Interoception and Mental Health: a Roadmap

Interoception and Mental Health: a Roadmap

Interoception and mental health: a roadmap Article (Published Version) Khalsa, Sahib S, Adolphs, Ralph, Cameron, Oliver G, Critchley, Hugo D, Davenport, Paul W, Feinstein, Justin S, Feusner, Jamie D, Garfinkel, Sarah N, Lane, Richard D, Mehling, Wolf E, Meuret, Alicia E, Nemeroff, Charles B, Oppenheimer, Stephen, Petzschner, Frederike H, Pollatos, Olga et al. (2018) Interoception and mental health: a roadmap. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 3 (6). pp. 501-513. ISSN 24519022 This version is available from Sussex Research Online: http://sro.sussex.ac.uk/id/eprint/74442/ This document is made available in accordance with publisher policies and may differ from the published version or from the version of record. If you wish to cite this item you are advised to consult the publisher’s version. Please see the URL above for details on accessing the published version. Copyright and reuse: Sussex Research Online is a digital repository of the research output of the University. Copyright and all moral rights to the version of the paper presented here belong to the individual author(s) and/or other copyright owners. To the extent reasonable and practicable, the material made available in SRO has been checked for eligibility before being made available. Copies of full text items generally can be reproduced, displayed or performed and given to third parties in any format or medium for personal research or study, educational, or not-for-profit purposes without prior permission or charge, provided that the authors, title and full bibliographic details are credited, a hyperlink and/or URL is given for the original metadata page and the content is not changed in any way. http://sro.sussex.ac.uk Biological Psychiatry: Review CNNI Interoception and Mental Health: A Roadmap Sahib S. Khalsa, Ralph Adolphs, Oliver G. Cameron, Hugo D. Critchley, Paul W. Davenport, Justin S. Feinstein, Jamie D. Feusner, Sarah N. Garfinkel, Richard D. Lane, Wolf E. Mehling, Alicia E. Meuret, Charles B. Nemeroff, Stephen Oppenheimer, Frederike H. Petzschner, Olga Pollatos, Jamie L. Rhudy, Lawrence P. Schramm, W. Kyle Simmons, Murray B. Stein, Klaas E. Stephan, Omer Van den Bergh, Ilse Van Diest, Andreas von Leupoldt, Martin P. Paulus, and the Interoception Summit 2016 participants ABSTRACT Interoception refers to the process by which the nervous system senses, interprets, and integrates signals originating from within the body, providing a moment-by-moment mapping of the body’s internal landscape across conscious and unconscious levels. Interoceptive signaling has been considered a component process of reflexes, urges, feelings, drives, adaptive responses, and cognitive and emotional experiences, highlighting its contributions to the maintenance of homeostatic functioning, body regulation, and survival. Dysfunction of interoception is increasingly recognized as an important component of different mental health conditions, including anxiety disorders, mood disorders, eating disorders, addictive disorders, and somatic symptom dis- orders. However, a number of conceptual and methodological challenges have made it difficult for interoceptive constructs to be broadly applied in mental health research and treatment settings. In November 2016, the Laureate Institute for Brain Research organized the first Interoception Summit, a gathering of interoception ex- perts from around the world, with the goal of accelerating progress in understanding the role of interoception in mental health. The discussions at the meeting were organized around four themes: interoceptive assessment, interoceptive integration, interoceptive psychopathology, and the generation of a roadmap that could serve as a guide for future endeavors. This review article presents an overview of the emerging consensus generated by the meeting. Keywords: Biomarker, Computational psychiatry, Interoception, Mental health, Research Domain Criteria, Treatment https://doi.org/10.1016/j.bpsc.2017.12.004 Interoception refers collectively to the processing of internal ASSESSMENT bodily stimuli by the nervous system. Parcellation of the nervous system’s processing of sensory signals into inter- Body Systems of Interoception oception, proprioception, and exteroception began more Interoceptive processing occurs across all major biological than 100 years ago (1), although it was predated by interest systems involved in maintaining bodily homeostasis, including in linking body–brain interactions with conscious experience the cardiovascular (9,10), pulmonary (11), gastrointestinal (2,3). Scientific interest in interoception has fluctuated (12,13), genitourinary (14), nociceptive (15), chemosensory (Figure 1A). During the 1980s, biological psychiatry was (16), osmotic (17), thermoregulatory (18), visceral1 (19), immune inundated with observations of interoceptive disturbances in (20,21), and autonomic systems (22,23) (Table 1). There has panic disorder (4–7), although the trend receded after it became clear that the etiological mechanism was broader 1 Visceroception has classically referred to the perception of bodily than a single molecular receptor target (8). Recent years signals arising specifically from visceral organs, such as the have witnessed a surge of interest on the topic of inter- heart, lungs, stomach, intestines, and bladder, along with other fi oception due in part to ndings highlighting its integral role internal organs in the trunk of the body (19). It did not include in emotional experience, self-regulation, decision making, organs such as the skin and skeletal muscle, in contrast to and consciousness. Importantly, interoception is not limited contemporary definitions of interoception that typically en- to conscious perception or even unique to the human spe- compasses signals from both the viscera and all other tissues cies. From this perspective, interdisciplinary efforts to un- that relay a signal to the central nervous system about the derstand different features of interoception have been current state of the body, including the skin and skeletal/ essential for advancing progress in cognitive and clinical smooth muscle fibers, via lamina I spinothalamic afferents neuroscience (Figure 1B). (41,138,139). ª 2017 Society of Biological Psychiatry. Published by Elsevier Inc. This is an open access article under the 1 CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). ISSN: 2451-9022 Biological Psychiatry: Cognitive Neuroscience and Neuroimaging - 2018; -:-–- www.sobp.org/BPCNNI Biological Psychiatry: CNNI Interoception and Mental Health A Figure 1. (A) Number of English language pub- lications per year on interoception from PubMed, PsycINFO, and Institute for Science Information Web of Knowledge. The timeline starts in 1905, one year before the publication of Charles Sherrington’s book, The Integrative Action of the Nervous Sys- tem, which first defined the concept of inter- oception. Key historical events relevant to interoception science are superimposed. (B) Pub- lications per year on interoception vs. those inves- tigating features of interoception that do not specifically refer to the term. These latter publica- tions are more numerous and arise mainly from basic neuroscience, physiology, and subspecialty disciplines within the biomedical field. Note the use of a logarithmic scale in the second panel. [Figure reproduced and modified with permission from Khalsa and Lapidus (33).] B been relatively little focus overall on the integration across many insights have been gained by the application of nonin- bodily systems; thus, it is not surprising that most in- vasive approaches within neuroscience and psychological vestigations of the topic have been siloed within distinct assessment contexts (29) (see “Eavesdropping on Brain–Body research areas or scientific disciplines [see (24,25) for note- Communication” section below). worthy exceptions]. Importance of an Interoceptive Taxonomy Features of Interoception There is no generally agreed-on taxonomy for interoception Interoception is not a simple process but rather has several science. Variable definitions have made it difficult to identify facets (26). The act of sensing, interpreting, and integrating the features under investigation, let alone evaluate the quality information about the state of inner body systems can be of the findings. Based on the number of physiological systems related to different elements such as interoceptive attention, involved, it could be questioned whether the terms “inter- detection, discrimination, accuracy, insight, sensibility, and oception” and “interoceptive awareness” are too broad. self-report (Table 2). However, most interoceptive processes Interoceptive awareness is an umbrella term that was first used occur outside the realm of conscious awareness. Consciously to describe a self-report subscale (30), but it has subsequently experienced elements are measured clinically via subjective been used to encompass any (or all) of the different inter- report, and there are few observable interoceptive signs (e.g., oception features accessible to conscious self-report. Re- heart rate, respiration rate, pupillary dilation, flushing, perspi- searchers from different fields developed definitions that only ration, piloerection, nociceptive reflexes) (Table 3). Experi- partially overlapped, reflecting the need for operationalization mental approaches can quantify different body systems and in neuroscience (31,32) and clinical practice (33,34). Here we features of interoceptive processing. Nevertheless,

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