Tonically discharging genioglossus motor units show no evidence of rate coding with hypercapnia

Abstract

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 CO(2) (3% inspired CO(2) 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 CO(2) 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.

Fig. 1.

Original recordings of (from topmost trace down) mask pressure, fractional inspired CO₂, fractional inspired O₂, airflow (inspiration represented by downward deflection), unprocessed genioglossus whole muscle, and single genioglossus (GG) motor-unit electromyographic (EMG) recordings obtained during a steady-state protocol. Segments of the record in normocapnia and steady-state hypercapnia (F_ICO₂ = 3%) are displayed on a faster time base below. Note steady-state hypercapnia was associated with an increase in inspiratory airflow and GG EMG activities. Inset: superimposition of 10 single motor-unit action potentials on a faster time base. MU, motor unit.

Fig. 2.

Original recordings of (topmost trace down) mask pressure, fractional inspired CO₂, fractional inspired O₂, airflow, unprocessed GG whole muscle and single MU recordings obtained in normocapnia and dead space breathing protocol. Segments of the record from both conditions are displayed on a faster time base below. Note that dead space breathing resulted in additional increases in airflow and GG EMG activities over and above that seen under the steady-state protocol. Inset: superimposition of 10 single motor-unit action potentials on a faster time base.

Fig. 3.

GG EMG and V_E relationship. Steady-state and dead space breathing associated increases in ventilation are paralleled by increases in whole muscle GG EMG. - - -, result of a least-squares regression analysis (beta coefficient = 0.80; r² = 0.64) shown with 95% confidence intervals.

Fig. 4.

MU firing frequency as a function of increments in P_ETCO₂. Steady-state (protocols 1 and 2) and dead space breathing associated GG single MU firing rates do not correspond with increments in P_ETCO₂.

Fig. 5.

MU firing frequency as a function of whole muscle GG EMG in steady-state and dead space protocols. Average single MU firing frequency declines despite clear increases in the magnitude of whole muscle GG EMG (%baseline).

Fig. 6.

Effect of steady state and progressive increases in P_ETCO₂ on single motor-unit discharge rate (bottom), tonic (middle), and phasic components of the whole muscle GG EMG. Average single MU firing rates decline whereas drive to the whole muscle as reflected in phasic and tonic components (% baseline) rise. *, significantly different relative to the normocapnic condition (P < 0.05).