Journal of neurophysiology | 2019
Diverse physiologic properties of hypoglossal motoneurons innervating intrinsic and extrinsic tongue muscles.
Abstract
The mammalian tongue contains eight muscles that collaborate to ensure that suckling, swallowing and other critical functions are robust and reliable. Seven of the eight tongue muscles are innervated by hypoglossal motoneurons (XIIMNs). A somatotopic organization of the XII motor nucleus, defined in part by the mechanical action of a neuron s target muscle has been described, but whether or not XIIMNs within a compartment are functionally specialized is unsettled. We hypothesize that developing XIIMNs are assigned unique functional properties that reflect the challenges that their target muscle faces upon the transition from in uteroto terrestrial life. To address this, we studied XIIMNs that innervate intrinsic and extrinsic tongue muscles, as intrinsic muscles play a more prominent role in suckling than the extrinsic muscles. We injected dextran-rhodamine into the intrinsic longitudinal muscles (IL) and the extrinsic genioglossus, and physiologically characterized the labeled XIIMNs. Consistent with earlier work, IL XIIMNs (n = 150) were located more dorsally within the nucleus, and GG XIIMNs (n = 55) more ventral. Whole-cell recordings showed that resting membrane potential was on average 9 mV more depolarized in IL than in GG XIIMNs (P=0.0019), and the firing threshold in response to current injection was lower in IL (-31 ±23 pA) than in GG XIIMNs (225 ±39 pA, P<0.0001). The appearance of net outward currents in GG motoneurons occurred at more hyperpolarized membrane potentials than IL motoneurons, consistent with lower excitability in GG motoneurons. These observations document muscle-specific functional specializations among hypoglossal motoneurons.