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REPORT

Firing Patterns of Human Genioglossus Motor Units During Voluntary Tongue Movement

Department of Physiology, University of Arizona, Tucson, Arizona

Submitted 17 July 2006; accepted in final form 2 October 2006

	ABSTRACT

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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.

	INTRODUCTION

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The tongue is a remarkable structure that participates in a range of complex oromotor behaviors including mastication, swallowing, breathing, and speaking. The muscles of the tongue differ from those of limbs in several important ways. They do not act on a lever or tendon and exhibit few spindles organs (Cooper 1953; Kubota et al. 1975), and there is scant evidence for either Renshaw-like recurrent inhibition or monosynaptic excitatory stretch reflexes (Cooper 1953; Porter 1966). Because the tongue lacks a bony skeleton, tongue muscles make nontendinous insertions into lingual soft tissue and overlap and interdigitate extensively and at various orientations throughout the tongue (Abd-El-Malek 1938). This interdigitation severely limits the EMG assessment of motor unit activities within the body of the tongue and continues to pose a considerable technical challenge to in vivo force measures traditionally used in limb or digit muscles.

In this study, we recorded single motor unit activities from a tongue protrudor muscle, the genioglossus (GG), and asked the following questions: 1) are the firing rates of GG motor units (MUs) comparable with those observed in other orofacial or limb muscles, 2) is interspike interval variability of GG MUs comparable with that observed in other orofacial or limb muscles, and 3) are individual GG MUs recruited at the same position in space on successive volitional protrusions. Importantly, we show that both the recruitment and rate modulation of GG MUs seem precisely tuned to tongue position.

	METHODS

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We performed 14 experiments in 10 healthy human volunteers (5 women and 5 men; age, 22–48 yr). All experimental procedures were approved by the Human Subjects Committee at The University of Arizona. Subjects gave their informed consent before participation in the study.

EMG recording

Single motor unit action potentials were recorded with submental tungsten microelectrodes inserted transcutaneously into the GG (1- to 5-µm tip diameter, 250-µm shaft diameter, 10 M at 1 KHz; Frederick Haer, Bowdoinham, ME). A surface electrode (4-mm-diameter Ag-AgCl) attached to the skin overlying the mastoid process served as an indifferent electrode, and both the intramuscular and surface electrodes were referenced to a ground strap placed around the upper arm. Motor unit potentials were amplified (1,000x), band-pass filtered (0.3–3 KHz; Grass Instruments, West Warwick, RI), and displayed on a storage oscilloscope and recorded on the Spike2 data acquisition and analysis program (CED, Cambridge, UK).

Intramuscular electrode placements were made 1.5 cm on either side of the midline at a distance 2–4 cm from the inferior margin of the mandible. To define the minimum depth for electrode insertion, the musculature of the floor of mouth initially was visualized by ultrasonography (Pro Sound 3500, Aloka, Tokyo, Japan), and the distance from the skin surface to the inferior border of the GG muscle was determined using an electronic caliper (Eastwood et al. 2003). The average depth to the inferior border of the genioglossus muscle was 13–15 mm, and MU activities were typically recorded at depths 18–24 mm from the skin surface.

Protocol

Subjects were seated upright in a dental chair with their head supported. Respiratory movements of the chest were monitored by a respiratory effort transducer (Biopac Systems, Goleta, CA) positioned around the rib cage at the level of the axilla.

Protrusion-retraction–related displacement of the tongue was detected by a battery powered isotonic transducer (Harvard Apparatus, Kent, UK). The transducer was connected to the tongue by a customized lever arm that engaged a thermoplastic housing (Fig. 1). The housing was affixed to the dorsum of the tongue in a two-step process. First, a foundation layer (polycarboxylate cement, ESPE America, Norristown, PA) was applied to the the distal portion of the tongue, after the tongue had been dried with gauze. After the foundation material had dried, cyano-acrylate glue (Ellman International, Oceanside, NY) was used to secure the housing to the foundation layer. At the termination of the experiment, the foundation layer could be readily removed from the tongue without causing discomfort to the subject. The coupling posed minimal impediment to movement, and subjects were able to swallow and speak during the experiment. The displacement signal was amplified (Grass) and displayed using the Spike2 data acquisition and analysis program (CED).

View larger version (21K): [in this window] [in a new window]   FIG. 1. Schematic representation of experimental setup. Protrusion-retraction–related displacement of the tongue was detected by a battery-powered isotonic transducer. The transducer was connected to the tongue via a lever arm connected to a plastic coupling that engaged the thermoplastic housing affixed to the dorsum of the tongue.

Each trial comprised a static holding task and three slow protrusions. Subjects were provided with both auditory and visual feedback (i.e., through an ongoing display of the spike record on a slowed time scale) of the discharge in both the static hold and protrusion tasks. For the holding task, subjects were instructed to maintain the tongue in the least-protruded position that was also associated with stable MU discharge (i.e., firing without interruption) for 20 s.

For slow protrusions, subjects first retracted the tongue (i.e., relative to the position during the holding task) and slowly advanced the tongue to recruit the target motor unit. Slow protrusion continued until the activity of additional motor units were detected on the electrode, at which point the subjects were instructed to slowly retract the tongue until discharge in the target motor unit ceased. Each protrusion/retrusion lasted 30 s and was repeated three times in quick succession. Trials in which swallows occurred between successive protrusions were excluded from the analysis.

Data analysis

Data were analyzed using Spike2 and custom-designed software. Initially, motor units were discriminated using a template-matching algorithm based on waveform shape and amplitude. For an analysis of firing rate during protrusions, only those units whose activity could be followed in three protrusions were included. Recruitment firing rate was calculated from the first 10 interspike intervals during the tongue protrusion task, and peak firing rate was determined as the highest rate for 10 consecutive interspike intervals during the task. Mean values for recruitment and peak firing rates were calculated from the three trials that were recorded for each motor unit. The average GG firing rate was calculated as the reciprocal of the average interspike interval (ISI) over the entire period of tonic discharge associated with the holding task. Variability in ISIs during the holding task was estimated as the coefficient of variation (CV) of the ISIs, expressed as a percentage [CV = (SD ISI/mean ISI) x 100].

	RESULTS

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We recorded a total of 50 single GG motor units. Figure 2 shows representative data for a single GG motor unit during four trials with increasing tongue displacement across trials. The unit was recruited at approximately the same tongue position on successive protrusions (0.14, 0.18, 0.13, and 0.51 mm). Firing rate initially increased steeply with tongue displacement beyond the recruitment position, from an initial mean rate in this unit of 12 ± 2 (SD) Hz up to a mean peak rate of 33 ± 2 Hz. However, for tongue displacements 4–6 mm beyond the recruitment position, there was little additional modulation in firing rate. This leveling-off in firing rate is highlighted when contrasting the overall extent of tongue displacement across the four trials—from 6.4 mm in the first trial to 13.6 mm in the fourth trial—yet the peak rates are nearly the same across trials (Fig. 2, horizontal dashed line). Furthermore, for trials 2–4, other units were recruited at times when the discriminated unit had ceased to increase its firing rate, implying that the overall neural drive to the GG motoneuron pool continued to increase throughout tongue protrusion.

View larger version (22K): [in this window] [in a new window]   FIG. 2. Example recording of motor unit activity during 4 trials of slow protrusion-retraction of the tongue. Top: instantaneous firing rate (dots) and firing rate averaged over 1-s bins (thin line). Dashed horizontal line indicates approximate peak firing rate across 4 trials (32 Hz). Middle: discriminated motor unit potentials; insets show overlay of 100 consecutive potentials of identified unit from each trial. Gray traces in trials 2, 3, and 4 indicate potentials of other motor units recruited during those trials. Bottom: protrusion position of tongue. Leftmost dashed line in each trial indicates position at which unit was recruited; rightmost dashed line indicates approximate position at which firing rate saturated.

View larger version (33K): [in this window] [in a new window]   FIG. 3. Firing rate as a function of tongue position for 50 genioglossus (GG) motor units. Each trace represents a 3rd-order polynomial fit to the firing rate–displacement data from a single trial of an individual unit. Zero displacement (vertical line) represents neutral position of tongue; positive values indicate protruded and negative values retracted positions relative to neutral position. Maximal displacement depicted for each trace represents position at which discrimination of the unit became unreliable because of activation of other units. Average firing rate at initiation of tongue protrusion trials is represented by dashed horizontal line.

On occasion, we encountered motor units that exhibited transient responses with remarkably high instantaneous firing rates up to 80 Hz. Whereas these units appeared to discharge sporadically or not at all during the slow tongue protrusions or the static holding task, they appeared to be robustly activated during rapid movements.

	DISCUSSION

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This study provides the first data on the firing patterns of human lingual motor units during a voluntary task. We characterized the relation between firing rate and displacement during tongue protrusions. For most GG motor units, firing rate increased steeply with tongue protrusion over a relatively limited displacement range, beyond which firing rate appeared to saturate. Such saturation in firing rate has been described previously for limb motor units (Johns and Fuglevand 2004; Monster and Chan 1977). While several possible causes of firing rate saturation have been discussed in the literature (Destexhe and Pare 1999; Heckman and Binder 1993; Taylor and Enoka 2004), the actual mechanisms underlying firing rate saturation have not yet been clearly delineated. Nevertheless, we showed that firing rate saturation is a prominent feature of hypoglossal motoneurons.

The average rate at which GG MUs were found to discharge tonically during the holding task was substantially higher than that reported for most limb motor units, which typically discharge at 6–10 Hz under similar conditions (Andreassen and Rosenfalck 1980; Hockensmith et al. 2005; Monster and Chan 1977). Because minimum firing rate is known to be inversely related to the duration of the afterhyperpolarization (AHP) after the action potential (Kernell 1965), perhaps human hypoglossal motoneurons possess briefer AHPs than do spinal motoneurons, as seems to be the case in the cat (Fung et al. 2000; Powers and Binder 2000).

Remarkably, GG MU recruitment seemed to be precisely related to a specific tongue position. For example, activity of the unit depicted in Fig. 2 reliably started within 0.5 mm of the same tongue position across four independent protrusions. Overall, recruitment of GG MUs was seen to occur throughout a wide range of tongue positions, with some units recruited at tongue positions less than the relaxed or "neutral" position (Fig. 3). Thus there is likely some degree of tonic motor unit activity in the GG even during presumed resting conditions.

Last, we encountered some motor units whose activity patterns were difficult to characterize within the parameters of our slow protrusion task. These units discharged transiently and at high firing rates during rapid tongue movements. Based on these preliminary observations, it seems possible that the GG motoneuron pool may comprise different populations of units, with some underlying more rapid tongue movements. Such task-dependent heterogeneity has been described previously in human masseter motor units wherein firing rate and firing rate variability varies with jaw position and direction of effort (Eriksson et al. 1984; McMillan and Hannam 1992). However, although these findings in GG MUs are suggestive of heterogeneity within the hypoglossal motoneuron pool, additional studies that characterize motor unit discharge during rapid tongue maneuvers are necessary before this can be confirmed.

Other studies of orofacial motor units

Although there are no data on hypoglossal MUs during the execution of volitional tasks, previous studies have characterized respiratory-related activities of GG MUs in human subjects (Bailey et al. 2005; Saboisky et al. 2006; Tsuiki et al. 2000). Available data show two respiratory-related MU populations, one that is active during inspiration and a second that is tonically active throughout the respiratory cycle (Saboisky et al. 2006; Tsuiki et al. 2000). The average discharge frequencies for these respiratory-related MUs range between 10 and 16 Hz. The peak frequencies attained by the inspiratory MUs range between 15 and 18 Hz (Bailey et al. 2005; Saboisky et al. 2006), whereas the range for the tonic units is somewhat higher, i.e., 22–24 Hz (Saboisky et al. 2006). Importantly, none of the GG MUs studied under the current protocol exhibited either phasic or tonic respiratory modulation. However, because all recordings were obtained with subjects seated in the upright position, the possibility that some or all of the MUs recorded during voluntary tongue protrusion may also exhibit respiratory type modulation in supine or head down position cannot be excluded.

Some data on the voluntary discharge behavior of motor units associated with other orofacial muscles are available. For example, firing rates in human lateral pterygoid and temporalis MUs, during jaw movements, seem comparable with these findings and range from 12 to 24 Hz (CV not reported) (Phanachet et al. 2002). Likewise, Luschei et al. (1999) recorded the activity of motor units in the laryngeal adductor muscle (the thyroarytenoid) during phonation and reported an average firing rate of 24 Hz (range, 5–30 Hz).

The discharge variability (CV) reported here in GG motor units (20.6%) during a volitional task is substantially higher than previous reports in orofacial muscles. For example, during phonatory tasks, >43% of the laryngeal motor units exhibit CVs of <10% (Luschei et al. 1999). Interestingly, the discharge variability in both inspiratory and tonic respiratory-related GG MUs is also very low (6%) (Bailey et al. 2005). The cause of this apparent task-related difference in discharge variability is not known and warrants further study.

	GRANTS

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This work was supported by National Institutes of Health Grants DC-07597 to E. F. Bailey and NS-39489 to A. J. Fuglevand.

	ACKNOWLEDGMENTS

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We thank Dr. Ralph Fregosi for helpful comments on the manuscript and Dr. Pascal Lieshout for technical advice.

	FOOTNOTES

 
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Address for reprint requests and other correspondence: E. F. Bailey, Dept. of Physiology, College of Medicine, Univ. of Arizona, Tucson, AZ 85721-0093 (E-mail: ebailey{at}u.arizona.edu)

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This Article Abstract Full Text (PDF) All Versions of this Article: 97/1/933    most recent 00737.2006v1 Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via ISI Web of Science (2) Citing Articles via Google Scholar Google Scholar Articles by Bailey, E. F. Articles by Fuglevand, A. J. Search for Related Content PubMed PubMed Citation Articles by Bailey, E. F. Articles by Fuglevand, A. J.