Interoception of breathing and its relationship with anxiety

Olivia K Harrison,Laura Köchli,Stephanie Marino,Roger Luechinger,Franciszek Hennel,Katja Brand,Alexander J Hess,Stefan Frässle,Sandra Iglesias,Fabien Vinckier,Frederike H Petzschner,Samuel J Harrison,Klaas E Stephan

doi:10.1016/j.neuron.2021.09.045

Abstract

SummaryInteroception, the perception of internal bodily states, is thought to be inextricably linked to affective qualities such as anxiety. Although interoception spans sensory to metacognitive processing, it is not clear whether anxiety is differentially related to these processing levels. Here we investigated this question in the domain of breathing, using computational modeling and high-field (7 T) fMRI to assess brain activity relating to dynamic changes in inspiratory resistance of varying predictability. Notably, the anterior insula was associated with both breathing-related prediction certainty and prediction errors, suggesting an important role in representing and updating models of the body. Individuals with low versus moderate anxiety traits showed differential anterior insula activity for prediction certainty. Multi-modal analyses of data from fMRI, computational assessments of breathing-related metacognition, and questionnaires demonstrated that anxiety-interoception links span all levels from perceptual sensitivity to metacognition, with strong effects seen at higher levels of interoceptive processes.

Highlights

We perceive the world through our body
Results overview Below we present the results from each of our task modalities: questionnaires, a breathing perception and metacognition task, and a novel interoceptive learning task, in which group-wise comparisons between each of the measures of interest were conducted
The results from the questionnaires and filter detection task (FDT) are contextualized by previous findings related to anxiety, while the results from the breathing learning task (BLT) were validated against an additional unseen dataset and the relationship with anxiety was assessed

Summary

Introduction

We perceive the world through our body. questions regarding how we sense and interpret our external environment (exteroception) have been highly prominent across centuries of research, the importance and cognitive mechanisms of monitoring our internal environment have only more recently gained traction within the neuroscience community (Barrett and Simmons, 2015; Craig, 2002; Seth, 2013; Tsakiris and Critchley, 2016). ‘‘Interoception,’’ the perception of our body and inner physiological condition (Seth, 2013), constitutes a fundamental component of cerebral processes for maintaining bodily homeostasis (Berntson and Khalsa, 2021; Chen et al, 2021; Pezzulo et al, 2015; Quigley et al, 2021; Stephan et al, 2016). Questions regarding how we sense and interpret our external environment (exteroception) have been highly prominent across centuries of research, the importance and cognitive mechanisms of monitoring our internal environment have only more recently gained traction within the neuroscience community (Barrett and Simmons, 2015; Craig, 2002; Seth, 2013; Tsakiris and Critchley, 2016). As sympathetic arousal is a reflexive response to a perceived threat, many symptoms associated with anxiety manifest themselves in the body (such as a racing heart or shortness of breath). Perceiving bodily states compatible with sympathetic arousal in the absence of external triggers can itself induce anxiety (Paulus, 2013). Miscommunications between the brain and body are thought to represent a key component of anxiety, where bodily sensations may be under-, over-, or mis-interpreted (Paulus and Stein, 2010), which can initiate and perpetuate symptoms of anxiety

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