Keeping the body in mind: insula functional organization and functional connectivity integrate interoceptive, exteroceptive, and emotional awareness.

doi:10.1002/HBM.22113

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Keeping the body in mind: insula functional organization and functional connectivity integrate interoceptive, exteroceptive, and emotional awareness.

Journal Article•DOI•

Keeping the body in mind: insula functional organization and functional connectivity integrate interoceptive, exteroceptive, and emotional awareness.

W. Kyle Simmons¹, W. Kyle Simmons², Jason A. Avery², Joel C. Barcalow², Jerzy Bodurka², Wayne C. Drevets², Wayne C. Drevets³, Patrick S.F. Bellgowan¹, Patrick S.F. Bellgowan² - Show less +5 more•Institutions (3)

University of Tulsa¹, McGovern Institute for Brain Research², University of Oklahoma³

01 Nov 2013-Human Brain Mapping (Hum Brain Mapp)-Vol. 34, Iss: 11, pp 2944-2958

TL;DR: This work provides the first experimental demonstration that there exists a functional topography across the insula, with distinct regions in the same participants responding in a highly selective fashion for interoceptive, exteroception, and affective processing.

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Abstract: Relatively discrete experimental literatures have grown to support the insula's role in the domains of interoception, focal exteroceptive attention and cognitive control, and the experience of anxiety, even as theoretical accounts have asserted that the insula is a critical zone for integrating across these domains. Here we provide the first experimental demonstration that there exists a functional topography across the insula, with distinct regions in the same participants responding in a highly selective fashion for interoceptive, exteroceptive, and affective processing. Although each insular region is associated with areas of differential resting state functional connectivity relative to the other regions, overall their functional connectivity profiles are quite similar, thereby providing a map of how interoceptive, exteroceptive, and emotional awareness are integrated within the insular cortex.

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Journal Article•DOI•

Interoceptive predictions in the brain

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Lisa Feldman Barrett¹, W. Kyle Simmons²•Institutions (2)

Harvard University¹, McGovern Institute for Brain Research²

01 Jul 2015-Nature Reviews Neuroscience

TL;DR: The Embodied Predictive Interoception Coding model is introduced, which integrates an anatomical model of corticocortical connections with Bayesian active inference principles, to propose that agranular visceromotor cortices contribute to interoception by issuing interoceptive predictions.

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Abstract: Intuition suggests that perception follows sensation and therefore bodily feelings originate in the body. However, recent evidence goes against this logic: interoceptive experience may largely reflect limbic predictions about the expected state of the body that are constrained by ascending visceral sensations. In this Opinion article, we introduce the Embodied Predictive Interoception Coding model, which integrates an anatomical model of corticocortical connections with Bayesian active inference principles, to propose that agranular visceromotor cortices contribute to interoception by issuing interoceptive predictions. We then discuss how disruptions in interoceptive predictions could function as a common vulnerability for mental and physical illness.

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996 citations

Journal Article•DOI•

Evidence for a Large-Scale Brain System Supporting Allostasis and Interoception in Humans.

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Ian R. Kleckner¹, Jiahe Zhang¹, Alexandra Touroutoglou², Lorena Chanes¹, Lorena Chanes², Chenjie Xia², W. Kyle Simmons³, W. Kyle Simmons⁴, Karen S. Quigley¹, Karen S. Quigley⁵, Bradford C. Dickerson², Lisa Feldman Barrett¹, Lisa Feldman Barrett² - Show less +9 more•Institutions (5)

Northeastern University¹, Harvard University², McGovern Institute for Brain Research³, University of Tulsa⁴, Edith Nourse Rogers Memorial Veterans Hospital⁵

24 Apr 2017-Nature Human Behaviour

TL;DR: This work uses tract-tracing studies of macaque monkeys, followed by two intrinsic functional magnetic resonance imaging samples, to evaluate the existence of an intrinsic allostatic–interoceptive system in the human brain and demonstrates its relation to regulating peripheral systems in the body, called allostasis.

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Abstract: Large-scale intrinsic brain systems have been identified for exteroceptive senses (e.g., sight, hearing, touch). We introduce an analogous system for representing sensations from within the body, called interoception, and demonstrate its relation to regulating peripheral systems in the body, called allostasis. Employing the recently introduced Embodied Predictive Interoception Coding (EPIC) model, we used tract-tracing studies of macaque monkeys, followed by two intrinsic functional magnetic resonance imaging samples (N = 280 and N = 270) to evaluate the existence of an intrinsic allostatic/interoceptive system in the human brain. Another sample (N = 41) allowed us to evaluate the convergent validity of the hypothesized allostatic/interoceptive system by showing that individuals with stronger connectivity between system hubs performed better on an implicit index of interoceptive ability related to autonomic fluctuations. Implications include insights for the brain's functional architecture, dissolving the artificial boundary between mind and body, and unifying mental and physical illness.

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374 citations

Journal Article•DOI•

Major depressive disorder is associated with abnormal interoceptive activity and functional connectivity in the insula

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Jason A. Avery¹, Jason A. Avery², Wayne C. Drevets², Wayne C. Drevets³, Scott E. Moseman², Scott E. Moseman⁴, Jerzy Bodurka⁴, Jerzy Bodurka², Joel C. Barcalow², W. Kyle Simmons¹, W. Kyle Simmons² - Show less +7 more•Institutions (4)

University of Tulsa¹, McGovern Institute for Brain Research², Johnson & Johnson³, University of Oklahoma⁴

01 Aug 2014-Biological Psychiatry

TL;DR: Activity within the insula during the interoceptive attention task was negatively correlated with both depression severity and somatic symptom severity in depressed subjects, and major depressive disorder was associated with greater resting-state functional connectivity between the dmIC and limbic brain regions implicated previously in MDD.

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338 citations

Cites background or methods from "Keeping the body in mind: insula fu..."

...Likewise, hemodynamic activity increases in mid-insular cortex in human subjects performing tasks involving visceral interoceptive attention (15,25,26) or direct visceral stimulation (27,28)....
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...Functional Connectivity Analyses Because our primary interests were group differences in interoception-related brain activity and earlier studies demonstrated homeostatic sensitivity and selectivity for interoceptive attention in the dmIC (15,24), this region was used as the seed for...
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...Notably, the mid-insula regions underlying interoception appear at least partially dissociable from dorsal and ventral anterior insula regions involved in cognitive and emotional processing, respectively (15), suggesting the hypothesis that multiple insula regions play distinct roles in the symptoms expressed in MDD, with somatic abnormalities observed in MDD conceivably resulting either from mood- and anxiety-related pathophysiology within the insula (29–32) or from abnormal visceral afferent input into this region (13)....
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...Depressed subjects (ma compared with healthy subjects (HC) within multiple brain regions during atten were observed in bilateral dorsal mid-insula cortex (dmIC) and bilateral orbit group differences in heartbeat interoception within the insula were confined to representation within the insula (15)....
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...We have previously demonstrated in healthy adults that this task is effective at mapping interoceptive regions in the insula (15)....
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Journal Article•DOI•

The multisensory basis of the self: From body to identity to others

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Manos Tsakiris¹•Institutions (1)

Royal Holloway, University of London¹

01 Apr 2017-Quarterly Journal of Experimental Psychology

TL;DR: The primary aim of this review article is to highlight recent advances in the study of body ownership and the understanding of the underlying neurocognitive processes in three ways, motivating a unified model of the self inspired by current predictive coding models.

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Abstract: By grounding the self in the body, experimental psychology has taken the body as the starting point for a science of the self. One fundamental dimension of the bodily self is the sense of body owne...

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236 citations

Cites background from "Keeping the body in mind: insula fu..."

...…that the interoceptive and the exteroceptive sides of the bodily self are integrated from the posterior to anterior subregions across the insular cortex (Simmons et al., 2013), which seems to underpin the experience of this body as mine, an experience that is the hallmark of the bodily self....
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...These findings suggest that the interoceptive and the exteroceptive sides of the bodily self are integrated from the posterior to anterior subregions across the insular cortex (Simmons et al., 2013), which seems to underpin the experience of this body as mine, an experience that is the hallmark of the bodily self....
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Journal Article•DOI•

Can Interoception Improve the Pragmatic Search for Biomarkers in Psychiatry

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Sahib S. Khalsa¹, Sahib S. Khalsa², Rachel C. Lapidus³, Rachel C. Lapidus²•Institutions (3)

College of Health Sciences, Bahrain¹, McGovern Institute for Brain Research², University of Tulsa³

25 Jul 2016-Frontiers in Psychiatry

TL;DR: It is concluded that interoception represents a viable avenue for clinical and translational research in psychiatry, with a well-established conceptual framework, a neural basis, measurable biomarkers, interdisciplinary appeal, and transdiagnostic targets for understanding and improving mental health outcomes.

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Abstract: Disrupted interoception is a prominent feature of the diagnostic classification of several psychiatric disorders. However, progress in understanding the interoceptive basis of these disorders has been incremental and the application of interoception in clinical treatment is currently limited to panic disorder. To examine the degree to which the scientific community has recognized interoception as a construct of interest, we identified and individually screened all articles published in the English language on interoception and associated root terms in Pubmed, Psychinfo and ISI Web of Knowledge. This search revealed that interoception is a multifaceted process that is being increasingly studied within the fields of psychiatry, psychology, neuroscience and biomedical science. To illustrate the multifaceted nature of interoception we provide a focused review of one of the most commonly studied interoceptive channels, the cardiovascular system, and give a detailed comparison of the most popular methods used to study cardiac interoception. We subsequently review evidence of interoceptive dysfunction in panic disorder, depression, somatic symptom disorders, anorexia nervosa, and bulimia nervosa. For each disorder, we suggest how interoceptive predictions constructed by the brain may erroneously bias individuals to express key symptoms and behaviors, and outline questions that are suitable for the development of neuroscience-based mental health interventions. We conclude that interoception represents a viable avenue for clinical and translational research in psychiatry, with a well-established conceptual framework, a neural basis, measurable biomarkers, interdisciplinary appeal, and transdiagnostic targets for understanding and improving mental health outcomes.

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213 citations

Cites background from "Keeping the body in mind: insula fu..."

...One noteworthy exception may be the combination of interoceptive attention tasks with functional neuroimaging, which have demonstrated insula activation in health samples (14, 15) as well as psychiatric patient samples (157, 162, 235)....
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...A recently developed minimalistic approach involves measuring brain activity while participants simply attend to the feeling of their heartbeat sensation (14)....
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References

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Open Access

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Book•

Descartes' Error: Emotion, Reason, and the Human Brain

[...]

Antonio R. Damasio

01 Jan 1994

TL;DR: The authors argued that rational decisions are not the product of logic alone - they require the support of emotion and feeling, drawing on his experience with neurological patients affected with brain damage, Dr Damasio showed how absence of emotions and feelings can break down rationality.

...read moreread less

Abstract: Descartes' Error offers the scientific basis for ending the division between mind and body. Antonio Damasio contends that rational decisions are not the product of logic alone - they require the support of emotion and feeling. Drawing on his experience with neurological patients affected with brain damage, Dr Damasio shows how absence of emotions and feelings can break down rationality. He also offers a new perspective on what emotions and feelings actually are: a direct view of our own body states; a link between the body and its survival-oriented regulation on the one hand, and consciousness on the other. Written as a conversation between the author and an imaginary listener, Descartes' Error leads us to conclude that human organisms are endowed from their very beginning with a spirited passion for making choices, which the social mind can then use to build rational behaviour.

...read moreread less

9,648 citations

Journal Article•DOI•

Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control

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William W. Seeley¹, Vinod Menon, Alan F. Schatzberg, Jennifer Keller, Gary H. Glover, Heather A. Kenna, Allan L. Reiss, Michael D. Greicius² - Show less +4 more•Institutions (2)

University of California, San Francisco¹, Stanford University²

28 Feb 2007-The Journal of Neuroscience

TL;DR: Two distinct networks typically coactivated during functional MRI tasks are identified, anchored by dorsal anterior cingulate and orbital frontoinsular cortices with robust connectivity to subcortical and limbic structures, and an “executive-control network” that links dorsolateral frontal and parietal neocortices.

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Abstract: Variations in neural circuitry, inherited or acquired, may underlie important individual differences in thought, feeling, and action patterns. Here, we used task-free connectivity analyses to isolate and characterize two distinct networks typically coactivated during functional MRI tasks. We identified a "salience network," anchored by dorsal anterior cingulate (dACC) and orbital frontoinsular cortices with robust connectivity to subcortical and limbic structures, and an "executive-control network" that links dorsolateral frontal and parietal neocortices. These intrinsic connectivity networks showed dissociable correlations with functions measured outside the scanner. Prescan anxiety ratings correlated with intrinsic functional connectivity of the dACC node of the salience network, but with no region in the executive-control network, whereas executive task performance correlated with lateral parietal nodes of the executive-control network, but with no region in the salience network. Our findings suggest that task-free analysis of intrinsic connectivity networks may help elucidate the neural architectures that support fundamental aspects of human behavior.

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6,049 citations

"Keeping the body in mind: insula fu..." refers background in this paper

...Finally, evidence has accrued that the anterior insula may be part of a domain-general, ‘‘multiple demand’’ network of brain regions that support task-level control and focal attention to salient stimuli [Dosenbach et al., 2007; Duncan and Owen, 2000; Menon and Uddin, 2010; Nelson et al., 2010; Seeley et al., 2007; Sterzer and Kleinschmidt, 2010]....
[...]
...…may be part of a domain-general, ‘‘multiple demand’’ network of brain regions that support task-level control and focal attention to salient stimuli [Dosenbach et al., 2007; Duncan and Owen, 2000; Menon and Uddin, 2010; Nelson et al., 2010; Seeley et al., 2007; Sterzer and Kleinschmidt, 2010]....
[...]

Journal Article•DOI•

How do you feel--now? The anterior insula and human awareness.

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A.D. (Bud) Craig¹•Institutions (1)

Barrow Neurological Institute¹

01 Jan 2009-Nature Reviews Neuroscience

TL;DR: New findings suggest a fundamental role for the AIC (and the von Economo neurons it contains) in awareness, and thus it needs to be considered as a potential neural correlate of consciousness.

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Abstract: The anterior insular cortex (AIC) is implicated in a wide range of conditions and behaviours, from bowel distension and orgasm, to cigarette craving and maternal love, to decision making and sudden insight. Its function in the re-representation of interoception offers one possible basis for its involvement in all subjective feelings. New findings suggest a fundamental role for the AIC (and the von Economo neurons it contains) in awareness, and thus it needs to be considered as a potential neural correlate of consciousness.

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5,279 citations

"Keeping the body in mind: insula fu..." refers background or result in this paper

...These findings appear to support theories [Craig, 2009; Damasio, 1993; Singer et al., 2009] positing the existence of multiple hierarchically organized insula regions underlying ‘‘meta-representations’’ of the body’s homeostatic state....
[...]
...One possibility derives from the aforementioned theories of Craig and Damasio positing hierarchically organized regions within the insula representing information about the body’s homeostatic state [Craig, 2002, 2009; Damasio, 1993]....
[...]
...For both Damasio and Craig [Craig, 2009; Damasio, 1993], these socalled ‘‘somatic markers’’ give rise to the emotionally textured sentience colloquially described as the ‘‘self’’....
[...]
...…are made aware of interoceptive sensations, including thirst, air hunger, heartbeat detection, and distension of the esophagus, stomach, bladder, or rectum [for reviews see (Craig, 2002; Craig, 2009)], as well as evidence that insula damage impairs interoceptive awareness [Khalsa et al., 2009]....
[...]
...VC 2012 Wiley Periodicals, Inc. of experimental tasks in healthy humans, and abnormal- ities of insular function have been reported in populations manifesting a variety of psychiatric or neurological disor- ders [Craig, 2009]....
[...]

Journal Article•DOI•

How do you feel? Interoception: the sense of the physiological condition of the body.

[...]

A.D. (Bud) Craig¹•Institutions (1)

Barrow Neurological Institute¹

01 Aug 2002-Nature Reviews Neuroscience

TL;DR: Functional anatomical work has detailed an afferent neural system in primates and in humans that represents all aspects of the physiological condition of the physical body that might provide a foundation for subjective feelings, emotion and self-awareness.

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Abstract: As humans, we perceive feelings from our bodies that relate our state of well-being, our energy and stress levels, our mood and disposition. How do we have these feelings? What neural processes do they represent? Recent functional anatomical work has detailed an afferent neural system in primates and in humans that represents all aspects of the physiological condition of the physical body. This system constitutes a representation of 'the material me', and might provide a foundation for subjective feelings, emotion and self-awareness.

...read moreread less

4,673 citations

"Keeping the body in mind: insula fu..." refers background in this paper

...…are made aware of interoceptive sensations, including thirst, air hunger, heartbeat detection, and distension of the esophagus, stomach, bladder, or rectum [for reviews see (Craig, 2002; Craig, 2009)], as well as evidence that insula damage impairs interoceptive awareness [Khalsa et al., 2009]....
[...]
...This insular region is near the terminus of the ascending neural pathway that carries information from the viscera through the nucleus of the solitary tract, and on to the ventral medial nucleus of the thalamus, before arriving in the mid-dorsal insula [Craig, 2002]....
[...]
...One possibility derives from the aforementioned theories of Craig and Damasio positing hierarchically organized regions within the insula representing information about the body’s homeostatic state [Craig, 2002, 2009; Damasio, 1993]....
[...]
...…middle aspects of the insula receive substantial, reciprocal projections with the surrounding somatosensory cortex, and also receive nociceptive, thermal, and visceral afferent projections that convey interoceptive information about bodily states important for homeostatic regulation [Craig, 2002]....
[...]

Journal Article•DOI•

Descartes' Error: Emotion, Reason and the Human Brain

[...]

Sean A Spence

06 May 1995-BMJ

TL;DR: Brain books are similarly popular: humans are considered from a pathological/laboratory perspective and computer metaphors abound (your mind is your software!) and there are boxes and arrows in profusion.

...read moreread less

Abstract: Antonio R Damasio Picador, pounds sterling16.99, pp 312 ISBN 0 330 33927 3 Documentary makers find the brain sexy at present; surf the television channels and the workings of the psyche are hard to avoid: violence, paraphilias, psychopathy, all are explained. Brain books are similarly popular. They come in three varieties. There is the “you're only” school: you're only a cluster of neurons (Francis Crick), processes (Daniel Dennett), microtubules (Sir Roger Penrose) and so on in a reductionist vein. Humans are considered from a pathological/laboratory perspective. Computer metaphors abound (your mind is your software!) and there are boxes and arrows in profusion. Such books …

...read moreread less

4,386 citations

"Keeping the body in mind: insula fu..." refers background in this paper

...Neuroanatomical tract-tracing studies demonstrate that the posterior and middle aspects of the insula receive substantial, reciprocal projections with the surrounding somatosensory cortex, and also receive nociceptive, thermal, and visceral afferent projections that convey interoceptive information about bodily states important for homeostatic regulation [Craig, 2002]....
[...]
...These findings appear to support theories [Craig, 2009; Damasio, 1993; Singer et al., 2009] positing the existence of multiple hierarchically organized insula regions underlying ‘‘meta-representations’’ of the body’s homeostatic state....
[...]
...One possibility derives from the aforementioned theories of Craig and Damasio positing hierarchically organized regions within the insula representing information about the body’s homeostatic state [Craig, 2002, 2009; Damasio, 1993]....
[...]
...Left anterior insula involvement has been reported previously in neuroimaging studies of worry [Shin et al., 2000], and multiple neuroimaging studies suggest preferential left > right anterior insula activation during tasks of emotional processing and awareness [Campbell-Sills et al., 2011; Craig, 2009]....
[...]
...This theoretical account is well supported by experiments demonstrating insula activation when participants are made aware of interoceptive sensations, including thirst, air hunger, heartbeat detection, and distension of the esophagus, stomach, bladder, or rectum [for reviews see (Craig, 2002; Craig, 2009)], as well as evidence that insula damage impairs interoceptive awareness [Khalsa et al., 2009]....
[...]