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Interoception
Interoception Andre´ Schulz, University of Luxembourg, Walferdange, Luxembourg Ó 2015 Elsevier Ltd. All rights reserved.
Abstract This article summarizes contemporary knowledge on the psychology of interoception, i.e., the perception of bodily processes, and the underlying physiological mechanisms. First, theoretical models of interoception are presented and brain regions are discussed, which may play a role for the processing of interoceptive neural signals. Second, the most relevant methods to assess interoceptive accuracy are described. Third, the relevance of interoception for disciplines of general psychology is outlined. Fourth, the role of interoceptive accuracy for the development and maintenance of symptoms in clinical mental disorders are presented. Finally, some future challenges in interoceptive research are discussed.
Introduction Sensory information from the body originates from different sensory receptor types, which can be distinguished (Dworkin, 2007) into (1) exteroceptors (e.g., mechanoreceptors in the skin), (2) proprioceptors (e.g., receptors in the spindles of skeletal muscles), and (3) interoceptors (e.g., mechano-, chemo-, thermo-, or metaboreceptors in visceral organs). Exteroceptors process external sensory information, such as visual, auditory, or tactile stimuli. A limited number of bodyinternal macroevents, such as heartbeats, may also partially be processed via exteroceptive, i.e., somatosensory receptors. Information on body position, muscular movement or tension are relayed by proprioceptors. Sensory information indicating the state of visceral organs is considered to constitute interoception. There is a variety of receptor subtypes that are responsible for interoceptive signal processing. Every organ system has its own population of interoceptors. They can be categorized using the following characteristics: (1) their functionality; receptors may be sensitive to physical movement or pressure (mechano- or stretch receptors), to a chemical substance or a specific concentration of this substance (chemoreceptors), to an under- or overrun of a threshold of a certain temperature (thermoreceptors), or to the registration of a metabolic process (metaboreceptor). (2) Their sensory threshold; e.g., one population of baroreceptors in arterial blood vessels respond to blood pressure changes within a range up to 100 mmHg, while another one responds to changes over 100 mmHg. (3) Their adaptability; the timeframe, within which interoceptors adapt to continuous stimulation may vary in subpopulations (fast- vs slow-adapting). Sensory information from interoceptors is continuously transmitted to the central nervous system. The majority is relayed over reflex circuits in the spinal cord or the brainstem without any conscious perception of these processes. However, this interoceptive information can reach consciousness if a predefined range of ‘normal’ functioning is exceeded. For instance, when body temperature will reach 38 C, it is perceived as fever, if the filling of the stomach is exceeded, it is perceived as nausea, or if heart rate and blood pressure dramatically increase in a stressful situation, it is perceived as aversive. Interoception research does not only focus on conscious perception of bodily processes, but it also aims to understand interoceptive signal
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processing below consciousness level. One objective of this article is to summarize psychological disciplines, in which the conscious or unconscious processing of interoceptive signals play a decisive role.
Neurophysiology and Neuropsychology of Interoception The majority of afferent signals from interoceptors are transmitted over the Nervus vagus and the Nervus glossopharyngeus and then relayed over the nucleus tractus solitarius (NTS), the main sensory brainstem center for visceral-afferent information. Reflex circuits for the maintenance of homeostasis in physiological processes, such as blood pressure (i.e., arterial baroreflex), oxygen saturation, or body temperature, involve synapses within the NTS. The NTS is in close exchange with other medullary structures, the caudal (CVLM) and rostral ventromedial medulla (RVLM), and the dorsal motor nucleus of the vagus (DMNV), which all play a role in these reflex circuits. From the NTS afferent signals are projected onto midbrain areas (parabrachial nucleus, PBN; periaquaeductal gray, PAG). The PBN and PAG are connected with higher structures, involving the limbic system, hypothalamus and thalamus, as well as cortical regions. The conscious perception of bodily signals certainly requires the involvement of the thalamus as important relay for sensory information. Cortical areas that are responsible for the processing of interoceptive neural signals are the anterior cingulate cortex (ACC), the anterior insula (AI) in the temporal lobe, the somatomotor cortex (SMC), the somatosensory cortex (SSC), and the prefrontal cortex (PFC). Neuroimaging studies have shown that a heartbeat detection task activates the right AI, the ACC, and the SMC, whereas the gray matter volume in the AI correlates with the accuracy in such tasks (Critchley et al., 2004). The processing of interoceptive signals, such as heartbeats, may result in the generation of specific electrocortical potentials (e.g., heartbeat-evoked potentials). These potentials are located in the ACC, the right IA, the SSC, and the PFC (Pollatos et al., 2005), which play a role in interoceptive signal processing. In addition to the transmission of afferent neural signals over the cranial nerves, another pathway over the spinal cord may also play an important role in interoception, the lamina1spinothalamocortical pathway (Craig, 2002). Projections over
International Encyclopedia of the Social & Behavioral Sciences, 2nd edition, Volume 12
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this pathway also reach the NTS and thalamic structures, but it also integrates other afferent information from the body, such as information on nociception and tissue damage.
to lower accuracy, or others may focus a maximal grade of awareness toward interoceptive stimuli that may still be below the sensory threshold.
Concepts of Interoception
Methods to Assess Interoception
There is an ongoing debate, which mechanisms in afferent signal processing from the body can be called ‘interoception.’ Given the importance of interoception for psychology, there is also a shortness on theoretical models to include different levels of interoceptive signal processing. Vaitl (1996) views interoception as a general term to be subdivided into somatosensory, proprioceptive, and visceroceptive subsystems. In his model of interoception, sensory information from all three subsystems is transmitted to the CNS, where their representations are processed. CNS representation may reach awareness if attention is focused on visceral sensations. Learning processes are assumed to be the consequence of conscious CNS representations and may influence subjective reports, behavior or evaluation and could further affect the previous levels of interoceptive signal processing. The assumption of this regulatory circuit is congruent with feed-forward models of somatosensory amplification. The integration of somatosensory, proprioceptive and visceroceptive afferent signals is well in line with models on interoception and emotion, which propose that the experience of emotions relies on afferent signals from different sources (Wiens, 2005). Each of the methods to assess interoception described below involve different components of interoception in Vaitl’s model. Heartbeat-evoked potentials, for example, require the stimulation of interoceptors and CNS representation, while awareness, report, or learning are not necessary, while they would be for performance in heartbeat detection tasks. From the current point of view, afferent signal transmission represents an independent factor, as it has been repeatedly shown that interoceptive signal processing is deficient in individuals with degeneration of afferent autonomic nerves, while interoceptors are still intact (Leopold and Schandry, 2001; Schulz et al., 2009). Furthermore, CNS representations can be differentiated into brainstem representations and higher (cortical) representations. The denomination of interoceptive measures has been extensively discussed in literature. Common terms are ‘interoceptive awareness,’ ‘interoceptive sensitivity,’ or ‘interoceptive accuracy,’ although they all describe the same kind of measure (here: accuracy in a heartbeat detection task). Garfinkel and Critchley (2013) have addressed this issue and postulated a hierarchical model of interoception. They understand ‘interoceptive sensibility’ as dispositional tendency to be internally focused and thus as a prerequisite for the successful completion of interoceptive tasks. In their words ‘interoceptive sensitivity’ should represent the objective accuracy in these tasks, whereas ‘interoceptive awareness’ could be understood as metacognitive measure that quantifies individuals’ explicit knowledge of their interoceptive accuracy. Although this differentiation is plausible, the measure indexed by interoceptive tasks should be called ‘interoceptive accuracy’ instead, since this term is rather neutral. It does not suggest that a specific score reflects ‘sensitivity’ or ‘awareness,’ since some individuals may be hypersensitive, which leads to misinterpretation of signals and thus
Heartbeat Detection Tasks The majority of research is based on experimental paradigms, in which participants are requested to detect their heartbeats. They are further divided into heartbeat counting tasks and discrimination tasks. Heartbeat counting tasks were developed by Schandry (1981), who named the task ‘mental tracking test.’ The task consists of time intervals of different duration (original version: 35, 45, and 55 s), during which the participants are instructed to silently count the number of their heartbeats. This number is later compared with the actual number of heartbeats in this interval. The absolute value of the difference between both is divided by the actual number of heartbeats and this ‘inaccuracy’ index is then subtracted from 1, which results in the accuracy score of the heartbeat counting task. It has been repeatedly demonstrated that the accuracy score depends on the wording of the instruction given. The comparison between a standard instruction (“count all heartbeats you feel in the body”) and a strict instruction (“count only those heartbeats about which you are sure”) suggests that an individual’s knowledge on their heart rate and capacity to accurately estimate the duration of time intervals may be important factors for the accuracy in heartbeat counting tasks (Ehlers and Breuer, 1996). Heartbeat discrimination tasks were originally developed by Brener and Jones (1974) and further elaborated by others. In these tasks participants are asked to judge whether a set of consecutive exteroceptive stimuli (e.g., lights, tones, tactile stimuli) appear simultaneously with their own heartbeats (Sþ trials) or not (S trials). The available variants of this task mainly differ in the setup of S trials, since some present exteroceptive stimuli with a fixed delay to heartbeats, while others simulate a set of artificial stimuli without any relation to the actual heartbeats. In a systematic investigation on possible time delays between heartbeats and the elicitation of an exteroceptive signal it was demonstrated that the optimal delay for the concurrent perception of both is about 230 ms after an R-wave (Brener and Ring, 1995). Heartbeat detection is reduced in individuals with a degeneration of afferent autonomic nerves due to diabetes mellitus.
Heartbeat-Evoked Potentials Heartbeat-evoked brain potentials (HEPs) represent electrocortical potentials, which are related to the perception of cardiac signals, such as heartbeats. HEPs can be measured 250– 600 ms after a cardiac R-wave and have their largest amplitude over the right hemisphere at frontal and central sites. HEP amplitudes have been demonstrated to reflect an individuals’ performance in heartbeat detection tasks, motivation to perform in those tasks, and attentional focus on heartbeats. Nevertheless, the conscious perception of heartbeats is not required to produce HEPs, since afferent signals from the cardiovascular system continuously reach higher cortical areas. As a consequence, HEPs are measured during heartbeat
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detection tasks (Leopold and Schandry, 2001), during rest (Schulz et al., 2013b) or during another foreground task (Gray et al., 2007). HEPs are calculated as event-related potentials with the R-wave in the ECG as ‘event.’ Since it was demonstrated that up to a time delay of 450 ms the electrocardiac field of the ECG and the HEP are partially overlapping, both effects have to be disentangled (Gray et al., 2007). Again, HEPs are reduced in individuals with a degeneration of afferent autonomic nerves (Leopold and Schandry, 2001).
Visceral Modulation of Startle Afferent signals from visceral organs have the potential to modulate higher central information processing. Initially, this relationship was investigated in the cardiovascular system. The additive stimulation or unloading of arterial baroreceptors by the cardiac cycle and an external pressure/suction device affects the human startle response to auditory stimuli, a defensive reflex that is relayed over the brainstem. Even without external stimulation startle responses are lower during the early cardiac cycle phase (R-wave þ 230 ms) than during the late cardiac cycle phase (R þ 530 ms), as are subjective intensity ratings of the startle stimuli. The difference of startle amplitudes during early and late cardiac cycle phase has been called ‘Cardiac Modulation of Startle’ (CMS) effect. This effect is also largely diminished in individuals with diabetic neuropathy (Schulz et al., 2009). The CMS effect, therefore, reflects baroafferent neural traffic from the cardiovascular system. In contrast to the other methods described, the CMS may serve as a methodology to estimate afferent neural signals relayed at the level of the brainstem, since only brainstem processes are involved (arterial baroreflex circuit, acoustic startle circuit). Furthermore, afferent signals from cardiopulmonary baroreceptors, the gastrointestinal system and the respiratory system may also influence the human startle response. Thus, the concept of CMS could eventually be extended to ‘Visceral Modulation of Startle.’ HEPs and CMS are considered psychophysiological indicators of interoceptive signal processing.
Factors Determining Accuracy in Interoception Tasks Differential Aspects of Interoceptive Accuracy A number of sociodemographic factors play a role in the accuracy in interoceptive tasks. In general, results suggest that men are more accurate in interoceptive tasks related to sensations of the cardiovascular, the respiratory or the gastrointestinal system than women. Possible explanations for these effects could be sex differences in vascular musculature or hemispheric lateralization, which also play a role in interoception. The higher proportion of body fat in women than in men could also account for these differences, as it has been shown that individuals with lower body fat perform better in heartbeat perception tasks, and accuracy in these tasks is negatively correlated with BMI (Herbert et al., 2013). Furthermore, Khalsa et al. (2009) have demonstrated that accuracy in heartbeat perception tasks and age show a negative association (r ¼ .30). This correlation could be explained by reduced sympathetic tone, decreased sensitivity of baroreceptors, or reduced arterial stiffness with increasing age. Contrary to
common wisdom, experienced meditators do not show higher accuracy in interoceptive tasks (Khalsa et al., 2008), than normal controls, although they report subjectively increased awareness to bodily states.
Physiological Determinants Arterial baroreceptors represent one important type of interoceptors, which are responsible for cardiac interoception. In response to head-up tilt or isometric exercise, accuracy in heartbeat detection tasks is highly correlated with stroke volume (SV; r ¼ .59) and momentum (r ¼ .67), which represents the product of SV and velocity of blood outflow (Schandry et al., 1993). Furthermore, accuracy in heartbeat detection is associated with the change in the pre-ejection period (PEP) and the cardiac output in response to a mental arithmetic stressor. It could thus be concluded that cardiodynamic parameters, which are considered reflecting inotropic activation (contractility), are positively associated with accuracy in heartbeat detection. Nevertheless, this relationship has not been consistently reported in the literature. Heartbeat perception accuracy is positively related to systolic blood pressure (SBP), but negatively related to heart rate. Typically, there is a negative relationship between heart rate (HR) and SV, except for conditions of extensive exercise or stress. Increased SV, decreased PEP, and increased SBP may generally induce higher stimulation of arterial baroreceptors. Psychophysiological parameters that imply increased stimulation of baroreceptors per single heartbeat are, therefore, positively correlated with accuracy in heartbeat detection tasks (SV[, PEPY, SBP[), while parameters that imply decreased stimulation per heartbeat (HR) show the opposite pattern. Individuals with a high degree of physical training tend to have superior accuracy in heartbeat detection compared with nontrained individuals.
Interoception and Emotions Early Concepts In the original James-Lange theory of emotion, all emotional processes are understood as epiphenomena of visceral activation, which takes place when an individual is confronted with an emotionally relevant stimulus. Nevertheless, this theory has not been empirically supported. According to the modified theory by Cannon and Bard, visceral responses and the genesis of emotions are concurrently elicited through the perception of an emotionally relevant stimulus. Individuals with interrupted transmission of visceral-afferent signals, for example, still experience emotions, although visceral activation is too slow to match the genesis of emotions. In the seminal study by Schachter and Singer (1962) individuals received epinephrine, which drives the sympathetic nervous system, or a placebo substance. One subgroup of participants was informed about the ‘adverse effects’ of the substance, another subgroup was naïve. The authors observed that the informed group attributed their subjective level of arousal to the adverse effects of the drug, while the naïve participants reported a higher intensity of anger after being exposed to anger provocation by an experimenter. These results suggest that both the perception of bodily states and cognitive appraisal are important for the experience of an emotion.
Interoception
Current Point of View Contemporary theories do not assume interoceptive signals as crucial for the experience of emotions anymore. Nevertheless, individuals with spinal cord injury have been found to report reduced intensity of emotions, which suggests that afferent information of bodily states is important, but not a prerequisite for emotion genesis. Current concepts assume that interoceptive neural traffic reaches ‘first order’ central structures, such as the dorsal pontine areas, the AI, and the somatosensory cortex, which may be associated with a phenomenological level of emotional experience. In a ‘second order’ of central representation of interoceptive signals, structures such as the anterior cingulum integrate these genuine interoceptive signals and other sources of bodily information, e.g., somatosensory feedback and attention. Self-reported emotional experience may thus be the consequence of integrating interoceptive signals and other information of bodily states, as well as paying attention to these processes (Wiens, 2005). A large body of evidence indicates that a more intense experience of emotions is positively associated with accurate heartbeat perception. Neuroimaging studies suggest that the processing of interoceptive signals and the experience of emotion share neural structures, such as the AI, the ventromedial prefrontal cortex (VMPFC), and the ACC (Pollatos et al., 2007).
Interocepion and Decision Making Damasio’s Somatic Marker Hypothesis The influential somatic marker hypothesis by Damasio (1994) postulates that interoceptive signals are regularly integrated into processes of decision making. In every context, in which decisions are expected to be made, the outcomes of possible action alternatives are anticipated. This anticipation produces a specific visceral response to be integrated in affective responses to the expected outcome. These responses, either transmitted over somatosensory or visceral-afferent circuits, are called ‘somatic markers.’ Damasio hypothesized that these ‘somatic markers’ shape decision making. The neural structure that is thought to be responsible for the integration and evaluation of somatic markers is the VMPFC. There is a large body of evidence supporting the somatic marker theory. In experimental research, human decision making is assessed through specific paradigms, such as the Iowa Gambling Task. Performance in this task is positively associated with sympathetic responses in anticipation of punishment or reward, putatively reflecting the availability of somatic markers, as well as with accuracy in interoceptive tasks. Patients with neurological damage in the VMPFC do not show comparable electrodermal responses to anticipated punishment or reward (Bechara et al., 1996). Dunn et al. (2006) provide a comprehensive review of the somatic marker hypothesis.
Interoception and Stress Interoceptive Accuracy during and after Acute Laboratory Stressors While interoception describes the transmission of ascending signals on the brain–body axis, stress represents a prominent
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example for descending information on the brain–body axis. Stress and activation drive the two physiological stress systems, the sympathetic–adrenomedullary (SAM) axis including the sympathetic nervous system, and the hypothalamus–pituitary–adrenocortical (HPA) axis with cortisol as final product. Neural and endocrine signaling resulting from the activation of both axes may change the activity of visceral organs (e.g., inotropic and chronotropic effects on the myocardium) and typical brain regions, which are responsible for their perception (e.g., thalamus, insular cortex). Thus it can be argued that interoception and stress are closely linked. Laboratory stress tests are designed to provide a stressful environment that guarantees for a maximal degree of standardization, ecological validity (i.e., cognitive, affective, and behavioral aspects of stress), and effectiveness. However, the direction of the effect of a laboratory stressor on interoceptive accuracy largely depends on the methods used to investigate interoception. Comparing both heartbeat detection tasks, these opposite effects were observed with a strong laboratory stressor, the Socially Evaluated Cold Pressor Test (SECPT) (Schulz et al., 2013a): Stress seems to increase interoceptive accuracy if attention is solely focused on visceral sensations (i.e., heartbeat counting), while it decreases if attention is additionally focused on exteroceptive stimuli (i.e., heartbeat discrimination). One possible conclusion is that stress effects on interoception depend on attentional processes. Evidence on the impact of stress on psychophysiological indicators of interoceptive signal processing is sparse. Acute stress induced by an SECPT was found to change the pattern of the cardiac modulation of startle (Schulz et al., 2011). Two studies investigated the impact of acute laboratory stressors on heartbeat-evoked potentials. A moderate arithmetic stressor could not modulate the HEP amplitude per se, but the HEP was correlated with cardiac responses to the stressor (Gray et al., 2007). Acute pain during a mild version of the cold pressor test attenuated HEP amplitudes (Shao et al., 2011), but possible later effects or relationships to both stress axes were not reported.
Stress Hormones Certain stress hormones are considered to play an important role in the processing of interoceptive signals. First, the activation of the autonomic nervous system may result in a release of catecholamines, such as epinephrine. Although catecholamines do not cross the blood–brain barrier and, therefore, cannot modulate the processing of interoceptive signals at the level of the CNS, epinephrine binds to beta1-adrenergic receptors at the myocardium. The binding of epinephrine to beta1-adrenoceptors causes positive inotropic (increased contractibility), chronotropic (increased heart rate), and dromotropic effects (faster depolarization), which lead to an increase of SV and a decrease of the PEP (Schachinger et al., 2001). It was repeatedly shown that cardiodynamic parameters, such as PEP or SV, are associated with the accuracy in heartbeat detection tasks (Schandry et al., 1993). It is likely that the increased stimulation of arterial baroreceptors caused by increased SV is responsible for this effect. Furthermore, peripheral sympathetic activation induced via beta1-adrenergic
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agents and central sympathetic activity elicited by alpha1-adrenergic agents increases heartbeat perception accuracy (Moor et al., 2005). Second, cortisol, the final product of HPA axis activation, may also have the potential to modulate interoceptive signal processing. A dose of 4 mg of intravenously administered cortisol may induce higher heartbeat-evoked potentials in a state of high alertness compared with a state of low alertness (Schulz et al., 2013b). This effect may feed into a vicious circle of increased attentional focus on physical symptoms, increased anxiety and higher levels of cortisol, which may represent possible psychoneuroendocrine mechanism underlying psychological feed-forward models of somatosensory amplification. Interestingly, cortisol does not affect the cardiac modulation of startle, suggesting that this effect is limited to the cortical representation of interoceptive signals, but does not alter the brainstem processing of afferent bodily signals (Schulz et al., submitted). In contrast to catecholamines, cortisol crosses the blood–brain barrier and affects cells in the entire body, including the CNS. The described results can be attributed to activity in the thalamus, which represents a major relay center for exteroceptive and interoceptive sensory information, and was demonstrated to be affected by cortisol administration. The importance of the HPA axis for altered perception of physical sensations is further underlined by the fact that dysregulation of the HPA axis can be observed in many body-related mental disorders, such as somatoform disorders (Rief and Barsky, 2005) or depression (Terhaar et al., 2012).
Chronic Stress There is very little research on chronic stress and interoception. This is surprising in view of the widely accepted notion that chronic stress exposure causes dysregulation of the SAM and the HPA axes, which in turn are of particular relevance for the above mentioned mental disorders. Clinical data suggests that these dysregulations contribute to the generation of physical symptoms and may thus disrupt the adequate processing of interoceptive signals (Rief and Barsky, 2005). Nevertheless, an association between self-reported chronic stress and interoceptive accuracy in laboratory paradigms has not been demonstrated, as yet (gastric stimulation: Rosenberger et al., 2009; heartbeat detection task: Schulz et al., 2013a). Both studies, however, assessed chronic stress in healthy participants. It remains for future studies to investigate possible abnormalities in interoceptive accuracy in chronically stressed individuals, which may already show SAM and HPA axes dysregulation.
signals are transmitted to the NTS and LC. From these structures, over noradrenergic pathways, beta-adrenergic synapses in the BLA are activated, which induces the release of cyclic adenosine monophosphate (cAMP) and cAMP-dependent protein kinase. Both substances can enhance memory consolidation. Postsynaptic efficacy of beta-adrenergic synapses is increased by glucocorticoids. Results from animal models show that both processes, glucocorticoid secretion and afferent signal transmission from visceral organs, are necessary for memory consolidation. In humans, the increase of baroafferent neural feedback induced by norepinephrine-infusion improved long-term memory (Moor et al., 2005). Interoceptive neural signals, therefore, play an important role for the stress-induced improvement of memory consolidation in animals and humans.
Interoception in Mental Disorders Panic Disorder The most frequently investigated disorder in relation to interoception is panic disorder. In cognitive models of panic disorder it is assumed that panic patients have enhanced selective attention for threat-related stimuli in general and body-related cues in particular. This attentional bias may result in increased interoceptive accuracy. In concordance with this hypothesis, many empirical papers/articles found superior accuracy in heartbeat counting tasks in patients with panic disorder as compared with healthy individuals or other mental disorders (Ehlers and Breuer, 1996). A positive relationship between panic symptoms and interoceptive accuracy has also been observed in children (Eley et al., 2004). Cognitivebehavioral therapy of panic disorder does not change performance in heartbeat perception, but heartbeat perception negatively predicts the outcome of therapeutic intervention (Ehlers and Breuer, 1996). Nevertheless, there are also negative reports, and Willem Van Der Does et al. (2000) conclude from a re-analysis of the data of many of these studies that the majority of patients with panic disorder do not have generally increased accuracy, but only a minority. Moreover, higher accuracy in heartbeat counting tasks was only found when using the standard instruction (“count all heartbeats you feel in the body”) and not in the strict instruction (“count only those heartbeats about which you are sure”) (Ehlers and Breuer, 1996). This highlights the importance of knowledge about one’s own heart rate in panic patients for performing this task, which may be more precise in panic patients, while healthy individuals tend to underestimate their heart rate in this task.
Depression
Interoception in Learning and Memory The model of stress and memory consolidation by McGaugh (2000) postulates that two physiological processes are crucial for the enhancement of memory consolidation after stress: (1) glucocorticoids (rodents: corticosterone; humans: cortisol) that bind on glucocorticoid receptors within the NTS, the locus coeruleus (LC), and the basolateral amygdala (BLA) and (2) peripherally circulating epinephrine, which cannot cross the blood–brain barrier, but activates visceral organs, whose afferent
Affective disorders are often accompanied by autonomic dysregulations, which are also reflected in specific symptoms, such as the disruption of the sleep–wake cycle, dysregulation of appetite, sexual dysfunction, or psychomotor inhibition or agitation. It is plausible that the dysregulation of autonomic processes also induces alterations in the perception of phenomena that are autonomically controlled. Dunn et al. (2007) have reported that individuals with a mild depression may have reduced interoceptive accuracy, while individuals with a severe depression may not differ in their accuracy
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from healthy controls. However, in this investigation it is unclear whether the difference between both depression groups is due to the severity of disease or to their use of medication, since the number and dosage of antidepressants was notably higher in the severe depression group. A reduction of interoceptive accuracy in major depression is also reflected in a decrease of heartbeat-evoked potentials as compared with healthy control individuals (Terhaar et al., 2012), which may be associated with altered activity in the insular cortex, which could be observed in depressed individuals. Since in a clinical setting there is a substantial overlap of depression and anxiety symptoms, it is not clear to what degree both components may differentially affect interoception. In a student sample it was demonstrated that there is a negative relationship between depression and interoceptive accuracy only in highly anxious individuals (Pollatos et al., 2009), which suggests the more important role of anxiety for interoception. Furthermore, it was reported that anxiety and anhedonia in a subclinical sample interact in that there is a positive relationship between anxiety and interoception only in individuals with low anhedonia (Dunn et al., 2010). Taken together, depressive symptomatology is associated with a tendency for decreased interoceptive accuracy, which may additionally be moderated by anxiety level.
Somatoform Disorders The perception-filter model of somatoform disorders (SD) postulates that hyperactivation of the autonomic nervous system and the HPA axis contribute to increased perception of physical sensations in SD (Rief and Barsky, 2005). Study findings, however, are very mixed. This could be due to the heterogeneity of the conditions classified as SD, some of which emphasize the misperception of bodily signals (e.g., medically unexplained symptoms), while others focus more on medically unestablished health-oriented anxiety (e.g., hypochondria). Even within the field of medically unexplained symptoms (MUS) it is questionable whether individuals with complaints in different organ systems should be classified under the same condition (e.g., cardiovascular symptoms vs. chronic back pain). Furthermore, there is a debate in the literature on the expected direction of the difference between somatoform patients and controls. As summarized by Schaefer et al. (2012), some models assume an increased focus of attention on bodily processes in SD, which may lead to increased accuracy in interoception, while opposing models propose deficient processing of interoceptive signals in SD. Empirical data are in partial support of both hypotheses. On the one hand, Pollatos et al. (2011) found that a mixed group of somatoform patients showed lower accuracy in a heartbeat counting task than a healthy control group. On the other hand, high symptom reporters in the normal population as well as patients with MUS both show less accurate perception of CO2 ratio in the air than healthy individuals (Bogaerts et al., 2010). Schaefer et al. (2012) reported that a mixed somatoform outpatient group and a matched healthy control group did not differ in the accuracy of the heartbeat counting or discrimination task. However, a negative correlation between the number of symptoms and the accuracy in the heartbeat counting task was observed. It can be summarized that there is
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a tendency to observe lower accuracy in interoceptive tasks in patients with MUS. Nevertheless, SD in general and MUS in particular may be characterized by an inappropriateness of processing afferent information from the body. It is questionable whether this deficiency is solely reflected by a quantitative reduction in interoceptive paradigms or if this alteration should not rather be seen as a qualitative change. Moreover, the role of possible dysregulated stress responses in SD, and the role of depression for altered interoception is still neglected in the current literature.
Eating Behavior and Eating Disorders Patients with anorexia nervosa (AN), bulimia nervosa (BN), and binge eating disorder (BED) all report increased subjective awareness to bodily processes. In contrast, patients with AN and BN show lower interoceptive accuracy than healthy controls (Herbert and Pollatos, 2014; Pollatos et al., 2008), while there is no data on patients with BED. One challenge in interoception research with eating disorders is to determine which components of a putatively altered interoception may be attributed to the mental disorder and which may be a physiological and metabolic result of the dysregulated food intake. For instance, the increased interoceptive accuracy in obesity could be a result of an increase in arterial blood pressure. Furthermore, with a quasiexperimental approach of clinical group comparisons, it is impossible to disentangle cause and effect. There is empirical evidence supporting both alternative hypotheses. On the one hand, eating behavior has been experimentally manipulated to assess possible effects on interoception. Short-term fasting was found to increase accuracy in heartbeat counting tasks (Herbert et al., 2012), and the amplitude of heartbeat-evoked potentials (Schulz et al., 2014). While short-term food deprivation induces an increase in sympathetic tone, these effects are inverted in long-term food deprivation. It is, therefore, plausible that long-term fasting, such as observed in AN, may be a way of regulating the perception of bodily sensations. This assumption is also in line with the finding that AN patients show reduced interoceptive accuracy (Pollatos et al., 2008). On the other hand, interoceptive accuracy is positively associated with intuitive eating (Herbert et al., 2013), suggesting that high interoceptive accuracy contributes to healthy eating behavior.
Future Directions In the majority of the studies described, interoception was operationalized using interoceptive tasks, e.g., heartbeat perception tasks, or psychophysiological indicators of interoceptive processing, e.g., heartbeat-evoked potentials. These studies demonstrate linear relationships between accuracy in interoceptive tasks or group comparisons in terms of ‘higher than’ or ‘lower than.’ A careful revision of the literature on stress and interoception, as well as interoception in mental disorders as compared with healthy controls demonstrates that the assumption of linear relationships does not hold. Future research should investigate more complex relationships between interoceptive measures and mental disorders, and also focus on qualitative instead of only quantitative changes in
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interoceptive processing. Another challenge for future research lies in the assessment of different interoception modalities at a time with the same technique (horizontal integration), as well as different levels of the same interoceptive modality (e.g., signals at the level of the brainstem, the cortex, and subjective reports; vertical integration).
See also: Chronic Pain: Models and Treatment Approaches; Co-morbidity of Mental and Physical Conditions; Explanatory Style and Health; Health Risk Perception; Illness Behavior and Care-Seeking; Stress and Cardiac Response; Stress, Coping and Health; Symptom Perception, Awareness and Interpretation.
Bibliography Bechara, A., Tranel, D., Damasio, H., Damasio, A.R., 1996. Failure to respond autonomically to anticipated future outcomes following damage to prefrontal cortex. Cerebral Cortex 6, 215–225. Bogaerts, K., Van Eylen, L., Li, W., Bresseleers, J., Van Diest, I., De Peuter, S., Stans, L., Decramer, M., Van Den Bergh, O., 2010. Distorted symptom perception in patients with medically unexplained symptoms. Journal of Abnormal Psychology 119, 226–234. Brener, J., Jones, J.M., 1974. Interoceptive discrimination in intact humans: detection of cardiac activity. Physiology & Behavior 13, 763–767. Brener, J., Ring, C., 1995. Sensory and perceptual factors in heart beat detection. In: Vaitl, D., Schandry, R. (Eds.), From the Heart to the Brain. The Psychophysiology of Circulation – Brain Interaction. Peter Lang, Frankfurt, pp. 193–221. Craig, A.D., 2002. How do you feel? Interoception: the sense of the physiological condition of the body. Nature Reviews Neuroscience 3, 655–666. 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., 1994. Descartes’ Error: Emotion, Reason and the Human Brain. Grosset/ Putnam, New York. Dunn, B.D., Dalgleish, T., Lawrence, A.D., 2006. The somatic marker hypothesis: a critical evaluation. Neuroscience & Biobehavioral Reviews 30, 239–271. 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., Stefanovitch, I., Evans, D., Oliver, C., Hawkins, A., Dalgleish, T., 2010. Can you feel the beat? Interoceptive awareness is an interactive function of anxiety- and depression-specific symptom dimensions. Behaviour Research and Therapy 48, 1133–1138. Dworkin, B.R., 2007. Interoception. In: Cacioppo, J.T., Tassinary, L.G., Berntson, G.G. (Eds.), Handbook of Psychophysiology, third ed. Cambrigde University Press, Cambridge. Ehlers, A., Breuer, P., 1996. How good are patients with panic disorder at perceiving their heartbeats? Biological Psychology 42, 165–182. Eley, T.C., Stirling, L., Ehlers, A., Gregory, A.M., Clark, D.M., 2004. Heart-beat perception, panic/somatic symptoms and anxiety sensitivity in children. Behaviour Research and Therapy 42, 439–448. Garfinkel, S.N., Critchley, H.D., 2013. Interoception, emotion and brain: new insights link internal physiology to social behaviour. Commentary on: “Anterior insular cortex mediates bodily sensibility and social anxiety” by Terasawa et al. (2012). Social Cognitive and Affective Neuroscience 8, 231–234. Gray, M.A., Taggart, P., Sutton, P.M., Groves, D., Holdright, D.R., Bradbury, D., Brull, D., Critchley, H.D., 2007. A cortical potential reflecting cardiac function. Proceedings of the National Academy of Sciences of the United States of America 104, 6818–6823. 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 70C, 22–30. Herbert, B.M., Herbert, C., Pollatos, O., Weimer, K., Enck, P., Sauer, H., Zipfel, S., 2012. Effects of short-term food deprivation on interoceptive awareness, feelings and autonomic cardiac activity. Biological Psychology 89, 71–79. Herbert, B.M., Pollatos, O., 2014. Attenuated interoceptive sensitivity in overweight and obese individuals. Eating Behaviors, 445–448.
Khalsa, S.S., Rudrauf, D., Damasio, A.R., Davidson, R.J., Lutz, A., Tranel, D., 2008. Interoceptive awareness in experienced meditators. Psychophysiology 45, 671–677. Khalsa, S.S., Rudrauf, D., Tranel, D., 2009. Interoceptive awareness declines with age. Psychophysiology 46, 1130–1136. Leopold, C., Schandry, R., 2001. The heartbeat-evoked brain potential in patients suffering from diabetic neuropathy and in healthy control persons. Clinical Neurophysiology 112, 674–682. McGaugh, J.L., 2000. Memory–a century of consolidation. Science 287, 248–251. Moor, T., Mundorff, L., Bohringer, A., Philippsen, C., Langewitz, W., Reino, S.T., Schachinger, H., 2005. Evidence that baroreflex feedback influences long-term incidental visual memory in men. Neurobiology of Learning and Memory 84, 168–174. 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., Sack, M., 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., 2005. Brain structures involved in interoceptive awareness and cardioafferent signal processing: a dipole source localization study. Human Brain Mapping 26, 54–64. Pollatos, O., Kurz, A.L., Albrecht, J., Schreder, T., Kleemann, A.M., Schopf, V., Kopietz, R., Wiesmann, M., Schandry, R., 2008. Reduced perception of bodily signals in anorexia nervosa. Eating Behaviors 9, 381–388. Pollatos, O., Traut-Mattausch, E., Schandry, R., 2009. Differential effects of anxiety and depression on interoceptive accuracy. Depress Anxiety 26, 167–173. Rief, W., Barsky, A.J., 2005. Psychobiological perspectives on somatoform disorders. Psychoneuroendocrinology 30, 996–1002. Rosenberger, C., Elsenbruch, S., Scholle, A., De Greiff, A., Schedlowski, M., Forsting, M., Gizewski, E.R., 2009. Effects of psychological stress on the cerebral processing of visceral stimuli in healthy women. Neurogastroenterology and Motility 21, 740-e45. Schachinger, H., Weinbacher, M., Kiss, A., Ritz, R., Langewitz, W., 2001. Cardiovascular indices of peripheral and central sympathetic activation. Psychosomatic Medicine 63, 788–796. Schachter, S., Singer, J.E., 1962. Cognitive, social, and physiological determinants of emotional state. Psychological Review 69, 379–399. Schaefer, M., Egloff, B., Witthoft, M., 2012. Is interoceptive awareness really altered in somatoform disorders? Testing competing theories with two paradigms of heartbeat perception. Journal of Abnormal Psychology 121, 719–724. 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. Schulz, A., Ferreira De Sá, D.S., Dierolf, A.M., Lutz, A., Van Dyck, Z., Vögele, C., Schächinger, H., 2014. Short-term Food Deprivation Increases Amplitudes of Heartbeat-evoked Potentials. Psychophysiology. Accepted for publication. Schulz, A., Lass-Hennemann, J., Nees, F., Blumenthal, T.D., Berger, W., Schachinger, H., 2009. Cardiac modulation of startle eye blink. Psychophysiology 46, 234–240. Schulz, A., Lass-Hennemann, J., Sutterlin, S., Schachinger, H., Vogele, C., 2013a. Cold pressor stress induces opposite effects on cardioceptive accuracy dependent on assessment paradigm. Biological Psychology 93, 167–174. Schulz, A., Plein, D.E., Richter, S., Blumenthal, T.D., Schachinger, H., 2011. Cold pressor stress affects cardiac attenuation of startle. International Journal of Psychophysiology 79, 385–391. Schulz, A., Richter, S., Ferreira De Sá, D.S., Vögele, C., Schächinger, H. Cardiac Modulation of Startle Is Not Affected by Intravenously Administered Cortisol, submitted for publication. Schulz, A., Strelzyk, F., Ferreira De Sa, D.S., Naumann, E., Vogele, C., Schachinger, H., 2013b. Cortisol rapidly affects amplitudes of heartbeat-evoked brain potentials-implications for the contribution of stress to an altered perception of physical sensations? Psychoneuroendocrinology 38, 2686–2693. Shao, S., Shen, K., Wilder-Smith, E.P., Li, X., 2011. Effect of pain perception on the heartbeat evoked potential. Clinical Neurophysiology 122, 1838–1845. Terhaar, J., Viola, F.C., Bar, K.J., Debener, S., 2012. Heartbeat evoked potentials mirror altered body perception in depressed patients. Clinical Neurophysiology 123, 1950–1957. Vaitl, D., 1996. Interoception. Biological Psychology 42, 1–27. Wiens, S., 2005. Interoception in emotional experience. Current Opinion in Neurology 18, 442–447. Willem Van Der Does, A.J., Antony, M.M., Ehlers, A., Barsky, A.J., 2000. Heartbeat perception in panic disorder: a reanalysis. Behaviour Research and Therapy 38, 47–62.
Abstract This article summarizes contemporary knowledge on the psychology of interoception, i.e., the perception of bodily processes, and the underlying physiological mechanisms. First, theoretical models of interoception are presented and brain regions are discussed, which may play a role for the processing of interoceptive neural signals. Second, the most relevant methods to assess interoceptive accuracy are described. Third, the relevance of interoception for disciplines of general psychology is outlined. Fourth, the role of interoceptive accuracy for the development and maintenance of symptoms in clinical mental disorders are presented. Finally, some future challenges in interoceptive research are discussed.
Introduction Sensory information from the body originates from different sensory receptor types, which can be distinguished (Dworkin, 2007) into (1) exteroceptors (e.g., mechanoreceptors in the skin), (2) proprioceptors (e.g., receptors in the spindles of skeletal muscles), and (3) interoceptors (e.g., mechano-, chemo-, thermo-, or metaboreceptors in visceral organs). Exteroceptors process external sensory information, such as visual, auditory, or tactile stimuli. A limited number of bodyinternal macroevents, such as heartbeats, may also partially be processed via exteroceptive, i.e., somatosensory receptors. Information on body position, muscular movement or tension are relayed by proprioceptors. Sensory information indicating the state of visceral organs is considered to constitute interoception. There is a variety of receptor subtypes that are responsible for interoceptive signal processing. Every organ system has its own population of interoceptors. They can be categorized using the following characteristics: (1) their functionality; receptors may be sensitive to physical movement or pressure (mechano- or stretch receptors), to a chemical substance or a specific concentration of this substance (chemoreceptors), to an under- or overrun of a threshold of a certain temperature (thermoreceptors), or to the registration of a metabolic process (metaboreceptor). (2) Their sensory threshold; e.g., one population of baroreceptors in arterial blood vessels respond to blood pressure changes within a range up to 100 mmHg, while another one responds to changes over 100 mmHg. (3) Their adaptability; the timeframe, within which interoceptors adapt to continuous stimulation may vary in subpopulations (fast- vs slow-adapting). Sensory information from interoceptors is continuously transmitted to the central nervous system. The majority is relayed over reflex circuits in the spinal cord or the brainstem without any conscious perception of these processes. However, this interoceptive information can reach consciousness if a predefined range of ‘normal’ functioning is exceeded. For instance, when body temperature will reach 38 C, it is perceived as fever, if the filling of the stomach is exceeded, it is perceived as nausea, or if heart rate and blood pressure dramatically increase in a stressful situation, it is perceived as aversive. Interoception research does not only focus on conscious perception of bodily processes, but it also aims to understand interoceptive signal
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processing below consciousness level. One objective of this article is to summarize psychological disciplines, in which the conscious or unconscious processing of interoceptive signals play a decisive role.
Neurophysiology and Neuropsychology of Interoception The majority of afferent signals from interoceptors are transmitted over the Nervus vagus and the Nervus glossopharyngeus and then relayed over the nucleus tractus solitarius (NTS), the main sensory brainstem center for visceral-afferent information. Reflex circuits for the maintenance of homeostasis in physiological processes, such as blood pressure (i.e., arterial baroreflex), oxygen saturation, or body temperature, involve synapses within the NTS. The NTS is in close exchange with other medullary structures, the caudal (CVLM) and rostral ventromedial medulla (RVLM), and the dorsal motor nucleus of the vagus (DMNV), which all play a role in these reflex circuits. From the NTS afferent signals are projected onto midbrain areas (parabrachial nucleus, PBN; periaquaeductal gray, PAG). The PBN and PAG are connected with higher structures, involving the limbic system, hypothalamus and thalamus, as well as cortical regions. The conscious perception of bodily signals certainly requires the involvement of the thalamus as important relay for sensory information. Cortical areas that are responsible for the processing of interoceptive neural signals are the anterior cingulate cortex (ACC), the anterior insula (AI) in the temporal lobe, the somatomotor cortex (SMC), the somatosensory cortex (SSC), and the prefrontal cortex (PFC). Neuroimaging studies have shown that a heartbeat detection task activates the right AI, the ACC, and the SMC, whereas the gray matter volume in the AI correlates with the accuracy in such tasks (Critchley et al., 2004). The processing of interoceptive signals, such as heartbeats, may result in the generation of specific electrocortical potentials (e.g., heartbeat-evoked potentials). These potentials are located in the ACC, the right IA, the SSC, and the PFC (Pollatos et al., 2005), which play a role in interoceptive signal processing. In addition to the transmission of afferent neural signals over the cranial nerves, another pathway over the spinal cord may also play an important role in interoception, the lamina1spinothalamocortical pathway (Craig, 2002). Projections over
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this pathway also reach the NTS and thalamic structures, but it also integrates other afferent information from the body, such as information on nociception and tissue damage.
to lower accuracy, or others may focus a maximal grade of awareness toward interoceptive stimuli that may still be below the sensory threshold.
Concepts of Interoception
Methods to Assess Interoception
There is an ongoing debate, which mechanisms in afferent signal processing from the body can be called ‘interoception.’ Given the importance of interoception for psychology, there is also a shortness on theoretical models to include different levels of interoceptive signal processing. Vaitl (1996) views interoception as a general term to be subdivided into somatosensory, proprioceptive, and visceroceptive subsystems. In his model of interoception, sensory information from all three subsystems is transmitted to the CNS, where their representations are processed. CNS representation may reach awareness if attention is focused on visceral sensations. Learning processes are assumed to be the consequence of conscious CNS representations and may influence subjective reports, behavior or evaluation and could further affect the previous levels of interoceptive signal processing. The assumption of this regulatory circuit is congruent with feed-forward models of somatosensory amplification. The integration of somatosensory, proprioceptive and visceroceptive afferent signals is well in line with models on interoception and emotion, which propose that the experience of emotions relies on afferent signals from different sources (Wiens, 2005). Each of the methods to assess interoception described below involve different components of interoception in Vaitl’s model. Heartbeat-evoked potentials, for example, require the stimulation of interoceptors and CNS representation, while awareness, report, or learning are not necessary, while they would be for performance in heartbeat detection tasks. From the current point of view, afferent signal transmission represents an independent factor, as it has been repeatedly shown that interoceptive signal processing is deficient in individuals with degeneration of afferent autonomic nerves, while interoceptors are still intact (Leopold and Schandry, 2001; Schulz et al., 2009). Furthermore, CNS representations can be differentiated into brainstem representations and higher (cortical) representations. The denomination of interoceptive measures has been extensively discussed in literature. Common terms are ‘interoceptive awareness,’ ‘interoceptive sensitivity,’ or ‘interoceptive accuracy,’ although they all describe the same kind of measure (here: accuracy in a heartbeat detection task). Garfinkel and Critchley (2013) have addressed this issue and postulated a hierarchical model of interoception. They understand ‘interoceptive sensibility’ as dispositional tendency to be internally focused and thus as a prerequisite for the successful completion of interoceptive tasks. In their words ‘interoceptive sensitivity’ should represent the objective accuracy in these tasks, whereas ‘interoceptive awareness’ could be understood as metacognitive measure that quantifies individuals’ explicit knowledge of their interoceptive accuracy. Although this differentiation is plausible, the measure indexed by interoceptive tasks should be called ‘interoceptive accuracy’ instead, since this term is rather neutral. It does not suggest that a specific score reflects ‘sensitivity’ or ‘awareness,’ since some individuals may be hypersensitive, which leads to misinterpretation of signals and thus
Heartbeat Detection Tasks The majority of research is based on experimental paradigms, in which participants are requested to detect their heartbeats. They are further divided into heartbeat counting tasks and discrimination tasks. Heartbeat counting tasks were developed by Schandry (1981), who named the task ‘mental tracking test.’ The task consists of time intervals of different duration (original version: 35, 45, and 55 s), during which the participants are instructed to silently count the number of their heartbeats. This number is later compared with the actual number of heartbeats in this interval. The absolute value of the difference between both is divided by the actual number of heartbeats and this ‘inaccuracy’ index is then subtracted from 1, which results in the accuracy score of the heartbeat counting task. It has been repeatedly demonstrated that the accuracy score depends on the wording of the instruction given. The comparison between a standard instruction (“count all heartbeats you feel in the body”) and a strict instruction (“count only those heartbeats about which you are sure”) suggests that an individual’s knowledge on their heart rate and capacity to accurately estimate the duration of time intervals may be important factors for the accuracy in heartbeat counting tasks (Ehlers and Breuer, 1996). Heartbeat discrimination tasks were originally developed by Brener and Jones (1974) and further elaborated by others. In these tasks participants are asked to judge whether a set of consecutive exteroceptive stimuli (e.g., lights, tones, tactile stimuli) appear simultaneously with their own heartbeats (Sþ trials) or not (S trials). The available variants of this task mainly differ in the setup of S trials, since some present exteroceptive stimuli with a fixed delay to heartbeats, while others simulate a set of artificial stimuli without any relation to the actual heartbeats. In a systematic investigation on possible time delays between heartbeats and the elicitation of an exteroceptive signal it was demonstrated that the optimal delay for the concurrent perception of both is about 230 ms after an R-wave (Brener and Ring, 1995). Heartbeat detection is reduced in individuals with a degeneration of afferent autonomic nerves due to diabetes mellitus.
Heartbeat-Evoked Potentials Heartbeat-evoked brain potentials (HEPs) represent electrocortical potentials, which are related to the perception of cardiac signals, such as heartbeats. HEPs can be measured 250– 600 ms after a cardiac R-wave and have their largest amplitude over the right hemisphere at frontal and central sites. HEP amplitudes have been demonstrated to reflect an individuals’ performance in heartbeat detection tasks, motivation to perform in those tasks, and attentional focus on heartbeats. Nevertheless, the conscious perception of heartbeats is not required to produce HEPs, since afferent signals from the cardiovascular system continuously reach higher cortical areas. As a consequence, HEPs are measured during heartbeat
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detection tasks (Leopold and Schandry, 2001), during rest (Schulz et al., 2013b) or during another foreground task (Gray et al., 2007). HEPs are calculated as event-related potentials with the R-wave in the ECG as ‘event.’ Since it was demonstrated that up to a time delay of 450 ms the electrocardiac field of the ECG and the HEP are partially overlapping, both effects have to be disentangled (Gray et al., 2007). Again, HEPs are reduced in individuals with a degeneration of afferent autonomic nerves (Leopold and Schandry, 2001).
Visceral Modulation of Startle Afferent signals from visceral organs have the potential to modulate higher central information processing. Initially, this relationship was investigated in the cardiovascular system. The additive stimulation or unloading of arterial baroreceptors by the cardiac cycle and an external pressure/suction device affects the human startle response to auditory stimuli, a defensive reflex that is relayed over the brainstem. Even without external stimulation startle responses are lower during the early cardiac cycle phase (R-wave þ 230 ms) than during the late cardiac cycle phase (R þ 530 ms), as are subjective intensity ratings of the startle stimuli. The difference of startle amplitudes during early and late cardiac cycle phase has been called ‘Cardiac Modulation of Startle’ (CMS) effect. This effect is also largely diminished in individuals with diabetic neuropathy (Schulz et al., 2009). The CMS effect, therefore, reflects baroafferent neural traffic from the cardiovascular system. In contrast to the other methods described, the CMS may serve as a methodology to estimate afferent neural signals relayed at the level of the brainstem, since only brainstem processes are involved (arterial baroreflex circuit, acoustic startle circuit). Furthermore, afferent signals from cardiopulmonary baroreceptors, the gastrointestinal system and the respiratory system may also influence the human startle response. Thus, the concept of CMS could eventually be extended to ‘Visceral Modulation of Startle.’ HEPs and CMS are considered psychophysiological indicators of interoceptive signal processing.
Factors Determining Accuracy in Interoception Tasks Differential Aspects of Interoceptive Accuracy A number of sociodemographic factors play a role in the accuracy in interoceptive tasks. In general, results suggest that men are more accurate in interoceptive tasks related to sensations of the cardiovascular, the respiratory or the gastrointestinal system than women. Possible explanations for these effects could be sex differences in vascular musculature or hemispheric lateralization, which also play a role in interoception. The higher proportion of body fat in women than in men could also account for these differences, as it has been shown that individuals with lower body fat perform better in heartbeat perception tasks, and accuracy in these tasks is negatively correlated with BMI (Herbert et al., 2013). Furthermore, Khalsa et al. (2009) have demonstrated that accuracy in heartbeat perception tasks and age show a negative association (r ¼ .30). This correlation could be explained by reduced sympathetic tone, decreased sensitivity of baroreceptors, or reduced arterial stiffness with increasing age. Contrary to
common wisdom, experienced meditators do not show higher accuracy in interoceptive tasks (Khalsa et al., 2008), than normal controls, although they report subjectively increased awareness to bodily states.
Physiological Determinants Arterial baroreceptors represent one important type of interoceptors, which are responsible for cardiac interoception. In response to head-up tilt or isometric exercise, accuracy in heartbeat detection tasks is highly correlated with stroke volume (SV; r ¼ .59) and momentum (r ¼ .67), which represents the product of SV and velocity of blood outflow (Schandry et al., 1993). Furthermore, accuracy in heartbeat detection is associated with the change in the pre-ejection period (PEP) and the cardiac output in response to a mental arithmetic stressor. It could thus be concluded that cardiodynamic parameters, which are considered reflecting inotropic activation (contractility), are positively associated with accuracy in heartbeat detection. Nevertheless, this relationship has not been consistently reported in the literature. Heartbeat perception accuracy is positively related to systolic blood pressure (SBP), but negatively related to heart rate. Typically, there is a negative relationship between heart rate (HR) and SV, except for conditions of extensive exercise or stress. Increased SV, decreased PEP, and increased SBP may generally induce higher stimulation of arterial baroreceptors. Psychophysiological parameters that imply increased stimulation of baroreceptors per single heartbeat are, therefore, positively correlated with accuracy in heartbeat detection tasks (SV[, PEPY, SBP[), while parameters that imply decreased stimulation per heartbeat (HR) show the opposite pattern. Individuals with a high degree of physical training tend to have superior accuracy in heartbeat detection compared with nontrained individuals.
Interoception and Emotions Early Concepts In the original James-Lange theory of emotion, all emotional processes are understood as epiphenomena of visceral activation, which takes place when an individual is confronted with an emotionally relevant stimulus. Nevertheless, this theory has not been empirically supported. According to the modified theory by Cannon and Bard, visceral responses and the genesis of emotions are concurrently elicited through the perception of an emotionally relevant stimulus. Individuals with interrupted transmission of visceral-afferent signals, for example, still experience emotions, although visceral activation is too slow to match the genesis of emotions. In the seminal study by Schachter and Singer (1962) individuals received epinephrine, which drives the sympathetic nervous system, or a placebo substance. One subgroup of participants was informed about the ‘adverse effects’ of the substance, another subgroup was naïve. The authors observed that the informed group attributed their subjective level of arousal to the adverse effects of the drug, while the naïve participants reported a higher intensity of anger after being exposed to anger provocation by an experimenter. These results suggest that both the perception of bodily states and cognitive appraisal are important for the experience of an emotion.
Interoception
Current Point of View Contemporary theories do not assume interoceptive signals as crucial for the experience of emotions anymore. Nevertheless, individuals with spinal cord injury have been found to report reduced intensity of emotions, which suggests that afferent information of bodily states is important, but not a prerequisite for emotion genesis. Current concepts assume that interoceptive neural traffic reaches ‘first order’ central structures, such as the dorsal pontine areas, the AI, and the somatosensory cortex, which may be associated with a phenomenological level of emotional experience. In a ‘second order’ of central representation of interoceptive signals, structures such as the anterior cingulum integrate these genuine interoceptive signals and other sources of bodily information, e.g., somatosensory feedback and attention. Self-reported emotional experience may thus be the consequence of integrating interoceptive signals and other information of bodily states, as well as paying attention to these processes (Wiens, 2005). A large body of evidence indicates that a more intense experience of emotions is positively associated with accurate heartbeat perception. Neuroimaging studies suggest that the processing of interoceptive signals and the experience of emotion share neural structures, such as the AI, the ventromedial prefrontal cortex (VMPFC), and the ACC (Pollatos et al., 2007).
Interocepion and Decision Making Damasio’s Somatic Marker Hypothesis The influential somatic marker hypothesis by Damasio (1994) postulates that interoceptive signals are regularly integrated into processes of decision making. In every context, in which decisions are expected to be made, the outcomes of possible action alternatives are anticipated. This anticipation produces a specific visceral response to be integrated in affective responses to the expected outcome. These responses, either transmitted over somatosensory or visceral-afferent circuits, are called ‘somatic markers.’ Damasio hypothesized that these ‘somatic markers’ shape decision making. The neural structure that is thought to be responsible for the integration and evaluation of somatic markers is the VMPFC. There is a large body of evidence supporting the somatic marker theory. In experimental research, human decision making is assessed through specific paradigms, such as the Iowa Gambling Task. Performance in this task is positively associated with sympathetic responses in anticipation of punishment or reward, putatively reflecting the availability of somatic markers, as well as with accuracy in interoceptive tasks. Patients with neurological damage in the VMPFC do not show comparable electrodermal responses to anticipated punishment or reward (Bechara et al., 1996). Dunn et al. (2006) provide a comprehensive review of the somatic marker hypothesis.
Interoception and Stress Interoceptive Accuracy during and after Acute Laboratory Stressors While interoception describes the transmission of ascending signals on the brain–body axis, stress represents a prominent
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example for descending information on the brain–body axis. Stress and activation drive the two physiological stress systems, the sympathetic–adrenomedullary (SAM) axis including the sympathetic nervous system, and the hypothalamus–pituitary–adrenocortical (HPA) axis with cortisol as final product. Neural and endocrine signaling resulting from the activation of both axes may change the activity of visceral organs (e.g., inotropic and chronotropic effects on the myocardium) and typical brain regions, which are responsible for their perception (e.g., thalamus, insular cortex). Thus it can be argued that interoception and stress are closely linked. Laboratory stress tests are designed to provide a stressful environment that guarantees for a maximal degree of standardization, ecological validity (i.e., cognitive, affective, and behavioral aspects of stress), and effectiveness. However, the direction of the effect of a laboratory stressor on interoceptive accuracy largely depends on the methods used to investigate interoception. Comparing both heartbeat detection tasks, these opposite effects were observed with a strong laboratory stressor, the Socially Evaluated Cold Pressor Test (SECPT) (Schulz et al., 2013a): Stress seems to increase interoceptive accuracy if attention is solely focused on visceral sensations (i.e., heartbeat counting), while it decreases if attention is additionally focused on exteroceptive stimuli (i.e., heartbeat discrimination). One possible conclusion is that stress effects on interoception depend on attentional processes. Evidence on the impact of stress on psychophysiological indicators of interoceptive signal processing is sparse. Acute stress induced by an SECPT was found to change the pattern of the cardiac modulation of startle (Schulz et al., 2011). Two studies investigated the impact of acute laboratory stressors on heartbeat-evoked potentials. A moderate arithmetic stressor could not modulate the HEP amplitude per se, but the HEP was correlated with cardiac responses to the stressor (Gray et al., 2007). Acute pain during a mild version of the cold pressor test attenuated HEP amplitudes (Shao et al., 2011), but possible later effects or relationships to both stress axes were not reported.
Stress Hormones Certain stress hormones are considered to play an important role in the processing of interoceptive signals. First, the activation of the autonomic nervous system may result in a release of catecholamines, such as epinephrine. Although catecholamines do not cross the blood–brain barrier and, therefore, cannot modulate the processing of interoceptive signals at the level of the CNS, epinephrine binds to beta1-adrenergic receptors at the myocardium. The binding of epinephrine to beta1-adrenoceptors causes positive inotropic (increased contractibility), chronotropic (increased heart rate), and dromotropic effects (faster depolarization), which lead to an increase of SV and a decrease of the PEP (Schachinger et al., 2001). It was repeatedly shown that cardiodynamic parameters, such as PEP or SV, are associated with the accuracy in heartbeat detection tasks (Schandry et al., 1993). It is likely that the increased stimulation of arterial baroreceptors caused by increased SV is responsible for this effect. Furthermore, peripheral sympathetic activation induced via beta1-adrenergic
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agents and central sympathetic activity elicited by alpha1-adrenergic agents increases heartbeat perception accuracy (Moor et al., 2005). Second, cortisol, the final product of HPA axis activation, may also have the potential to modulate interoceptive signal processing. A dose of 4 mg of intravenously administered cortisol may induce higher heartbeat-evoked potentials in a state of high alertness compared with a state of low alertness (Schulz et al., 2013b). This effect may feed into a vicious circle of increased attentional focus on physical symptoms, increased anxiety and higher levels of cortisol, which may represent possible psychoneuroendocrine mechanism underlying psychological feed-forward models of somatosensory amplification. Interestingly, cortisol does not affect the cardiac modulation of startle, suggesting that this effect is limited to the cortical representation of interoceptive signals, but does not alter the brainstem processing of afferent bodily signals (Schulz et al., submitted). In contrast to catecholamines, cortisol crosses the blood–brain barrier and affects cells in the entire body, including the CNS. The described results can be attributed to activity in the thalamus, which represents a major relay center for exteroceptive and interoceptive sensory information, and was demonstrated to be affected by cortisol administration. The importance of the HPA axis for altered perception of physical sensations is further underlined by the fact that dysregulation of the HPA axis can be observed in many body-related mental disorders, such as somatoform disorders (Rief and Barsky, 2005) or depression (Terhaar et al., 2012).
Chronic Stress There is very little research on chronic stress and interoception. This is surprising in view of the widely accepted notion that chronic stress exposure causes dysregulation of the SAM and the HPA axes, which in turn are of particular relevance for the above mentioned mental disorders. Clinical data suggests that these dysregulations contribute to the generation of physical symptoms and may thus disrupt the adequate processing of interoceptive signals (Rief and Barsky, 2005). Nevertheless, an association between self-reported chronic stress and interoceptive accuracy in laboratory paradigms has not been demonstrated, as yet (gastric stimulation: Rosenberger et al., 2009; heartbeat detection task: Schulz et al., 2013a). Both studies, however, assessed chronic stress in healthy participants. It remains for future studies to investigate possible abnormalities in interoceptive accuracy in chronically stressed individuals, which may already show SAM and HPA axes dysregulation.
signals are transmitted to the NTS and LC. From these structures, over noradrenergic pathways, beta-adrenergic synapses in the BLA are activated, which induces the release of cyclic adenosine monophosphate (cAMP) and cAMP-dependent protein kinase. Both substances can enhance memory consolidation. Postsynaptic efficacy of beta-adrenergic synapses is increased by glucocorticoids. Results from animal models show that both processes, glucocorticoid secretion and afferent signal transmission from visceral organs, are necessary for memory consolidation. In humans, the increase of baroafferent neural feedback induced by norepinephrine-infusion improved long-term memory (Moor et al., 2005). Interoceptive neural signals, therefore, play an important role for the stress-induced improvement of memory consolidation in animals and humans.
Interoception in Mental Disorders Panic Disorder The most frequently investigated disorder in relation to interoception is panic disorder. In cognitive models of panic disorder it is assumed that panic patients have enhanced selective attention for threat-related stimuli in general and body-related cues in particular. This attentional bias may result in increased interoceptive accuracy. In concordance with this hypothesis, many empirical papers/articles found superior accuracy in heartbeat counting tasks in patients with panic disorder as compared with healthy individuals or other mental disorders (Ehlers and Breuer, 1996). A positive relationship between panic symptoms and interoceptive accuracy has also been observed in children (Eley et al., 2004). Cognitivebehavioral therapy of panic disorder does not change performance in heartbeat perception, but heartbeat perception negatively predicts the outcome of therapeutic intervention (Ehlers and Breuer, 1996). Nevertheless, there are also negative reports, and Willem Van Der Does et al. (2000) conclude from a re-analysis of the data of many of these studies that the majority of patients with panic disorder do not have generally increased accuracy, but only a minority. Moreover, higher accuracy in heartbeat counting tasks was only found when using the standard instruction (“count all heartbeats you feel in the body”) and not in the strict instruction (“count only those heartbeats about which you are sure”) (Ehlers and Breuer, 1996). This highlights the importance of knowledge about one’s own heart rate in panic patients for performing this task, which may be more precise in panic patients, while healthy individuals tend to underestimate their heart rate in this task.
Depression
Interoception in Learning and Memory The model of stress and memory consolidation by McGaugh (2000) postulates that two physiological processes are crucial for the enhancement of memory consolidation after stress: (1) glucocorticoids (rodents: corticosterone; humans: cortisol) that bind on glucocorticoid receptors within the NTS, the locus coeruleus (LC), and the basolateral amygdala (BLA) and (2) peripherally circulating epinephrine, which cannot cross the blood–brain barrier, but activates visceral organs, whose afferent
Affective disorders are often accompanied by autonomic dysregulations, which are also reflected in specific symptoms, such as the disruption of the sleep–wake cycle, dysregulation of appetite, sexual dysfunction, or psychomotor inhibition or agitation. It is plausible that the dysregulation of autonomic processes also induces alterations in the perception of phenomena that are autonomically controlled. Dunn et al. (2007) have reported that individuals with a mild depression may have reduced interoceptive accuracy, while individuals with a severe depression may not differ in their accuracy
Interoception
from healthy controls. However, in this investigation it is unclear whether the difference between both depression groups is due to the severity of disease or to their use of medication, since the number and dosage of antidepressants was notably higher in the severe depression group. A reduction of interoceptive accuracy in major depression is also reflected in a decrease of heartbeat-evoked potentials as compared with healthy control individuals (Terhaar et al., 2012), which may be associated with altered activity in the insular cortex, which could be observed in depressed individuals. Since in a clinical setting there is a substantial overlap of depression and anxiety symptoms, it is not clear to what degree both components may differentially affect interoception. In a student sample it was demonstrated that there is a negative relationship between depression and interoceptive accuracy only in highly anxious individuals (Pollatos et al., 2009), which suggests the more important role of anxiety for interoception. Furthermore, it was reported that anxiety and anhedonia in a subclinical sample interact in that there is a positive relationship between anxiety and interoception only in individuals with low anhedonia (Dunn et al., 2010). Taken together, depressive symptomatology is associated with a tendency for decreased interoceptive accuracy, which may additionally be moderated by anxiety level.
Somatoform Disorders The perception-filter model of somatoform disorders (SD) postulates that hyperactivation of the autonomic nervous system and the HPA axis contribute to increased perception of physical sensations in SD (Rief and Barsky, 2005). Study findings, however, are very mixed. This could be due to the heterogeneity of the conditions classified as SD, some of which emphasize the misperception of bodily signals (e.g., medically unexplained symptoms), while others focus more on medically unestablished health-oriented anxiety (e.g., hypochondria). Even within the field of medically unexplained symptoms (MUS) it is questionable whether individuals with complaints in different organ systems should be classified under the same condition (e.g., cardiovascular symptoms vs. chronic back pain). Furthermore, there is a debate in the literature on the expected direction of the difference between somatoform patients and controls. As summarized by Schaefer et al. (2012), some models assume an increased focus of attention on bodily processes in SD, which may lead to increased accuracy in interoception, while opposing models propose deficient processing of interoceptive signals in SD. Empirical data are in partial support of both hypotheses. On the one hand, Pollatos et al. (2011) found that a mixed group of somatoform patients showed lower accuracy in a heartbeat counting task than a healthy control group. On the other hand, high symptom reporters in the normal population as well as patients with MUS both show less accurate perception of CO2 ratio in the air than healthy individuals (Bogaerts et al., 2010). Schaefer et al. (2012) reported that a mixed somatoform outpatient group and a matched healthy control group did not differ in the accuracy of the heartbeat counting or discrimination task. However, a negative correlation between the number of symptoms and the accuracy in the heartbeat counting task was observed. It can be summarized that there is
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a tendency to observe lower accuracy in interoceptive tasks in patients with MUS. Nevertheless, SD in general and MUS in particular may be characterized by an inappropriateness of processing afferent information from the body. It is questionable whether this deficiency is solely reflected by a quantitative reduction in interoceptive paradigms or if this alteration should not rather be seen as a qualitative change. Moreover, the role of possible dysregulated stress responses in SD, and the role of depression for altered interoception is still neglected in the current literature.
Eating Behavior and Eating Disorders Patients with anorexia nervosa (AN), bulimia nervosa (BN), and binge eating disorder (BED) all report increased subjective awareness to bodily processes. In contrast, patients with AN and BN show lower interoceptive accuracy than healthy controls (Herbert and Pollatos, 2014; Pollatos et al., 2008), while there is no data on patients with BED. One challenge in interoception research with eating disorders is to determine which components of a putatively altered interoception may be attributed to the mental disorder and which may be a physiological and metabolic result of the dysregulated food intake. For instance, the increased interoceptive accuracy in obesity could be a result of an increase in arterial blood pressure. Furthermore, with a quasiexperimental approach of clinical group comparisons, it is impossible to disentangle cause and effect. There is empirical evidence supporting both alternative hypotheses. On the one hand, eating behavior has been experimentally manipulated to assess possible effects on interoception. Short-term fasting was found to increase accuracy in heartbeat counting tasks (Herbert et al., 2012), and the amplitude of heartbeat-evoked potentials (Schulz et al., 2014). While short-term food deprivation induces an increase in sympathetic tone, these effects are inverted in long-term food deprivation. It is, therefore, plausible that long-term fasting, such as observed in AN, may be a way of regulating the perception of bodily sensations. This assumption is also in line with the finding that AN patients show reduced interoceptive accuracy (Pollatos et al., 2008). On the other hand, interoceptive accuracy is positively associated with intuitive eating (Herbert et al., 2013), suggesting that high interoceptive accuracy contributes to healthy eating behavior.
Future Directions In the majority of the studies described, interoception was operationalized using interoceptive tasks, e.g., heartbeat perception tasks, or psychophysiological indicators of interoceptive processing, e.g., heartbeat-evoked potentials. These studies demonstrate linear relationships between accuracy in interoceptive tasks or group comparisons in terms of ‘higher than’ or ‘lower than.’ A careful revision of the literature on stress and interoception, as well as interoception in mental disorders as compared with healthy controls demonstrates that the assumption of linear relationships does not hold. Future research should investigate more complex relationships between interoceptive measures and mental disorders, and also focus on qualitative instead of only quantitative changes in
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interoceptive processing. Another challenge for future research lies in the assessment of different interoception modalities at a time with the same technique (horizontal integration), as well as different levels of the same interoceptive modality (e.g., signals at the level of the brainstem, the cortex, and subjective reports; vertical integration).
See also: Chronic Pain: Models and Treatment Approaches; Co-morbidity of Mental and Physical Conditions; Explanatory Style and Health; Health Risk Perception; Illness Behavior and Care-Seeking; Stress and Cardiac Response; Stress, Coping and Health; Symptom Perception, Awareness and Interpretation.
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