Multisensory integration across exteroceptive and interoceptive domains modulates self-experience in the rubber-hand illusion

doi:10.1016/J.NEUROPSYCHOLOGIA.2013.08.014

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Multisensory integration across exteroceptive and interoceptive domains modulates self-experience in the rubber-hand illusion

Journal Article•DOI•

Multisensory integration across exteroceptive and interoceptive domains modulates self-experience in the rubber-hand illusion

Keisuke Suzuki¹, Sarah N. Garfinkel², Sarah N. Garfinkel¹, Hugo D. Critchley², Hugo D. Critchley¹, Anil K. Seth¹ - Show less +2 more•Institutions (2)

University of Sussex¹, Brighton and Sussex Medical School²

01 Nov 2013-Neuropsychologia (Neuropsychologia)-Vol. 51, Iss: 13, pp 2909-2917

TL;DR: It is demonstrated that both subjective and objective measures of virtual-hand ownership are enhanced by cardio-visual feedback in-time with the actual heartbeat, as compared to asynchronous feedback.

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About: This article is published in Neuropsychologia.The article was published on 2013-11-01 and is currently open access. It has received 347 citations till now. The article focuses on the topics: Multisensory integration & Illusion.

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Journal Article•DOI•

Interoceptive inference, emotion, and the embodied self

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Anil K. Seth¹•Institutions (1)

University of Sussex¹

01 Nov 2013-Trends in Cognitive Sciences

TL;DR: A predictive, inferential perspective on interoception: 'interoceptive inference' conceives of subjective feeling states (emotions) as arising from actively-inferred generative (predictive) models of the causes of interoceptive afferents.

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1,104 citations

Journal Article•DOI•

Knowing your own heart: distinguishing interoceptive accuracy from interoceptive awareness.

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Sarah N. Garfinkel¹, Sarah N. Garfinkel², Anil K. Seth², Adam B. Barrett², Keisuke Suzuki², Hugo D. Critchley¹ - Show less +2 more•Institutions (2)

Brighton and Sussex Medical School¹, University of Sussex²

01 Jan 2015-Biological Psychology

TL;DR: Empirical support for dissociation between dimensions of interoceptive accuracy, sensibility and awareness is provided and set the context for defining how the relative balance of accuracy, Sensibility and Awareness dimensions explain cognitive, emotional and clinical associations of interOceptive ability.

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846 citations

Journal Article•DOI•

Active interoceptive inference and the emotional brain

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Anil K. Seth¹, Karl J. Friston²•Institutions (2)

University of Sussex¹, Wellcome Trust Centre for Neuroimaging²

19 Nov 2016-Philosophical Transactions of the Royal Society B

TL;DR: A recent shift in conceptions of interoception and its relationship to hierarchical inference in the brain is reviewed, highlighting its enactivist (embodied) aspects and the key role of uncertainty or precision and how this might translate into neuromodulation.

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Abstract: We review a recent shift in conceptions of interoception and its relationship to hierarchical inference in the brain. The notion of interoceptive inference means that bodily states are regulated by...

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470 citations

Journal Article•DOI•

Interoception and emotion.

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Hugo D. Critchley¹, Hugo D. Critchley², Sarah N. Garfinkel²•Institutions (2)

University of Sussex¹, Brighton and Sussex Medical School²

01 Oct 2017-Current opinion in psychology

TL;DR: This work describes the afferent signalling, central processing, and neural and mental representation of internal bodily signals in interoception, and describes the recognition of dissociable psychological dimensions of interoceptions.

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Abstract: Influential theories suggest emotional feeling states arise from physiological changes from within the body. Interoception describes the afferent signalling, central processing, and neural and mental representation of internal bodily signals. Recent progress is made in conceptualizing interoception and its neural underpinnings. These developments are supported by empirical data concerning interoceptive mechanisms and their contribution to emotion. Fresh insights include description of short-term interoceptive effects on neural and mental processes (including fear-specific cardiac effects), the recognition of dissociable psychological dimensions of interoception, and models of interoceptive predictive coding that explain emotions and selfhood (reinforced by structural anatomical models and brain and experimental findings). This growing grasp of interoception is enriching our understanding of emotion and its disorders.

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379 citations

Cites background from "Multisensory integration across ext..."

...For example individuals that perform well on heartbeat detection tasks (good ‘interoceptive accuracy’), are less susceptible to the deleterious impact of cardiac signals at systole signals on memory encoding [36], yet in other contexts show an enhanced processing of self-related signals [39]....
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Journal Article•DOI•

Interoception, contemplative practice, and health.

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Norman A. S. Farb¹, Jennifer Daubenmier², Cynthia J. Price³, Tim Gard⁴, Catherine E. Kerr⁵, Barnaby D. Dunn⁶, Anne Carolyn Klein⁷, Martin P. Paulus⁸, Wolf E. Mehling² - Show less +5 more•Institutions (8)

University of Toronto¹, University of California, San Francisco², University of Washington³, Maastricht University⁴, Brown University⁵, University of Exeter⁶, Rice University⁷, University of California, San Diego⁸

09 Jun 2015-Frontiers in Psychology

TL;DR: It is concluded that maladaptive construal of bodily sensations may lie at the heart of many contemporary maladies, and that contemplative practices may attenuate these interpretative biases, restoring a person’s sense of presence and agency in the world.

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Abstract: Interoception can be broadly defined as the sense of signals originating within the body. As such, interoception is critical for our sense of embodiment, motivation, and well-being. And yet, despite its importance, interoception remains poorly understood within modern science. This paper reviews interdisciplinary perspectives on interoception, with the goal of presenting a unified perspective from diverse fields such as neuroscience, clinical practice, and contemplative studies. It is hoped that this integrative effort will advance our understanding of how interoception determines well-being, and identify the central challenges to such understanding. To this end, we introduce an expanded taxonomy of interoceptive processes, arguing that many of these processes can be understood through an emerging predictive coding model for mind-body integration. The model, which describes the tension between expected and felt body sensation, parallels contemplative theories, and implicates interoception in a variety of affective and psychosomatic disorders. We conclude that maladaptive construal of bodily sensations may lie at the heart of many contemporary maladies, and that contemplative practices may attenuate these interpretative biases, restoring a person's sense of presence and agency in the world.

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376 citations

Cites background from "Multisensory integration across ext..."

...Furthermore, mindfulness training appears to alter interoceptive attention tendencies, focusing attention on interoceptive sensations rather than cognitive appraisals of such sensations (Garland et al., 2012), in keeping with a model in which contemplative practices shift regulatory strategy from…...
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...…in body ownership show that a sense of one’s body can be manipulated by experimentally induced visual and tactile feedback (Ainley et al., 2013; Suzuki et al., 2013) but those with greater interoceptive accuracy (as assessed by heartbeat detection) are less susceptible to illusions of…...
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References

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Journal Article•DOI•

Controlling the false discovery rate: a practical and powerful approach to multiple testing

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Yoav Benjamini, Yosef Hochberg

01 Jan 1995-Journal of the royal statistical society series b-methodological

TL;DR: In this paper, a different approach to problems of multiple significance testing is presented, which calls for controlling the expected proportion of falsely rejected hypotheses -the false discovery rate, which is equivalent to the FWER when all hypotheses are true but is smaller otherwise.

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Abstract: SUMMARY The common approach to the multiplicity problem calls for controlling the familywise error rate (FWER). This approach, though, has faults, and we point out a few. A different approach to problems of multiple significance testing is presented. It calls for controlling the expected proportion of falsely rejected hypotheses -the false discovery rate. This error rate is equivalent to the FWER when all hypotheses are true but is smaller otherwise. Therefore, in problems where the control of the false discovery rate rather than that of the FWER is desired, there is potential for a gain in power. A simple sequential Bonferronitype procedure is proved to control the false discovery rate for independent test statistics, and a simulation study shows that the gain in power is substantial. The use of the new procedure and the appropriateness of the criterion are illustrated with examples.

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83,420 citations

"Multisensory integration across ext..." refers methods in this paper

...To explore this, we conducted planned t-tests comparing synchronous vs. asynchronous feedback in each condition, correcting for multiple comparisons using the false discovery rate (pFDR, Benjamini & Hochberg, 1995)....
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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

"Multisensory integration across ext..." refers background in this paper

...This region has been proposed as a neural substrate for self-awareness in the form of the “material me” (Craig, 2009), and is activated by mismatches between predicted and actual interoceptive signals induced by false physiological feedback (Gray, Harrison, Wiens, & Critchley, 2007)....
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...The right-hemisphere anterior insular cortex provides one cortical focus for the integration of exteroceptive and interoceptive signals (Craig, 2009; Critchley & Harrison, 2013; Critchley et al., 2004; Seth et al., 2011)....
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...A separate tradition emphasizes the importance of interoception – the sense of the internal physiological state of the body – in underpinning the sense of self (Craig, 2009; Critchley, Wiens, Rotshtein, Ohman, & Dolan, 2004; Damasio, 2010; Seth, Suzuki, & Critchley, 2011)....
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Journal Article•DOI•

Whatever next? Predictive brains, situated agents, and the future of cognitive science

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Andrew G. Clark¹•Institutions (1)

University of Edinburgh¹

01 Jun 2013-Behavioral and Brain Sciences

TL;DR: This target article critically examines this "hierarchical prediction machine" approach, concluding that it offers the best clue yet to the shape of a unified science of mind and action.

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Abstract: Brains, it has recently been argued, are essentially prediction machines. They are bundles of cells that support perception and action by constantly attempting to match incoming sensory inputs with top-down expectations or predictions. This is achieved using a hierarchical generative model that aims to minimize prediction error within a bidirectional cascade of cortical processing. Such accounts offer a unifying model of perception and action, illuminate the functional role of attention, and may neatly capture the special contribution of cortical processing to adaptive success. This target article critically examines this "hierarchical prediction machine" approach, concluding that it offers the best clue yet to the shape of a unified science of mind and action. Sections 1 and 2 lay out the key elements and implications of the approach. Section 3 explores a variety of pitfalls and challenges, spanning the evidential, the methodological, and the more properly conceptual. The paper ends (sections 4 and 5) by asking how such approaches might impact our more general vision of mind, experience, and agency.

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3,640 citations

"Multisensory integration across ext..." refers methods in this paper

...Essentially, the predictive coding view adapts to the case of self-perception the “Bayesian brain” framework, which describes perception as the process of inference about the most likely causes of sensory input (Clark, 2013; Friston, 2009)....
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...predictive coding view adapts to the case of self-perception the “Bayesian brain” framework, which describes perception as the process of inference about the most likely causes of sensory input (Clark, 2013; Friston, 2009)....
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Journal Article•DOI•

Rubber hands ‘feel’ touch that eyes see

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Matthew Botvinick¹, Jonathan D. Cohen¹•Institutions (1)

Carnegie Mellon University¹

19 Feb 1998-Nature

TL;DR: An illusion in which tactile sensations are referred to an alien limb is reported, which reveals a three-way interaction between vision, touch and proprioception, and may supply evidence concerning the basis of bodily self-identification.

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Abstract: Illusions have historically been of great use to psychology for what they can reveal about perceptual processes. We report here an illusion in which tactile sensations are referred to an alien limb. The effect reveals a three-way interaction between vision, touch and proprioception, and may supply evidence concerning the basis of bodily self-identification.

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3,422 citations

"Multisensory integration across ext..." refers background or methods in this paper

...In the “rubber hand illusion” (RHI), the stroking of an artificial hand synchronously with a participant's real hand, while visual attention is focused on the artificial hand, leads the participant to experience the artificial hand as part of his or her own body (Botvinick & Cohen, 1998)....
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...…conflicts between vision, touch, and proprioception are minimized by visual capture of visual and felt (tactile) events occurring in close peri-hand space, on the basis of statistical correlations among sensory signals together with visual dominance (Botvinick & Cohen, 1998; Makin et al., 2008)....
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...The first four questions were adapted from Botvinick and Cohen (1998), [Q1–Q4] and were designed to assess the strength of the subjective experience of virtual hand ownership....
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Journal Article•DOI•

Neural systems supporting interoceptive awareness.

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Hugo D. Critchley¹, Stefan Wiens, Pia Rotshtein¹, Arne Öhman, Raymond J. Dolan¹ - Show less +1 more•Institutions (1)

University College London¹

01 Feb 2004-Nature Neuroscience

TL;DR: In right anterior insular/opercular cortex, neural activity predicted subjects' accuracy in the heartbeat detection task and local gray matter volume correlated with both interoceptive accuracy and subjective ratings of visceral awareness.

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Abstract: 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.

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2,972 citations

"Multisensory integration across ext..." refers background in this paper

...The right-hemisphere anterior insular cortex provides one cortical focus for the integration of exteroceptive and interoceptive signals (Craig, 2009; Critchley & Harrison, 2013; Critchley et al., 2004; Seth et al., 2011)....
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