Sensing, feeling and regulating: investigating the association of focal brain damage with voluntary respiratory and motor control

Henrik Bischoff; Christopher Kovach; Sukbhinder Kumar; Joel Bruss; Daniel Tranel; Sahib S. Khalsa

doi:10.1098/rstb.2023.0251

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Sensing, feeling and regulating: investigating the association of focal brain damage with voluntary respiratory and motor control

Journal article

Peer reviewed

Sensing, feeling and regulating: investigating the association of focal brain damage with voluntary respiratory and motor control

Henrik Bischoff, Christopher Kovach, Sukbhinder Kumar, Joel Bruss, Daniel Tranel and Sahib S. Khalsa

Philosophical Transactions of the Royal Society B, Vol.379(1908), 20230251

08/26/2024

DOI: 10.1098/rstb.2023.0251

PMCID: PMC11528364

PMID: 39005040

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https://pmc.ncbi.nlm.nih.gov/articles/PMC11528364/pdf/rstb.2023.0251.pdfView

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Abstract

Breathing is a complex, vital function that can be modulated to influence physical and mental well-being. However, the role of cortical and subcortical brain regions in voluntary control of human respiration is underexplored. Here we investigated the influence of damage to human frontal, temporal or limbic regions on the sensation and regulation of breathing patterns. Participants performed a respiratory regulation task across regular and irregular frequencies ranging from 6 to 60 breaths per minute (bpm), with a counterbalanced hand motor control task. Interoceptive and affective states induced by each condition were assessed via questionnaire, and autonomic signals were indexed via skin conductance. Participants with focal lesions to the bilateral frontal lobe, right insula/basal ganglia and left medial temporal lobe showed reduced performance relative to individually matched healthy comparisons during the breathing and motor tasks. They also reported significantly higher anxiety during the 60 bpm regular and irregular breathing trials, with anxiety correlating with difficulty in rapid breathing specifically within this group. This study demonstrates that damage to frontal, temporal or limbic regions is associated with abnormal voluntary respiratory and motor regulation and tachypnoea-related anxiety, highlighting the role of the forebrain in affective and motor responses during breathing. This article is part of the theme issue ‘Sensing and feeling: an integrative approach to sensory processing and emotional experience’.

Amygdala

Articles

Brain Damage

Emotion

Interoception

Motor Control

Respiration

Details

Title: Subtitle: Sensing, feeling and regulating: investigating the association of focal brain damage with voluntary respiratory and motor control
Creators: Henrik Bischoff - Carl von Ossietzky Universität Oldenburg
Christopher Kovach - University of Iowa
Sukbhinder Kumar - Department of Neurosurgery, University of Iowa, Iowa City, IA 52242, USA
Joel Bruss - University of Iowa
Daniel Tranel - University of Iowa
Sahib S. Khalsa - Laureate Institute for Brain Research
Resource Type: Journal article
Publication Details: Philosophical Transactions of the Royal Society B, Vol.379(1908), 20230251
DOI: 10.1098/rstb.2023.0251
PMID: 39005040
PMCID: PMC11528364
NLM abbreviation: Philos Trans R Soc Lond B Biol Sci
ISSN: 0962-8436
eISSN: 1471-2970
Publisher: The Royal Society
Grant note: F31AT003061 / National Center for Complementary and Integrative Health (http://dx.doi.org/10.13039/100008460) Kiwanis International Neuroscience Research Foundation
Language: English
Date published: 08/26/2024
Academic Unit: Neurology; Stead Family Department of Pediatrics; Psychological and Brain Sciences; Iowa Neuroscience Institute; Neurosurgery
Record Identifier: 9984658259202771

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