Complex and Counterintuitive Relationships between Genioglossus Neural Drive and Dilatory Tongue Movement during Inspiration during Wakefulness
Authors List
L. Jugé1,2, A. Liao (co-first author)1,2, J. Yeung1, F. Knapman1,2, C. Bull1,2, P. Burke1,3, E. Brown1,2, S. Gandevia1,2, D. J. Eckert1,5, J. Butler1,2, L. E. Bilston1,2
1 Neuroscience Research Australia, Sydney, New South Wales, Australia.
2 Faculty of Medicine, University of New South Wales, Sydney, New South Wales, Australia.
3 Macquarie Medical School, Macquarie University, Sydney, New South Wales, Australia.
4 Prince of Wales Hospital, Sydney, New South Wales, Australia.
5 Flinders Health and Medical Research Institute, Flinders University, Adelaide, Australia
Introduction
Inspiratory tongue dilatory movement to maintain airway patency is thought to reflect regional neural drive to the genioglossus, the largest intrinsic dilator muscle of the upper airway. As such, respiratory upper airway dynamic behaviour is often inferred from tongue electromyography (EMG), including in people with obstructive sleep apnoea (OSA) (e.g. Eckert et al. 2009). However, this has never been comprehensively evaluated. Therefore, this study aims to examine the relationship between respiratory-related dilatory tongue movement, as measured by tagged magnetic resonance imaging (MRI), and neural drive, as measured by EMG, and to investigate how this relationship is related to OSA pathophysiology.
Methods
During awake nasal breathing, tongue movement (measured with tagged MRI), and phasic and tonic genioglossus intramuscular EMG normalised to tongue protrusion, were measured in 4 tongue neuromuscular compartments in nine healthy controls (AHI 2.8 ± 1.9 [0.5 – 5.0] events/hr sleep), and 37 people with OSA (28.5 ± 21.4 [5.6 - 94.3] events/hr sleep) prior to commencing treatment. Ethics approval HREC/13/POWH/745.
Results
Tagged MRI and EMG measurements were obtained for 156 tongue neuromuscular compartments from 46 participants. i.e. 85% coverage of 4 compartments for each participant). For 119 neuromuscular compartments (76%), a larger anterior (dilatory) movement was associated with a higher phasic EMG (r = 0.31, P < 0.001, hereafter EMG↗/mvt↗). In contrast, for the remaining 37 (24%) compartments, a larger dilatory movement was associated with a lower phasic EMG (r = -0.50, P = 0.002, hereafter EMG↘/mvt↗). Approximately half of the OSA patients (19/37) had at least one EMG↘/mvt↗ neuromuscular compartments, and this was less common in controls (11%, 1/9). Dilatory tongue movement was minimal in nearly all participants with only EMG↗/mvt↗ compartments (93%, 25/27), while larger dilatory movements (>1mm) were present in a majority of the participants with at least one EMG↘/mvt↗ (58%, 11/19).
Conclusion
This is the first study investigating how the regional neural drive of the tongue muscle contributes to airway dilation during inspiration, and it showed that there are complex and, in some cases, counterintuitive relationships between genioglossus neural drive and dilatory tongue movement, suggesting that upper airway dilatory mechanics cannot be predicted from genioglossus EMG alone. Future studies using these methods may elucidate the mechanisms underpinning these observations and their contribution to OSA pathogenesis.
Research Funding Source This research was funded by the National Health & Medical Research Council (NHMRC) of Australia (#APP1058974). L. Bilston, S. Gandevia, D. Eckert, and J. Butler are supported by NHMRC Fellowships.
L. Jugé1,2, A. Liao (co-first author)1,2, J. Yeung1, F. Knapman1,2, C. Bull1,2, P. Burke1,3, E. Brown1,2, S. Gandevia1,2, D. J. Eckert1,5, J. Butler1,2, L. E. Bilston1,2
1 Neuroscience Research Australia, Sydney, New South Wales, Australia.
2 Faculty of Medicine, University of New South Wales, Sydney, New South Wales, Australia.
3 Macquarie Medical School, Macquarie University, Sydney, New South Wales, Australia.
4 Prince of Wales Hospital, Sydney, New South Wales, Australia.
5 Flinders Health and Medical Research Institute, Flinders University, Adelaide, Australia
Introduction
Inspiratory tongue dilatory movement to maintain airway patency is thought to reflect regional neural drive to the genioglossus, the largest intrinsic dilator muscle of the upper airway. As such, respiratory upper airway dynamic behaviour is often inferred from tongue electromyography (EMG), including in people with obstructive sleep apnoea (OSA) (e.g. Eckert et al. 2009). However, this has never been comprehensively evaluated. Therefore, this study aims to examine the relationship between respiratory-related dilatory tongue movement, as measured by tagged magnetic resonance imaging (MRI), and neural drive, as measured by EMG, and to investigate how this relationship is related to OSA pathophysiology.
Methods
During awake nasal breathing, tongue movement (measured with tagged MRI), and phasic and tonic genioglossus intramuscular EMG normalised to tongue protrusion, were measured in 4 tongue neuromuscular compartments in nine healthy controls (AHI 2.8 ± 1.9 [0.5 – 5.0] events/hr sleep), and 37 people with OSA (28.5 ± 21.4 [5.6 - 94.3] events/hr sleep) prior to commencing treatment. Ethics approval HREC/13/POWH/745.
Results
Tagged MRI and EMG measurements were obtained for 156 tongue neuromuscular compartments from 46 participants. i.e. 85% coverage of 4 compartments for each participant). For 119 neuromuscular compartments (76%), a larger anterior (dilatory) movement was associated with a higher phasic EMG (r = 0.31, P < 0.001, hereafter EMG↗/mvt↗). In contrast, for the remaining 37 (24%) compartments, a larger dilatory movement was associated with a lower phasic EMG (r = -0.50, P = 0.002, hereafter EMG↘/mvt↗). Approximately half of the OSA patients (19/37) had at least one EMG↘/mvt↗ neuromuscular compartments, and this was less common in controls (11%, 1/9). Dilatory tongue movement was minimal in nearly all participants with only EMG↗/mvt↗ compartments (93%, 25/27), while larger dilatory movements (>1mm) were present in a majority of the participants with at least one EMG↘/mvt↗ (58%, 11/19).
Conclusion
This is the first study investigating how the regional neural drive of the tongue muscle contributes to airway dilation during inspiration, and it showed that there are complex and, in some cases, counterintuitive relationships between genioglossus neural drive and dilatory tongue movement, suggesting that upper airway dilatory mechanics cannot be predicted from genioglossus EMG alone. Future studies using these methods may elucidate the mechanisms underpinning these observations and their contribution to OSA pathogenesis.
Research Funding Source This research was funded by the National Health & Medical Research Council (NHMRC) of Australia (#APP1058974). L. Bilston, S. Gandevia, D. Eckert, and J. Butler are supported by NHMRC Fellowships.
