Functional MRI localisation of central nervous system regions associated with volitional inspiration in humans

Abstract

1. Functional magnetic resonance imaging (fMRI) provides a means of studying neuronal circuits that control respiratory muscles in humans with better spatial and temporal resolution than in previous positron emission tomography (PET) studies. 2. Whole brain blood oxygenation level-dependent (BOLD) changes determined by fMRI were used to identify areas of neuronal activation associated with volitional inspiration in five healthy men. Four series of scans of each subject were acquired during voluntary breathing (active task) and mechanical ventilation (passive task). Ventilation and end-tidal PCOµ were similar between tasks. Scan data were re-aligned to correct for movement artefacts and cross-referenced breath by breath to respiratory data for selective averaging of inspiratory and expiratory images. 3. Group analysis identified significant increases in the fMRI signal with volitional inspiration in the superior motor cortex, premotor cortex and supplementary motor area at loci similar to those detected in earlier studies that used PET. Additional regions activated by volitional inspiration included inferolateral sensorimotor cortex, prefrontal cortex and striatum (these foci were only revealed by PET under significant inspiratory load). 4. This study represents the first synchronised breath-by-breath analysis of respiratory-related neuronal activity with whole brain imaging in humans. Temporal resolution is sufficient to distinguish individual breaths at a normal breathing frequency.

Central nervous system control of the laryngeal muscles in humans

“…No activation was seen, however, in LX during either inspiration or expiration. When fMRI was used during other respiratory tasks, no clear activation was found in LX (Evans et al, 1999;McKay et al, 2003) in contrast with the previous results seen with PET (Ramsay et al, 1993). This leaves open the question of whether laryngeal muscle control during volitional breathing tasks in humans is controlled via the cortex or by modulation of other respiratory control centers such as in the medulla.…”

“…The areas of activation for swallowing are more extensive (Fig. 5C), than those active for volitional breathing control (Ramsay et al, 1993;Evans et al, 1999;McKay et al, 2003), or for vocalization with prolonged expiration during speech (Murphy et al, 1997;Huang et al, 2002). This may be because several functions are involved, such as the taste sensation from the bolus, jaw and tongue movement associated with moving the bolus to the oropharynx, and eliciting the reflexive pharyngeal swallow.…”

“…In one study the authors contrasted passive ventilation and volitional breathing, as well as inspiration and expiration (Evans et al, 1999). They found activation during inspiration in the same high primary motor area (M1), likely responsible for the diaphragm and chest wall musculature, with left lateralized brain activation for expiration in the inferolateral sensory area and auditory cortex.…”

A bilateral cortico-bulbar network associated with breath holding in humans, determined by functional magnetic resonance imaging

“…In this study, we aimed to highlight only the inhibitory components of breath holding by investigating short breath holds that were voluntarily terminated to remove the variability of breaking point, and were performed at the resting expiratory lung volume when the respiratory musculature is presumed to be relaxed. Previous respiratory related imaging studies have highlighted specific loci within the sensorimotor cortices and the subcortex, specifically the thalamus and basal ganglia ( (Evans et al, 1999;McKay et al, 2000), that underlie volitional respiratory control; however, these studies have investigated active respiratory control rather than inhibition. Direct parallels of breath holding do not exist in other human behaviours but imaging studies of response inhibition during Go/NoGo and Stop-signal tasks (Aron and Poldrack, 2006;Liddle et al, 2001;Watanabe et al, 2002) and those related to inhibiting saccadic eye reflexes (Jueptner et al, 1996), highlight the dorsolateral prefrontal cortex, basal ganglia and thalamus as having a role in inhibiting behaviours.…”

Effects of mandibular advancement on brain activation during inspiratory loading in healthy subjects: a functional magnetic resonance imaging study

“…It is known that the frontal cortex adjacent to the primary motor cortex is related to motor control. Recent studies have provided evidence that this area is also involved in voluntary inspiratory effort (10,11,13). The premotor area indirectly innervates respiratory muscles and, therefore, does not contribute to respiratory drive on a breath-by-breath basis.…”