Synchronization of presynaptic input to motor units of tongue, inspiratory intercostal, and diaphragm muscles

Abstract

The respiratory central pattern generator distributes rhythmic excitatory input to phrenic, intercostal, and hypoglossal premotor neurons. The degree to which this input shapes motor neuron activity can vary across respiratory muscles and motor neuron pools. We evaluated the extent to which respiratory drive synchronizes the activation of motor unit pairs in tongue (genioglossus, hyoglossus) and chest-wall (diaphragm, external intercostals) muscles using coherence analysis. This is a frequency domain technique, which characterizes the frequency and relative strength of neural inputs that are common to each of the recorded motor units. We also examined coherence across the two tongue muscles, as our previous work shows that, despite being antagonists, they are strongly coactivated during the inspiratory phase, suggesting that excitatory input from the premotor neurons is distributed broadly throughout the hypoglossal motoneuron pool. All motor unit pairs showed highly correlated activity in the low-frequency range (1-8 Hz), reflecting the fundamental respiratory frequency and its harmonics. Coherence of motor unit pairs recorded either within or across the tongue muscles was similar, consistent with broadly distributed premotor input to the hypoglossal motoneuron pool. Interestingly, motor units from diaphragm and external intercostal muscles showed significantly higher coherence across the 10-20-Hz bandwidth than tongue-muscle units. We propose that the lower coherence in tongue-muscle motor units over this range reflects a larger constellation of presynaptic inputs, which collectively lead to a reduction in the coherence between hypoglossal motoneurons in this frequency band. This, in turn, may reflect the relative simplicity of the respiratory drive to the diaphragm and intercostal muscles, compared with the greater diversity of functions fulfilled by muscles of the tongue.

Fig. 1.

Representative dual motor unit recordings from within 4 muscles: the genioglossus (GG-GG), hyoglossus (HG-HG), inspiratory intercostal (IC-IC), and diaphragm (Dia-Dia). The phasic discharge is confined largely to the inspiratory phase of the respiratory cycle.

Fig. 2.

The coefficient of variation (CV) of the interspike interval (ISI) for all recorded motor units from the GG, HG, IC, and diaphragm muscles. The horizontal bars indicate the mean value. The CV of ISI in diaphragm motor units was significantly lower that in all other muscles. ***P < 0.001 vs. diaphragm.

Fig. 3.

Proportion of coherent motor unit pairs and average coherence magnitude for all within-muscle comparisons. A: proportion of within-muscle motor unit pairs showing significant coherence at each frequency, for all 4 muscles. The proportion of coherent motor unit pairs in each of the 4 muscles and at each frequency was compared statistically (see methods), and the results of this analysis are depicted as P values in the lower section of A. B: average coherence magnitude between motor unit pairs within each of the muscles, with the P values derived from one-way ANOVA located beneath the coherence data. There were significant differences in coherence magnitude across the 9–20-Hz bandwidth.

Fig. 4.

Power-spectral density of representative single motor unit discharges from each of the muscles. Note the large power values at the fundamental respiratory frequency and the first 2–3 harmonics of this fundamental frequency. The power in the 30–60-Hz range reflects the approximate mean firing rate of the motor units.

Fig. 5.

Proportion and average coherence magnitude for motor units recorded simultaneously from the GG and HG. A: proportion of GG-HG motor unit pairs showing significant coherence at each frequency. B: average coherence-magnitude coherence between GG-HG motor unit pairs. Both the proportion of coherent GG-HG pairs and the coherence magnitude for these across-muscle comparisons are very similar to the within-muscle comparisons (GG-GG and HG-HG) shown in Fig. 3A.

Fig. 6.

The proportion (A) and magnitude (B) of coherence in motor unit pairs from tongue and chest-wall muscles. For this analysis we combined all motor unit pairs from both tongue muscles and all pairs from the two chest-wall muscles to compare the proportion and magnitude of coherence in cranial and spinal motoneurons. Note that coherent oscillations in chest-wall muscle motor units are significantly higher than tongue-muscle units over the 8–20-Hz bandwidth.

Fig. 7.

Coherence magnitude (transformed into Fisher's Z-scores) as a function of discharge rate for all motor unit pairs studied. The mean discharge rate was computed as the geometric mean of the average discharge rate of each motor unit in a pair. The regression line and r² values are shown.

Fig. 8.

Relationship between the average discharge rate that we recorded in rodent hyoglossus, genioglossus external intercostal, and diaphragm muscles and the percentage of type I muscle fibers in each muscle, as reported by others (Cunningham et al. 1991; LaFramboise et al. 1992; Prakash et al. 2000; Smith et al. 2005; Sutlive et al. 2000).