Intrinsic and Extrinsic Tongue Muscles are Driven by Physiologically Distinct Motoneuron Pools
Authors: Frazure Michael , Wollman Lila , Fregosi Ralph 
Published: May 2024

The hypoglossal motor nucleus innervates six of the seven tongue muscles responsible for wide-ranging behaviors including speech, breathing, and swallowing. Despite the task-specific nature of tongue movements, neurophysiologic research has historically treated hypoglossal motoneurons as a homogeneous population. Our previous work showed that hypoglossal motoneurons innervating specific tongue muscles had different firing thresholds and resting membrane potential. Here, we extend this work by comparing potassium conductance in motor neurons innervating the superior longitudinalis (SL; intrinsic) and genioglossus (GG; extrinsic), tongue muscles with opposing actions of tongue retraction and tongue protrusion, respectively. Experiments were performed using N=10 neonatal rat pups aged post-natal day 0-5 ( n=5 each of SL and GG). Motoneurons were back-labeled by injection of dextran rhodamine conjugated to Texas Red into either the SL or GG muscle. > 24-hours after injection, animals were anesthetized on ice and decapitated. The brainstem and spinal cord were removed and 250 μm transverse slices of the medulla containing the hypoglossal nucleus were obtained. SL or GG motor neurons were visualized under a fluorescence microscope and resting membrane potential, rheobase current, frequency-current relation and potassium currents were recorded using whole-cell patch clamp. Statistical analysis revealed that SL motoneurons were ~11 mV more depolarized than GG motoneurons (resting membrane potential of -49 vs -60 mV, p<0.05). Rheobase current (the minimal electrical current required to evoke an action potential) was greater in GG motoneurons than SL motoneurons (approximately 300 vs 150 pA, p<0.05). SL motoneurons had a higher firing rate than GG motoneurons in response to current injection ( p<0.05). Evaluation of neuronal potassium channel conductance showed that the magnitude of transient ( p < 0.01) and sustained (p < 0.01) potassium currents were greater in GG than SL motoneurons, consistent with our finding that resting membrane potential was more negative, and firing rate was slower, in GG than SL motoneurons. Finally, additional SL motoneuron recordings were performed to evaluate for potential sex differences in N=12 (6 male) rat pups aged post-natal day 0-5. Preliminary analysis revealed no significant difference in resting membrane potential between male (-49 mV) and female (-52 mV) SL motoneurons, suggesting that the properties of a specific hypoglossal motoneuron pool are consistent across sexes. Overall, these results demonstrate that GG motoneurons are less excitable than SL motoneurons, which supports the idea that intrinsic and extrinsic tongue muscles are driven by physiologically distinct motoneuron pools. This work has potential to guide development of therapeutics for disordered speech, breathing, and swallowing, all of which depend on proper neuromotor control of the tongue.

This work was funded by NIH 5R01DC020889-02.

This is the full abstract presented at the American Physiology Summit 2024 meeting and is only available in HTML format. There are no additional versions or additional content available for this abstract. Physiology was not involved in the peer review process.