1141, 178–187. Schandry, R. (1981). Heart beat perception and emotional experience. Psychophysiology, 18, 483–488. Schandry, R., Bestler, M., & Montoya, P. (1993). On the relation between cardiodynamics and heartbeat perception. Psychophysiology, 30, 467–474. Whitehead, W. E., & Drescher, V. M. (1980). Perception of gastric contractions and selfcontrol of gastric motility. Psychophysiology, 17, 552–558. Wildman, H. E., & Jones, G. E. (1982). Consistency of heartbeat discrimination scores on the Whitehead procedure in knowledge-of-results — Trained and untrained subjects. Psychophysiology, 19, 592.