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

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.Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use: http://www.nature.com/authors/editorial_policies/license.html#terms * Corresponding authors: ian_kleckner@urmc.rochester.edu, l.barrett@neu.edu. ǂ Shared senior authorshipAuthor contributions: The study was designed by all the authors, analyzed by all the authors, and the manuscript was written by I.R.K. and L.F.B with comments and edits from other authors. Competing interests:The authors declare no competing interests. HHS Public AccessAuthor manuscript Nat Hum Behav. Author manuscript; available in PMC 2017 October 24.Published in final edited form as: Nat Hum Behav. 2017 ; 1: . doi:10.1038/s41562-017-0069. Author Manuscript Author ManuscriptAuthor Manuscript Author ManuscriptThe brain contains intrinsic systems for processing exteroceptive sensory inputs from the world, such as vision, audition, and proprioception/touch (e.g., 1 ). Accumulating evidence indicates that these systems work via the principles of predictive coding (e.g., 2-7 ), where sensations are anticipated and then corrected by sensory inputs from the world. The brain, as a generative system, models the world by predicting, rather than reacting to, sensory inputs.Predictions guide action and perception by continually constructing possible representations of the immediate future based on their prior probabilities relative to the present context 8,9 . We and others have recently begun studying the hypothesis that ascending sensory inputs from the organs and systems within the body's internal milieu are similarly anticipated and represented (i.e., autonomic visceral and vascular function, neuroendocrine fluctuations, and neuroimmune function) [10][11][12][13][14][15][16] . These sensations are referred to as interoception [17][18][19] .Engineering studies of neural design 20 , alo...

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“…Within the brain, different interoceptive channels share common regional neural substrates that likely permit integrative processing toward (predictive) representations that might ultimately direct adaptive behaviour [10]. However, not all signals are integrated with other modialties: Organ-specific and signal-selective afferent representations are present in insular cortex and associated 'interoceptive' cortical regions [4].…”

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“…Importantly, the EPIC model’s Bayesian predictive coding perspective asserts that interoception and homeostatic–allostatic control are unified within an integrated neural architecture centered around the insula and the agranular visceromotor cortices to which it is highly connected [10,33]. Using both past experiences (empirical prior probabilities in Bayesian terms) and prediction error signals received from the mid/posterior insula, agranular visceromotor circuitry estimates the body’s upcoming autonomic, metabolic and immunological needs given the demands of the current context.…”

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“…At time t, a cascade of predicted experience (light blue) is initiated in the limbic cortices of the allostatic/interoceptive network [14]; incoming sensory input (in this simplified example, from primary visual cortex) is anticipated, so there is no prediction error. At t+1 , predictions in light blue are compared against input (prediction error, darker blue); differences may be incorporated into updated predictions (darker blue, t+2 ).…”