Gastrointestinal Interoception in Eating Disorders: Charting a New Path

Current Psychiatry Reports https://doi.org/10.1007/s11920-022-01318-3 EATING DISORDERS (S WONDERLICH AND S ENGEL, SECTION EDITORS) Gastrointestinal Interoception in Eating Disorders: Charting a New Path Sahib S. Khalsa1,2 · Laura A. Berner3 · Lisa M. Anderson4 Accepted: 12 November 2021 © The Author(s) 2022 Abstract Purpose of Review Abnormal interoception has been consistently observed across eating disorders despite limited inclusion in diagnostic conceptualization. Using the alimentary tract as well as recent developments in interoceptive neuroscience and predictive processing as a guide, the current review summarizes evidence of gastrointestinal interoceptive dysfunction in eating disorders. Recent Findings Eating is a complex process that begins well before and ends well after food consumption. Abnormal prediction and prediction-error signals may occur at any stage, resulting in aberrant gastrointestinal interoception and dysregulated gut sensations in eating disorders. Several interoceptive technologies have recently become available that can be paired with computational modeling and clinical interventions to yield new insights into eating disorder pathophysiology. Summary Illuminating the neurobiology of gastrointestinal interoception in eating disorders requires a new generation of studies combining experimental probes of gut physiology with computational modeling. The application of such techniques within clinical trials frameworks may yield new tools and treatments with transdiagnostic relevance. Keywords Anorexia nervosa · Bulimia nervosa · Binge-eating disorder · Avoidant/restrictive food intake disorder · Interoceptive awareness · Digestion Introduction Eating disorders are psychiatric conditions characterized by aberrant eating and compensatory behavior patterns that are associated with severe medical complications, psychological comorbidities, and increased mortality [1]. Neurobiological models of eating disorders commonly emphasize the role of interactions among psychological traits and various This article is part of the Topical Collection on Eating Disorders * Sahib S. Khalsa 1 Laureate Institute for Brain Research, 6655 South Yale Ave, Tulsa, OK 74136, USA 2 Oxley College of Health Sciences, University of Tulsa, Tulsa, OK, USA 3 Department of Psychiatry, Icahn School of Medicine at Mount Sinai, New York, NY, USA 4 Department of Psychiatry and Behavioral Sciences, University of Minnesota Medical School, Minneapolis, MN, USA cognitive functions (e.g., cognitive control, habit-learning), value processing (e.g., reward learning), and affective functioning (e.g., fear learning/generalization) [2–6]. Although interoceptive signaling is often linked with these processes, less attention is paid to the role of interoception. The current review critically re-evaluates the role of interoception in eating disorders, with a focus on gastrointestinal interoception. It is organized around the potential points of altered interoception throughout the gastrointestinal tract and considers the associated implications for eating disorders.1 While prior reviews have touched on the role of interoception in eating disorders [7–9], gastrointestinal symptoms [10, 11], or related processes such as hunger/thirst [12], here we emphasize the importance of understanding gastrointestinal interoception through the lens of predictive processing, whereby the nervous system is engaged in predicting upcoming states in relation to current states, and 1 There are also emerging suggestions that the microbiome plays a role in eating disorders. However, the complexities of this “world within a world” combined with a limited knowledge of microbiomehost interactions at the level of interoceptive signaling renders this topic too early for us to review. 13 Vol.:(0123456789) Current Psychiatry Reports refining these predictions via error signaling. Finally, we highlight several methodological developments relevant to the study of gastrointestinal interoception and discuss their implications for advancing the clinical understanding and treatment of eating disorders. Interoception Overview 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 [13]. Interoception has traditionally been considered to be a one-way street in which “bottom-up” signals traveling from the body to the brain cause sensation and elicit “top-down” regulatory responses when bodily homeostasis is disrupted [14••]. More recently, interoception has been adopted into the conceptual framework of Bayesian inference (a method of statistical inference in which new observations are used to continuously update or infer the statistical probability that a hypothesis/outcome may be true), based on the premise that afferent sensory input to the brain is constantly shaped and modified by the individual’s expectations [15–18]. Thus, interoception can be reconceptualized as a bidirectional process between the brain and the body, with feedback and feedforward loops that constantly update an internal model aimed at predicting and regulating future states of the body [19••]. Despite these theoretical advances and evidence supporting the idea that the brain and the body cannot be fully understood when studied separately, most explanatory neuroscientific approaches attempting to understand cognitive, emotional, and behavioral functioning in eating disorders have not integrated these two dimensions. Neurobiology of Interoception The brain sits at the interface between the external world, which it samples through the exteroceptive senses, and the inner world of the body, which it accesses through interoceptive sensory channels. Interoceptive brain regions play primary roles in directly mapping the autonomic, chemosensory, endocrine, and immune systems, which relay information through peripheral nerves and direct neurochemical interfaces to the brainstem, hypothalamus, thalamus, and ultimately into cortical sectors including principally the insular and somatosensory cortices (for a detailed review see [14••]). The processing of information across these channels occurs in a hierarchical fashion, with multiple feedback loops starting in the autonomic nervous system and lower brainstem [20], providing a scaffold to delineate peripheral from central interoceptive dysfunction. 13 Perceptual Inference and Predictive Processing While distinct from interoception, perceptual inference is an overlapping construct referring to the process by which a person generates beliefs or explanations about the causes and effects of events occurring in the world [21]. Perceptual inferences are strongly influenced by expectations. They may be explicit or implicit and can rapidly change depending on the environmental context. Eating disorders are conditions t (...truncated)