Motor unit recruitment in human genioglossus muscle in response to hypercapnia

Abstract

Study objectives: single motor unit recordings of the genioglossus (GG) muscle indicate that GG motor units have a variety of discharge patterns, including units that have higher discharge rates during inspiration (inspiratory phasic and inspiratory tonic), or expiration (expiratory phasic and expiratory tonic), or do not modify their rate with respiration (tonic). Previous studies have shown that an increase in GG muscle activity is a consequence of increased activity in inspiratory units. However, there are differences between studies as to whether this increase is primarily due to recruitment of new motor units (motor unit recruitment) or to increased discharge rate of already active units (rate coding). Sleep-wake state studies in humans have suggested the former, while hypercapnia experiments in rats have suggested the latter. In this study, we investigated the effect of hypercapnia on GG motor unit activity in humans during wakefulness.

Setting: sleep research laboratory.

Participants: sixteen healthy men.

Measurements and results: each participant was administered at least 6 trials with P(et)CO(2) being elevated 8.4 (SD = 1.96) mm Hg over 2 min following a 30-s baseline. Subjects were instrumented for GG EMG and respiratory measurements with 4 fine wire electrodes inserted subcutaneously into the muscle. One hundred forty-one motor units were identified during the baseline: 47% were inspiratory modulated, 29% expiratory modulated, and 24% showed no respiratory related modulation. Sixty-two new units were recruited during hypercapnia. The distribution of recruited units was significantly different from the baseline distribution, with 84% being inspiratory modulated (P < 0.001). Neither units active during baseline, nor new units recruited during hypercapnia, increased their discharge rate as P(et)CO(2) increased (P > 0.05 for all comparisons).

Conclusions: increased GG muscle activity in humans occurs because of recruitment of previously inactive inspiratory modulated units.

Keywords: Single motor unit; motor control; obstructive sleep apnea; upper airway muscles.

Figure 1

Total spikes/second, irrespective of motor unit affiliation, during inspiration and expiration as a function of consecutive 30-s blocks over a trial. Error bars indicate standard errors.

Figure 2

Percentage distribution of motor units with different discharge patterns during baseline that were recruited during hypercapnia and were present at the end of the trial during recovery. IP = inspiratory phasic; IT = inspiratory tonic; EP = expiratory phasic; ET = expiratory tonic; TT = tonic.

Figure 3

The top 2 traces show instantaneous frequency plots for a recruited inspiratory phasic unit (top trace) and a tonic unit (second trace) as a function of time in the trial. This segment is taken from a period during the final 30 sec of a CO₂ trial. Also shown is the raw EMG, rate of flow, and CO₂ recordings.

Figure 4

The top tracing shows an instantaneous frequency plot for a tonic unit that acquired an expiratory phasic component late in the trial. The left panel is taken from early in the trial and the right panel from late in the trial. The average maximum cross correlation values were 0.38 and 0.70 respectively; 60 sec intervened between the 2 panels. Also shown are the raw EMG, rate of flow, and CO₂ recordings.

Figure 5

Mean frequency (Hz) for inspiratory phasic (IT), recruited IP, inspiratory tonic (IT), expiratory tonic (ET), and tonic (TT) motor units as a function of consecutive 30-s blocks. CO₂ was added to the inspiratory line during blocks 2 through 5. Error bars indicate standard errors.

Figure 6

The top 2 tracings show 2 inspiratory phasic motor units recorded on a single electrode, neither of which shows any evidence of rate coding in response to hypercapnia. The left vertical line indicates the onset of CO₂ administration and the right line the offset. Also shown are the raw GG_EMG, flow, and CO₂ recordings.