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Heart rate response after emotional picture presentation is modulated by interoceptive awareness.

The perception of visceral signals plays a crucial role in many theories of emotions. The present study was designed to investigate the relationship between interoceptive awareness, emotional experience and heart rate responses in an emotional stimulation paradigm. Based on their performance in a heartbeat perception task 38 participants (16 males, 22 females) were classified as subjects with either high (n=19; 8 males) or low interoceptive awareness (n=19; 8 males). 120 pictures (40 pleasant, 40 unpleasant, 40 neutral slides) from the International Affective Picture System served as emotional stimuli. Heart rate changes were recorded during baseline and during slide presentation. After each slide, the subjects had to rate emotional valence and arousal on a 9-point self-report scale. Statistical analyses revealed significantly stronger heart rate responses to pleasant and unpleasant stimuli in subjects with high interoceptive awareness. Furthermore, subjects with high interoceptive awareness rated pleasant and unpleasant slides as significantly more arousing; no differences were found in the emotional valence ratings. Heartbeat perception scores correlated significantly positive with both the mean arousal rating and with the mean heart rate changes. Our results demonstrate a strong relationship between the perception of cardiac signals and the peripheral processing of emotional stimuli.

Adult↗

Brain structures involved in interoceptive awareness and cardioafferent signal processing: a dipole source localization study.

Afferent signals from the body play an important role for emotional and motivational aspects of behavior. Nevertheless, little is known about the cortical and subcortical structures involved in interoceptive processes. Recently, a functional MRI study demonstrated that insula, somatomotor, and cingulated cortices are activated when subjects focus attention on their heartbeats. Aside from the use of imaging data, cardiac awareness has frequently been studied by using the heartbeat-evoked potential (HEP), a brain wave that appears contingent on the heartbeat. The present study aimed at localizing sources of the HEP. Multichannel EEG was recorded in 44 subjects while they performed a heartbeat perception task. This task was used to quantify interoceptive awareness and to subdivide the subjects into good and poor heartbeat perceivers. Analyses showed highest HEP amplitudes over frontal and frontocentral electrode locations in the time range of later than 200 ms after R-wave onset. By means of a BESA dipole-source-analysis, four sources of the HEP were identified which were located in the anterior cingulate, the right insula, the prefrontal cortex, and the left secondary somatosensory cortex. Good heartbeat perceivers showed both significantly higher HEP amplitudes and higher dipole strength than poor heartbeat perceivers in all four cortical sources. We conclude that the identified structures are involved in the processing of cardiac signals, whereby anterior cingulate and right insula seem to serve as interoceptive centers for cardioception.

Adolescent↗

Yawning: unsuspected avenue for a better understanding of arousal and interoception.

Almost all the vertebrates yawn, testifying the phylogenetic old origins of this behavior. Correlatively speaking, yawning shows an ontogenical precociousness since it occurs as early as 12 weeks after conception and remains relatively unchanged throughout life. Thus, it is contended that these common characteristics and their diencephalic origin allow to model an approach from which emerges a pivotal link between yawning and REM sleep. Yawning and stretching reverse the muscular atonia of the REM-sleep and reopen the collapsed airways. Yawning appears as a powerful muscular stretch, recruiting specific control systems particularly the paraventricular nucleus of the hypothalamus, the locus coeruleus and the reticular activating system from which the vigor of this ancestral vestige, surviving throughout evolution with little variation, may increase arousal. On the other hand, the James-Lange theory proposes that afferent feedback from muscles and viscera provides the brain with a feeling that characterizes the active motivational state and arousal. On this basis and using selected supporting findings from the literature and from data provided by daily life, it is contended that yawning takes part in interoceptiveness by its capacity to increase arousal and self-awareness. Adaptative behaviors depend on interactions among the nervous system and the body by a continuous feedback between them. The body's schema is a main component of the self, and interoceptive process is essential to awareness of the body and arousal. Yawning contributes to bodily consciousness as a behavior affiliating a sensory motor act and his perception from which pleasure is derived. Yawning can be seen as a proprioceptive performance awareness which inwardly provides a pre-reflective sense of one's body and a reappraisal of the body schema. The behavioral consequences of adopting specific regulatory strategies and the neural systems involved act upon attention and cognitive changes.Thus, it is proposed that yawning is a part of interoceptiveness by its capacity to increase arousal and self-awareness.

Animals↗

Interoceptive accuracy and panic.

Psychophysiological models of panic hypothesize that panickers focus attention on and become anxious about the physical sensations associated with panic. Attention on internal somatic cues has been labeled interoception. The present study examined the role of physiological arousal and subjective anxiety on interoceptive accuracy. Infrequent panickers and nonanxious participants participated in an initial baseline to examine overall interoceptive accuracy. Next, participants ingested caffeine, about which they received either safety or no safety information. Using a mental heartbeat tracking paradigm, participants' count of their heartbeats during specific time intervals were coded based on polygraph measures. Infrequent panickers were more accurate in the perception of their heartbeats than nonanxious participants. Changes in physiological arousal were not associated with increased accuracy on the heartbeat perception task. However, higher levels of self-reported anxiety were associated with superior performance.

Adult↗

Interoception: the sense of the physiological condition of the body.

Converging evidence indicates that primates have a distinct cortical image of homeostatic afferent activity that reflects all aspects of the physiological condition of all tissues of the body. This interoceptive system, associated with autonomic motor control, is distinct from the exteroceptive system (cutaneous mechanoreception and proprioception) that guides somatic motor activity. The primary interoceptive representation in the dorsal posterior insula engenders distinct highly resolved feelings from the body that include pain, temperature, itch, sensual touch, muscular and visceral sensations, vasomotor activity, hunger, thirst, and 'air hunger'. In humans, a meta-representation of the primary interoceptive activity is engendered in the right anterior insula, which seems to provide the basis for the subjective image of the material self as a feeling (sentient) entity, that is, emotional awareness.

Afferent Pathways↗

Neural systems supporting interoceptive awareness.

Influential theories of human emotion argue that subjective feeling states involve representation of bodily responses elicited by emotional events. Within this framework, individual differences in intensity of emotional experience reflect variation in sensitivity to internal bodily responses. We measured regional brain activity by functional magnetic resonance imaging (fMRI) during an interoceptive task wherein subjects judged the timing of their own heartbeats. We observed enhanced activity in insula, somatomotor and cingulate cortices. In right anterior insular/opercular cortex, neural activity predicted subjects' accuracy in the heartbeat detection task. Furthermore, local gray matter volume in the same region correlated with both interoceptive accuracy and subjective ratings of visceral awareness. Indices of negative emotional experience correlated with interoceptive accuracy across subjects. These findings indicate that right anterior insula supports a representation of visceral responses accessible to awareness, providing a substrate for subjective feeling states.

Acoustic Stimulation↗

Interoceptive and integrative contributions of forebrain and brainstem to energy balance control.

An anatomically distributed model of energy balance control contrasts with the widely held hypothalamic center model. The distributionist model is recommended by the observations that the caudal brainstem contains critical interoceptive, integrative and neurochemical mediating functions. A prominent example of interoceptive function is sensitivity to the adipose tissue-derived hormone, leptin. To complement the well established focus on hypothalamic leptin receptors (Ob-Rb), we describe an extensive distribution of Ob-Rb in the brainstem. These receptors, moreover, are functionally relevant given the intake suppressive effects of fourth-intracerebroventricular (i.c.v) and brainstem intraparenchymal (in dorsal vagal complex) delivery. A wide variety of intake relevant peptides receptors are found in hypothalamus, but these receptors are also widely distributed in the caudal brainstem. As an example of the functional relevance of these neurochemical mediators, we describe ingestive effects of ligands for melanocortin 3/4 and corticotrophin-releasing hormone receptors obtained with brainstem ventricular and parenchymal (dorsal vagal complex and parabrachial nucleus) delivery. It is clear that responses obtained from hypothalamic treatments can arise independently from stimulation of caudal brainstem receptors. We have used the chronic decerebrate preparation to ask whether the brainstem contains integrative substrates sufficient to mediate behavioral responses to variations in physiological state. The experiments reveal that the brainstem is indeed sufficient for the integration of taste and gastrointestinal signals that co-determine the size of meals in the short term. Decerebrate rats, however, do not respond to food deprivation or to reductions in the number of daily feeding opportunities. These results suggest that the brainstem in neural isolation from forebrain influence is not sufficient for ingestive response to systemic/metabolic signals that affect intake over the long term. The relative contribution of brainstem and forebrain substrates to long-term intake and body weight control in the neurologically intact animal, remains unclear. The data reviewed support a distributed anatomical model of energy balance and recommend increased attention to specific responses (behavioral, autonomic and endocrine) that are mediated by local (brainstem or forebrain) interoceptive and integrative processes, and those requiring bi-directional interactions.

Animals↗

Interoception: the inside story--a model for psychosomatic processes.

OBJECTIVE: To comprehend psychosomatic processes, it will be necessary to understand the brain's influences on bodily functions and also the body's afferent sensory input to the central nervous system, including the effects of this input on behavior and cognitive functions, especially emotion. The objective of this Presidential Address is to review what is known circa the year 2000 of the processes and mechanisms of visceral sensory psychobiology, often called interoception. METHODS: Over 1000 publications that have appeared since the 19th century were reviewed to prepare this review, including a group that are specifically cited here. RESULTS: Factors and data were reviewed that were identified as germane to understanding interoception. These included definitional issues, historical roots, the neural basis, studies and results in the cardiovascular-respiratory and alimentary-gastrointestinal systems, studies of emotion, and studies in people with mental disorders. Drug and hormone effects, pain, proprioception, and phantom limb or organ factors, and the role of awareness were briefly described. Methodological issues, methods of study including functional imaging, and possible future directions for study were identified. CONCLUSIONS: Understanding the physical basis of psychosomatic processes, including the so-called mind-body problem, will require a detailed understanding the psychobiology of interoception.

Brain↗

Chronic ethanol consumption by C57BL/6 mice promotes tolerance to its interoceptive cues and increases extracellular dopamine, an effect blocked by naltrexone.

BACKGROUND: C57BL/6 (B6) mice voluntarily consume ethanol. Although preingestive factors might be accountable, the fact that B6 mice voluntarily consume sufficient ethanol to set the conditions for an ethanol-deprivation effect suggest that post-ingestive pharmacological induced changes also occur. In this study, we determined the amounts of ethanol voluntarily consumed by B6 mice and associated blood ethanol levels (BEL), the effects of this consumption on extracellular dopamine (DA) and how this was altered by naltrexone, as well as on its interoceptive discriminative cues. METHODS: In experiment 1, the amounts of 12% ethanol consumed at 2, 4, and 6 hr into the active phase of the circadian cycle and associated BEL were determined. In experiment 2, dialysate samples were collected for 1 hr to establish basal DA levels. Mice were then injected with saline or naltrexone (6 mg/kg) and given access to water and 12% ethanol or to water only, and samples were collected at 20-min intervals for the next 2 hr. In experiment 3, mice were trained to discriminate ethanol's interoceptive cues via operant techniques, and half were given 3 weeks access to ethanol and water, the other half water only. Ethanol-consuming and water control mice were again tested for their ability to discriminate the drug's interoceptive cues. RESULTS: Mice ingested nearly 6 g/kg of ethanol and attained BEL near 100 mg/100 mL by 6 hr into the active phase. Ethanol intake at 2-hr into the dark phase was approximately 2.5 g/kg, and increased DA to approximately 100% above basal levels. Naltrexone reduced ethanol consumption and blocked the DA increase. Ethanol consumption for 3 weeks attenuated its discriminative cues. CONCLUSIONS: B6 mice voluntarily consume sufficient ethanol (1) to produce intoxicating BEL; (2) to increase DA levels in nucleus accumbens, an effect blocked by naltrexone; and (3) to attenuate its discriminative cues.

Alcoholism↗

Regional brain activation due to pharmacologically induced adrenergic interoceptive stimulation in humans.

OBJECTIVE: Identifying the brain regions associated with visceral sensory activation and awareness (interoception) was a neglected area of neural science until quite recently despite being essential to a comprehensive understanding of psychosomatic processes, baroreception, and higher brain functions such as fear and anxiety, other emotions, and pain. METHODS: In this study regional changes in the cerebral metabolic rate for glucose were determined with positron emission tomography in response to cardiovascular-respiratory activation induced in healthy humans by beta-adrenergic stimulation produced with intravenous isoproterenol, which acts predominantly in the periphery because of minimal transport across the blood-brain barrier. RESULTS: Interoceptive activation raised heart rate to approximately 120 beats per minute, produced somatic and to a lesser extent psychological symptoms, and significantly increased cerebral glucose metabolism in the left primary somatosensory cortex and medial portion of the cingulate gyrus; right insular cortex showed a trend toward an increase that was significant in homogeneous subgroups of right-handed or female subjects. CONCLUSIONS: These results demonstrate the involvement of specific brain regions as well as hemispheric laterality of function in visceral perception, and they suggest that during emotional reactions involving changes in visceral organ function, activation of some of the brain regions observed could be due specifically to interoceptive processes.

Adrenergic beta-Agonists↗

Self-exposure therapy for panic disorder with agoraphobia: randomised controlled study of external v. interoceptive self-exposure.

BACKGROUND: Exposure to external phobic cues is an effective therapy for panic/agoraphobia but the value of exposure to interoceptive cues is unclear. AIMS: Randomised controlled comparison in panic/agoraphobia of the effects of (a) external, (b) interceptive or (c) combined external and interoceptive self-exposure to (d) control subjects. METHOD: Eighty out-patients were randomised to a control group or to one of three forms of self-exposure treatment (external, interoceptive, or combined). Each treatment included seven sessions over 10 weeks and daily self-exposure homework. Assessments were at pre- and post-treatment and up to 1 year post-entry. Assessors remained blind during treatment. RESULTS: The three self-exposure groups improved significantly and similarly at post-treatment and up to 1-year followup, and significantly more than did the control subjects. Rates of improvement on main outcome measures averaged 60% at post-treatment and 77% at follow-up. CONCLUSIONS: The three methods of self-exposure were equally effective in reducing panic and agoraphobic symptoms in the short- and long-term.

Adolescent↗

Modulation and experience of external stimuli: toward a science of experience and interoception.

The concept of interoception can be found in various writing over the past 100 or more years dating back to Sherrington, James and Lange. Professor György Adám that made American scientists increasingly aware of the importance of interoception with his 1967 book Interoception and Behavior. In this article we want to discuss two areas of research from out laboratory that have been influenced from this perspective. First, we will focus on electrocortical correlates of error detection during visuo-motor task and examine the manner in which an individual becomes aware of making an error as well as the way in which this awareness directs behavior on an ongoing basis. Second, we will examine hypnotic modulation of the pain experience and describe the manner in which electrocortical processes reflect the modulation and experience of pain. In this discussion, we suggest the importance of the anterior cingulate in not only modulating these processes in particular but also in its more general role as an interface between the limbic system and the neocortex and the integration of cognitive with emotional stimuli.

Electroencephalography↗

Changes in the number of EEG-paroxysms, and in the ongoing and instant frequencies of neurones from one population under the effect of a series of interoceptive stimuli.

The changes in the number of EEG-paroxysms and in the average ongoing and instant frequencies of the neuronal discharges from one population (GS or VPL) under the effect of series of mechanoreceptor stimulations of the stomach, are studied simultaneously in acute experiments on cats. The application of a large number of interoceptive stimuli is found to increase the after-effect and the cumulative effect at macro- and micro-levels. The changes in the ongoing and instant frequencies, accompanying the rise in number of the EEG-paroeysms suggest increased excitation of the neurones under the effect of the interoceptive stimulations. No qualitative changes characteristic of the pathologic epileptic neurones are observed. The result obtained give evidence that the paroxysms formed under the effect of adequate interoceptive stimuli, are a manifestation of changes in the excitability of the nervous system, which do not exceed the limits of pysiological homeostasis.

Animals↗

Serotonin receptor subtype mediation of the interoceptive discriminative stimuli induced by 5-methoxy-N,N-dimethyltryptamine.

Male Wistar rats were trained to discriminate the interoceptive effects of 5-methoxy-N,N-dimethyltryptamine (5-OMe-DMT; 1.25 mg/kg, IP) from saline in a two-lever operant chamber. Following discrimination learning, the following drugs (with ED50 dose in mg/kg IP) dose-dependently generalized: lysergic acid diethylamide (LSD, 0.04), 8-hydroxy-2-(di-n-propylamino) tetralin (8-OH-DPAT, 0.11), 6-methoxy-4-(dipropyl-amino)-1,3,4,5-tetrahydrobenz(c,d)indole hydrochloride (BAY R 1531, 0.15), 5-OMe-DMT itself (0.63), ipsapirone (TVX Q 7821, 2.7), and buspirone (3.8). The potencies of these drugs in generalization tests were best correlated with their binding affinities for the 5-HT1A serotonin receptor subtype (as measured by displacement of 3H-ipsapirone in the hippocampus). Drugs not, or only partially generalizing included quipazine, bufotenin, m-trifluoromethylphenylpiperazine (TFMPP), 5-methoxy-3(1,2,3,6-tetrahydropyridine-4-yl)-1H-indole succinate (RU 24969), citalopram, clomipramine, 1,4-dihydro-2,6-dimethyl-3-nitro-4(2-trifluoromethylphenyl)-pyridine-5- carboxylate (BAY K 8644), the buspirone metabolite 1-pyrimidinyl-piperazine (1-PP), methysergide, metergoline, and metitepine. Of the last three compounds with antagonistic activity at 5-HT receptors, as well as ketanserin, pizotifen, and ritanserin, only metitepine and pindolol could fully block the 5-OMe-DMT stimulus. Pizotifen blocked the generalization of quipazine fully, that of 5-OMe-DMT only partially, and that of ipsapirone not at all. These data indicate that the 5-HT1A receptor subtype is strongly involved in the transduction of the interoceptive discriminative stimuli induced by 5-OMe-DMT, with 5-HT2 agonism also playing a possible role.

Animals↗

Cyclical processes in neuronal populations of the cat somatosensory cortex during extero- and interoceptive activation and in the course of its extinction.

The EEG reactions were recorded in chronic experiments in awake cats and the slow periodic changes in the frequency of the multicellular impulse activity were observed at points (standard localization) of the somatosensory (1) zone of the cortex. Results of the analysis of both processes were combined in graphs in a single time scale. The correlation of the expressivity of the activation reaction and degree of modulation of the cyclical fluctuations of the frequency of the impulse activity were followed both during the action of exteroceptive (conditional, light; unconditional, sound) and the interoceptive (mechanical and chemical) stimuli. A particular characteristic of the interoceptive stimulation as compared with the exteroceptive consisted in the inertia of the respondent reaction and the lesser contrast in relation to the background. During the extinction of the responses the decrease in the activation reaction correlated with a decrease in the initial (after the switching on of the stimulus) fluctuation of the frequency of the multicellular impulse activity. The data obtained serves as proof of the unity of the two processes: the regulation of the activation of the brain and the regulation of the periodicity of the neuronal impulse activity.

Acoustic Stimulation↗

Participation of interoceptive afferent impulses in polymodal responses of superior collicular neurons in the cat.

Experiments on immobilized, unanesthetized cats showed that interoceptive afferent impulses reaching the brain via the vagus nerves evoke marked responses in, on average, 43% of superior collicular neurons. Both excitatory and inhibitory effects were observed. The latter were found more often during single stimulation of the vagus nerve. In half of the cases the inhibitory responses were characterized by the development of initial inhibition, clearly limited in time to between 180 and 1700 msec. Changes in spike activity of 60% of units were tonic in character. The onset of phasic responses with an initial period of activation was observed in only 9-11% of neurons. The number of these cells and also the total number of responding neurons were greater than when series of stimuli were applied to the vagus nerve. In individual cells during prolonged repetitive stimulation of the nerve gradual weakening of the responses took place. Somatic stimulation evoked mainly the development of phasic responses of excitatory type. Most of the neurons tested were bimodal and often the temporal structure of their responses was determined by the modality of the stimulus applied. The functional role of the changes discovered in spontaneous activity of superior collicular neurons under interoceptive influences and the central mechanisms of realization of such influences on the activity of the neuronal system in this brain structure are discussed.

Afferent Pathways↗

Behavioral analysis and treatment of reflexive vomiting associated with visceral sensations: a case study of interoceptive conditioning?

Behavior analytic methods are applied to the conceptualization and treatment of a complex case of interoceptive classical conditioning. The subject exhibited a gagging and vomiting response to bladder and/or similar visceral sensations. A two-factor learning model of the problem led to a successful exposure and response prevention intervention, which was based on single-case experimental methodology. We discuss the possible relevance of this case in the context of the growing attention to interoceptive conditioning in behavioral problems, and comment upon the importance of behavior analytic principles and procedures to the behavioral clinician.

Avoidance Learning↗

Panic attacks and interoceptive acuity for cardiac sensations.

It has been suggested that perception of visceral changes, and cognitive reactions to such changes, may be important for triggering panic attacks. It remains to be determined, however, whether people with panic attacks are actually characterized by enhanced perceptual acuity for interoceptive stimuli. The purpose of this study was to explore the relationship between panic attacks and awareness for cardiac sensations using an objective heartbeat discrimination procedure. Twenty panickers and 20 nonpanickers were given 60 trials of the Whitehead heartbeat discrimination procedure. Thirty trials were given during rest and 30 following hyperventilation. Results indicated that panic attacks were not related to enhanced interoceptive acuity for cardiac sensations, either at rest or following hyperventilation. These results are discussed in terms of their relevance to cognitive models of panic.

Adult↗