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

Author:

Bischoff Henrik12,Kovach Christopher34,Kumar Sukbhinder3,Bruss Joel5,Tranel Daniel6,Khalsa Sahib S.789ORCID

Affiliation:

1. Department of Psychology, University of Stockholm, 10691 Stockholm, Sweden

2. Department of Psychology, Carl-von-Ossietzky University Oldenburg, 26129 Oldenburg, Germany

3. Department of Neurosurgery, University of Iowa, Iowa City, IA 52242, USA

4. Department of Neurosurgery, University of Nebraska Medical Center, Omaha, NE 68198, USA

5. Departments of Pediatrics, Neurology, and Psychiatry, University of Iowa, Iowa City, IA 52242, USA

6. Departments of Neurology and Psychological and Brain Sciences, University of Iowa, Iowa City, IA 52242, USA

7. Laureate Institute for Brain Research, Tulsa, OK 74136, USA

8. Oxley College of Health Sciences, University of Tulsa, Tulsa, OK 74119, USA

9. Department of Psychiatry and Biobehavioral Sciences, Semel Institute for Neuroscience and Human Behavior, David Geffen School of Medicine, University of California at Los Angeles, Los Angeles, CA 90095, USA

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’.

Funder

Kiwanis International Neuroscience Research Foundation

National Center for Complementary and Integrative Health

Publisher

The Royal Society

Cited by 1 articles. 订阅此论文施引文献 订阅此论文施引文献,注册后可以免费订阅5篇论文的施引文献,订阅后可以查看论文全部施引文献

1. Sensing and feeling: an overview;Philosophical Transactions of the Royal Society B: Biological Sciences;2024-07-15

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