Firing Patterns of Human Genioglossus Motor Units During Voluntary Tongue Movement

2007 ◽  
Vol 97 (1) ◽  
pp. 933-936 ◽  
Author(s):  
E. Fiona Bailey ◽  
Amber D. Rice ◽  
Andrew J. Fuglevand

The tongue participates in a range of complex oromotor behaviors, including mastication, swallowing, respiration, and speech. Previous electromyographic studies of the human tongue have focused on respiratory-related tongue muscle activities and their role in maintaining upper airway patency. Remarkably, the activities of human hypoglossal motor units have not been studied during the execution of voluntary maneuvers. We recorded single motor unit activity using tungsten microelectrodes in the genioglossus muscle of 10 healthy human subjects performing both slow tongue protrusions and a static holding maneuver. Displacement of the tongue was detected by an isotonic transducer coupled to the lingual surface through a customized lever arm. For protrusion trials, the firing rate at recruitment was 13.1 ± 3 Hz and increased steeply to an average of 24 ± 6 Hz, often with very modest increases in tongue protrusion. For the static holding task, the average firing rate was 16.1 ± 4 Hz, which is surprisingly high relative to limb motor units. The average coefficient of variation of interspike intervals was ∼20% (range, 10–28%). These are the first recordings of their type obtained in human subjects and provide an initial glimpse into the voluntary control of hypoglossal motoneurons during tongue movements presumably instigated by activity in the motor cortex.

2010 ◽  
Vol 103 (3) ◽  
pp. 1315-1321 ◽  
Author(s):  
Patrick A. Richardson ◽  
E. Fiona Bailey

The genioglossus (GG) is considered the principle protrudor muscle of the human tongue. Unlike most skeletal muscles, GG electromyographic (EMG) activities are robustly preserved in sleep and thus may fulfill a critical role in preserving airway patency. Previous studies in human subjects also confirm that the GG EMG increases in response to chemoreceptor and mechanoreceptor stimulation. This increase occurs secondary to the recruitment of previously inactive motor units (MUs) and/or an increase in firing rate of already active MUs. Which strategy the nervous system uses when the synaptic drive onto GG motoneurons increases is not known. Here we report on GG whole muscle and tonic MU activities under conditions that mimic sleep, i.e., mild-moderate elevations in CO2 (3% inspired CO2 or the addition of a 1.0 l dead space) and elevated airway resistance. Based on previous work in rat, we hypothesized that mild hypercapnia would increase the firing rates of tonic MUs and that these effects would be further potentiated by a modest increase in airway resistance. Fine wire and tungsten microelectrodes were inserted into the GG to record whole muscle and single MU activities in 21 subjects (13 women, 8 men; 20–55 yr). Either 3% inspired CO2 or added dead space resulted in a 200–300% increase in the amplitude of both tonic and phasic components of the whole muscle GG EMG and a doubling of minute ventilation. Despite these changes, recordings obtained from a total of 84 tonically discharging GG single MUs provide no evidence of a change in firing rate under any of the conditions. On this basis we conclude that in healthy adults, the increase in the tonic component of the whole muscle GG EMG secondary to mild hypercapnia is due almost exclusively to the recruitment of previously inactive MUs.


1995 ◽  
Vol 73 (1) ◽  
pp. 113-123 ◽  
Author(s):  
Louise Smith ◽  
Tao Zhong ◽  
Parveen Bawa

When ramp-and-hold currents are injected into a motoneuron of an anesthetized cat, the motoneuron responds with a high initial firing rate (dynamic phase), which then adapts to a lower steady-state firing rate. The firing rates during the dynamic and the steady-state phases are linearly related to the rate of change and the magnitude of the injected current, respectively. In human subjects, where inputs to the motoneurons are not accessible, force parameters are used to describe motoneuron behaviour. Population responses of human motoneurons, measured in terms of gross electromyographic (EMG) activity, increase linearly with the magnitude and the rate of change of force. No study has attempted to examine the question of linearity of single motor units during the dynamic as well as the steady-state phases. The following study recorded single motor unit and EMG activities simultaneously from the flexor carpi radialis muscle in human subjects completing ramp-and-hold force trajectories. Although the results confirmed the linear relationship between EMG activities and the rate and magnitude of the force, a nonlinear activity pattern was observed between the single motor unit firing and the force parameters, suggesting that recruitment must be responsible for the linear behaviour of EMG activity. Comparisons of different background activity levels on the firing patterns of a given motor unit, as well as comparisons of two simultaneously recorded units, further supported nonlinear response patterns of single motor units.Key words: human, motoneurons, motor units, nonlinearity, force trajectory, repetitive firing.


2020 ◽  
Vol 128 (5) ◽  
pp. 1130-1145
Author(s):  
Hsiao-Sen Chang ◽  
Kun-Ze Lee

Tongue muscle activity plays an important role in the regulation of upper airway patency. This study aimed to investigate the respiratory activity of the extrinsic tongue muscle in response to capsaicin-induced bronchopulmonary C-fiber activation following cervical spinal cord contusion. Midcervical spinal-contused animals exhibited a greater baseline preinspiratory burst amplitude of the extrinsic tongue muscle and were resistant to inhaled capsaicin-induced reduction of respiratory tongue muscle activity at the acute injured stage. However, inhalation of capsaicin caused a more severe attenuation of preinspiratory activity of the extrinsic tongue muscle at the chronic injured stage. These results suggest that the upper airway may be predisposed to collapse in response to bronchopulmonary C-fiber activation following chronic cervical spinal cord injury.


1986 ◽  
Vol 61 (4) ◽  
pp. 1523-1533 ◽  
Author(s):  
J. L. Roberts ◽  
W. R. Reed ◽  
O. P. Mathew ◽  
B. T. Thach

The genioglossus (GG) muscle activity of four infants with micrognathia and obstructive sleep apnea was recorded to assess the role of this tongue muscle in upper airway maintenance. Respiratory air flow, esophageal pressure, and intramuscular GG electromyograms (EMG) were recorded during wakefulness and sleep. Both tonic and phasic inspiratory GG-EMG activity was recorded in each of the infants. On occasion, no phasic GG activity could be recorded; these silent periods were unassociated with respiratory embarrassment. GG activity increased during sigh breaths. GG activity also increased when the infants spontaneously changed from oral to nasal breathing and, in two infants, with neck flexion associated with complete upper airway obstruction, suggesting that GG-EMG activity is influenced by sudden changes in upper airway resistance. During sleep, the GG-EMG activity significantly increased with 5% CO2 breathing (P less than or equal to 0.001). With nasal airway occlusion during sleep, the GG-EMG activity increased with the first occluded breath and progressively increased during the subsequent occluded breaths, indicating mechanoreceptor and suggesting chemoreceptor modulation. During nasal occlusion trials, there was a progressive increase in phasic inspiratory activity of the GG-EMG that was greater than that of the diaphragm activity (as reflected by esophageal pressure excursions). When pharyngeal airway closure occurred during a nasal occlusion trial, the negative pressure at which the pharyngeal airway closed (upper airway closing pressure) correlated with the GG-EMG activity at the time of closure, suggesting that the GG muscle contributes to maintaining pharyngeal airway patency in the micrognathic infant.


2011 ◽  
Vol 105 (1) ◽  
pp. 380-387 ◽  
Author(s):  
Christopher M. Laine ◽  
E. Fiona Bailey

The tongue plays a key role in various volitional and automatic functions such as swallowing, maintenance of airway patency, and speech. Precisely how hypoglossal motor neurons, which control the tongue, receive and process their often concurrent input drives is a subject of ongoing research. We investigated common synaptic input to the hypoglossal motor nucleus by measuring the coordination of spike timing, firing rate, and oscillatory activity across motor units recorded from unilateral (i.e., within a belly) or bilateral (i.e., across both bellies) locations within the genioglossus (GG), the primary protruder muscle of the tongue. Simultaneously recorded pairs of motor units were obtained from 14 healthy adult volunteers using tungsten microelectrodes inserted percutaneously into the GG while the subjects were engaged in volitional tongue protrusion or rest breathing. Bilateral motor unit pairs showed concurrent low frequency alterations in firing rate (common drive) with no significant difference between tasks. Unilateral motor unit pairs showed significantly stronger common drive in the protrusion task compared with rest breathing, as well as higher indices of synchronous spiking (short-term synchrony). Common oscillatory input was assessed using coherence analysis and was observed in all conditions for frequencies up to ∼5 Hz. Coherence at frequencies up to ∼10 Hz was strongest in motor unit pairs recorded from the same GG belly in tongue protrusion. Taken together, our results suggest that cortical drive increases motor unit coordination within but not across GG bellies, while input drive during rest breathing is distributed uniformly to both bellies of the muscle.


2015 ◽  
Vol 113 (7) ◽  
pp. 2692-2699 ◽  
Author(s):  
Jennifer R. Vranish ◽  
E. Fiona Bailey

The genioglossus (GG) is an extrinsic muscle of the human tongue that plays a critical role in preserving airway patency. In the last quarter century, >50 studies have reported on respiratory-related GG electromyographic (EMG) activity in human subjects. Remarkably, of the studies performed, none have duplicated subject body position, electrode recording locations, and/or breathing task(s), making interpretation and integration of the results across studies extremely challenging. In addition, more recent research assessing lingual anatomy and muscle contractile properties has identified regional differences in muscle fiber type and myosin heavy chain expression, giving rise to the possibility that the anterior and posterior regions of the muscle fulfill distinct functions. Here, we assessed EMG activity in anterior and posterior regions of the GG, across upright and supine, in rest breathing and in volitionally modulated breathing tasks. We tested the hypotheses that GG EMG is greater in the posterior region and in supine, except when breathing is subject to volitional modulation. Our results show differences in the magnitude of EMG (%regional maximum) between anterior and posterior muscle regions (7.95 ± 0.57 vs. 11.10 ± 0.99, respectively; P < 0.001), and between upright and supine (8.63 ± 0.73 vs. 10.42 ± 0.90, respectively; P = 0.008). Although the nature of a task affects the magnitude of EMG ( P < 0.001), the effect is similar for anterior and posterior muscle regions and across upright and supine ( P > 0.2).


2015 ◽  
Vol 114 (5) ◽  
pp. 2883-2892 ◽  
Author(s):  
Michael J. Woods ◽  
Christian L. Nicholas ◽  
John G. Semmler ◽  
Julia K. M. Chan ◽  
Amy S. Jordan ◽  
...  

Common drive is thought to constitute a central mechanism by which the efficiency of a motor neuron pool is increased. This study tested the hypothesis that common drive to the upper airway muscle genioglossus (GG) would increase with increased respiratory drive in response to an inspiratory load. Respiration, GG electromyographic (EMG) activity, single-motor unit activity, and coherence in the 0–5 Hz range between pairs of GG motor units were assessed for the 30 s before an inspiratory load, the first and second 30 s of the load, and the 30 s after the load. Twelve of twenty young, healthy male subjects provided usable data, yielding 77 pairs of motor units: 2 Inspiratory Phasic, 39 Inspiratory Tonic, 15 Expiratory Tonic, and 21 Tonic. Respiratory and GG inspiratory activity significantly increased during the loads and returned to preload levels during the postload periods (all showed significant quadratic functions over load trials, P < 0.05). As hypothesized, common drive increased during the load in inspiratory modulated motor units to a greater extent than in expiratory/tonic motor units (significant load × discharge pattern interaction, P < 0.05). Furthermore, this effect persisted during the postload period. In conclusion, common drive to inspiratory modulated motor units was elevated in response to increased respiratory drive. The postload elevation in common drive was suggestive of a poststimulus activation effect.


2002 ◽  
Vol 93 (6) ◽  
pp. 2129-2136 ◽  
Author(s):  
A. S. Jordan ◽  
P. G. Catcheside ◽  
F. J. O'Donoghue ◽  
R. D. McEvoy

Obstructive sleep apnea (OSA) is more common in men than in women for reasons that are unclear. The stability of the respiratory controller has been proposed to be important in OSA pathogenesis and may be involved in the gender difference in prevalence. Repetitive hypoxia elicits a progressive rise in ventilation in animals [long-term facilitation (LTF)]. There is uncertainty whether LTF occurs in humans, but if present it may stabilize respiration and possibly also the upper airway. This study was conducted to determine 1) whether LTF exists during wakefulness in healthy human subjects and, if so, whether it is more pronounced in women than men and 2) whether inspiratory pump and upper airway dilator muscle activities are affected differently by repetitive hypoxia. Twelve healthy young men and ten women in the luteal menstrual phase were fitted with a nasal mask and intramuscular genioglossal EMG (EMGgg) recording electrodes. After 5 min of rest, subjects were exposed to ten 2-min isocapnic hypoxic periods (∼9% O2 in N2, arterial O2 saturation ∼80%) separated by 2 min of room air. Inspired minute ventilation (V˙i) and peak inspiratory EMGgg activity were averaged over 30-s intervals, and respiratory data were compared between genders during and after repetitive hypoxia by using ANOVA for repeated measures. V˙i during recovery from repetitive hypoxia was not different from the resting level and not different between genders. There was no facilitation of EMGgg activity during or after repetitive hypoxia. EMGgg activity was reduced below baseline during recovery from repetitive hypoxia in women. In conclusion, we have found no evidence of LTF of ventilation or upper airway dilator muscle activity in healthy subjects during wakefulness.


2006 ◽  
Vol 101 (5) ◽  
pp. 1377-1385 ◽  
Author(s):  
E. Fiona Bailey ◽  
Yu-Hsien Huang ◽  
Ralph F. Fregosi

We recently showed respiratory-related coactivation of both extrinsic and intrinsic tongue muscles in the rat. Here, we test the hypothesis that intrinsic tongue muscles contribute importantly to changes in velopharyngeal airway volume. Spontaneously breathing anesthetized rats were placed in a MRI scanner. A catheter was placed in the hypopharynx and connected to a pressure source. Axial and sagittal images of the velopharyngeal airway were obtained, and the volume of each image was computed at airway pressures ranging from +5.0 to −5.0 cmH2O. We obtained images in the hypoglossal intact animal (i.e., coactivation of intrinsic and extrinsic tongue muscles) and after selective denervation of the intrinsic tongue muscles, with and without electrical stimulation. Denervation of the intrinsic tongue muscles reduced velopharyngeal airway volume at atmospheric and positive airway pressures. Electrical stimulation of the intact hypoglossal nerve increased velopharyngeal airway volume; however, when stimulation was repeated after selective denervation of the intrinsic tongue muscles, the increase in velopharyngeal airway volume was significantly attenuated. These findings support our working hypothesis that intrinsic tongue muscles play a critical role in modulating upper airway patency.


1988 ◽  
Vol 65 (1) ◽  
pp. 210-217 ◽  
Author(s):  
E. van Lunteren ◽  
N. S. Cherniack ◽  
T. E. Dick

To examine the effects of upper airway negative pressure (UAW NP) afferents on respiratory muscle activity during expiration (TE), diaphragm electromyograms (EMG) and triangularis sterni EMG and single motor unit activity were recorded from supine anesthetized tracheotomized cats while they breathed 100% O2. The period of TE during which the diaphragm was electrically active (TE-1) and the period of TE during which the diaphragm was quiescent (TE-2) were both increased with continuous UAW NP (P less than 0.001 and P less than 0.05, respectively), as was TE-1 as a percent of TE (P less than 0.001). Continuous UAW NP reduced peak triangularis sterni EMG (P less than 0.001) and delayed its expiratory onset (P less than 0.005) but did not alter its duration of firing. Changes in triangularis sterni EMG were due to a combination of complete cessation of motor unit activity (2 of 17 motor units), a reduction in mean motor unit firing frequency (P less than 0.02), and a delay in the expiratory onset of motor unit activity (P less than 0.001). Qualitatively similar results were obtained when UAW NP was applied during inspiration only. We conclude that 1) UAW NP has reciprocal stimulatory and inhibitory influences on diaphragm and triangularis sterni muscle electrical activity, respectively, during expiration, and 2) the reductions in triangularis sterni EMG are due to both motor unit derecruitment and a slowing of motor unit firing frequency.


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