Differential responses to breath-holding, voluntary deep breathing and hypercapnia in left and right dorsal anterior cingulate.

Patrick Holton,Yongzhi Huang,Jonathan A Hyam,Alexander L Green,Nor Faizal Ahmad Bahuri,Sandra Boccard,Keith L Dorrington,David J Paterson,Shakeeb H Moosavi,Tipu Z Aziz

doi:10.1113/ep088961

Abstract

What is the central question of this study? What is the role of dorsal anterior cingulate cortex (ACC) in respiration control in humans? What is the main finding and its importance? Direct evidence is provided for a role of the ACC in respiratory control in humans. The neurophysiological responses in dorsal ACC to different breathing tasks varied and were different between left and right ACC. The role of subcortical structures and cerebral cortex in the maintenance of respiratory homeostasis in humans remains poorly understood. Emerging evidence suggests an important role of the anterior cingulate cortex (ACC) in respiratory control. In this study, local field potentials (LFPs) from dorsal ACC were recorded in humans through implanted deep brain electrodes during several breathing activities, including voluntary activities of breath-holding and deep breathing, and involuntary activities of inspiration of varying concentrations of carbon dioxide (1%, 3%, 5% and 7%). We found that the breath-holding task induced significant unilateral left-sided ACC changes in LFP power, including an increased activity in lower frequency bands (3-5Hz) and decreased activity in higher frequency bands (12-26Hz). The respiratory task involving reflex increase in ventilation due to hypercapnia (raised inspired CO2 ) was associated with bilateral changes in activity of the ACC (again with increased activity in lower frequency bands and reduced activity in higher frequency bands). The voluntary breathing task with associated hypocapnia (deep breathing) induced bilateral changes in activity within low frequency bands. Furthermore, probabilistic diffusion tractography analysis showed left-sided connection of the ACC with the insula and frontal operculum, and bilateral connections within subsections of the cingulate gyrus and the thalamus. This electrophysiological analysis provides direct evidence for a role of the ACC in respiratory control in humans.

Highlights

Control of respiration at the subcortical level involving midbrain and brainstem has been relatively well-studied albeit primarily in animalPatrick Holton and Yongzhi Huang () contributed to this work.models (Smith et al, 2013)
Higher areas that may be indirectly involved in respiratory control include the insula, frontal cortex, thalamus and basal ganglia, which have been shown to increase in activity during voluntary breathholding
In the left anterior cingulate cortex (ACC) there was a significant decrease in activity between 5 and 8 Hz (−9.1%, P = 0.033) and 12–26 Hz (−15.9%, P = 0.043)

Summary

Introduction

Control of respiration at the subcortical level involving midbrain and brainstem has been relatively well-studied albeit primarily in animalPatrick Holton and Yongzhi Huang () contributed to this work.models (Smith et al, 2013). Little is known about the interaction between these subcortical structures and the cerebral cortex in the maintenance of respiratory homeostasis Such interactions have been suggested in the context of perception of dyspnoea with external. Higher areas that may be indirectly involved in respiratory control include the insula, frontal cortex (including cingulate cortex), thalamus and basal ganglia, which have been shown to increase in activity during voluntary breathholding. It is uncertain whether the response is related to the ‘central command’ facilitating breath-hold as opposed to a response to the physiological changes accompanying the breath-hold (McKay et al, 2008)

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