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Interoceptive predictions in the brain

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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Figure 1: Intracortical architecture and intercortical connectivity for predictive coding.

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Acknowledgements

The authors thank M. Á. García-Cabezas for helpful discussions and advice in preparing figure 1. They also thank K. Friston, H. Barbas, B. Finlay, H. Mayberg, J. Feinstein, S. Khalsa, J. Avery, M. Paulus, A. Satpute, L. Chanes, A. Touroutoglou and I. Kleckner for helpful discussions about the EPIC model and comments offered on the manuscript. In addition, they thank L. Chanes, A. Touroutoglou and J. Zhang for their assistance in summarizing the interoceptive system from the macaque tract-tracing literature. This work was supported by a US National Institute on Aging grant (R01AG030311), a US National Science Foundation grant (BCS-1052790) and contracts from the US Army Research Institute for the Behavioural and Social Sciences (contracts W5J9CQ-12-C-0049 and W5J9CQ-11-C-0046) to L.F.B., as well as a US National Institute of Mental Health grant (K01MH096175-01), a US National Alliance for Research on Schizophrenia and Depression (NARSAD) Young Investigator Award, and funding from the Oklahoma Tobacco Research Center to W.K.S. The views, opinions and findings contained in this article are those of the authors and should not be construed as an official position, policy or decision of the US National Institutes of Health or Department of the Army unless so designated by other documents.

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Supplementary information

Supplementary information S1

Strengths of the structural model (PDF 169 kb)

Supplementary information S2

An example of how interoceptive perceptions arise in the brain (PDF 105 kb)

Supplementary information S3

Implications for Theories of Emotion (PDF 205 kb)

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Glossary

Agranular cortex

An isocortical region with a relatively undifferentiated layer II and layer III and lacking a fully expressed layer IV.

Allostasis

The process of activating physiological systems (such as hormonal, autonomic or immune systems) with the aim of returning the body to homeostasis.

Bayesian approach to probability

Models for assessing the probability of an event (that is, the posterior probability) based on the prior likelihood of an event and the evidence currently available as to its existence.

Centrifugal

A proposed hierarchical organization whereby the agranular and heteromodal association cortices form a collection of hubs, from which connections to unimodal sensory systems can be depicted as concentric rings.

Corollary discharge

Signals generated by the motor cortex that influence or inhibit the sensory processing of self-generated motor actions. Such signals convey simultaneous 'efference copies' of motor commands to sensory regions.

Default mode network

(DMN). A collection of midline and parietal brain regions that show more activity when people are constructing representations of the past and the future, simulating the present or processing semantic and conceptual content.

Degeneracy

The capacity of a system to perform identical functions or yield identical outputs with structurally different sets of elements.

Deterministic models

Mathematical models in which, given initial conditions or parameter values, there is no variation in the outcome.

Dysgranular cortex

An isocortical region defined by the presence of a differentiated layer II and layer III, and a rudimentary layer IV that contains stellate granule cells receiving thalamocortical inputs.

Granular cortex

An isocortical region with six differentiated layers, including a well-defined layer IV that contains many stellate granule cells receiving thalamocortical inputs.

Homeostasis

A set of dynamic functions (not a single set point) that interact to maintain an optimal use of energy in the body across all conditions at all times.

Interoception

The perception and integration of autonomic, hormonal, visceral and immunological homeostatic signals that collectively describe the physiological state of the body.

Interoceptive sensations

Activity within the nervous system indexing the autonomic, hormonal, visceral and immunological homeostatic signals that collectively describe the physiological state of the body — for example, concerning vagal signals, levels of insulin or cortisol, heart rate, gastric distension or inflammatory cytokine levels.

Lamina I pathway

Small-diameter sensory fibres that carry ascending interoceptive sensory signals (about muscle contractions in blood vessels, temperature, pain, hormonal activity, immunological inflammation and other variables) in the lateral spinothalamic pathway.

Positive alliesthesia

Transformation of a sensation from aversive to pleasurable, depending on the homeostatic needs of the body.

Precision units

Pyramidal cells that represent prediction-error signals; these cells modulate the activity of other neurons within a cortical column according to confidence in the predictions or the reliability of the incoming sensory signals.

Vagus nerve

Cranial nerve X, which carries ascending interoceptive sensory information about internal organs and the enteric nervous system.

Visceromotor cortices

Agranular regions of isocortex and allocortex that modulate the regulation of the autonomic nervous system as well as of the hormonal and immune systems.

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Barrett, L., Simmons, W. Interoceptive predictions in the brain. Nat Rev Neurosci 16, 419–429 (2015). https://doi.org/10.1038/nrn3950

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