Functional specializations of hypoglossal motoneurons innervating intrinsic and extrinsic tongue muscles

Abstract

The mammalian tongue contains eight muscles that collaborate to ensure that breathing, swallowing, suckling and other important behaviors are robust and reliable. Seven of these muscles are innervated by hypoglossal motoneurons (XIIMNs). Most studies of XIIMNs have considered them to be a homogeneous population, however a given tongue movement requires precisely allocated contributions from all tongue muscles. Thus, XIIMNs may have unique functional properties that reflect the usage pattern of the muscle that they innervate. To better understand the functional specializations of muscle‐specific XIIMNs, intrinsic (superior longitudinalis) and extrinsic (genioglossus) muscles were injected with dextran‐rhodamine to illuminate the XIIMNs innervating those muscles. The labeled XIIMNs were anatomically and electrophysiologically differentiable. Intrinsic XIIMNs were located more medial and dorsal, and extrinsic muscles more lateral and ventral. Whole‐cell patch‐clamp experiments showed that resting membrane potential was on average 10 millivolts more depolarized in intrinsic compared to extrinsic XIIMNs, and that the firing rate response to current injection was higher in intrinsic compared to extrinsic XIIMNs. These observations show muscle‐specific functional specializations in XIIMNs, and this information lays the foundation for more detailed experiments, and the development of “neuron‐specific” therapeutic approaches for tongue‐related respiratory disorders.Support or Funding InformationNIH (R01 HD071302).