Diverse physiological properties of hypoglossal motoneurons innervating intrinsic and extrinsic tongue muscles
Autor: | Marina Cholanian, Ralph F. Fregosi, Emily Gayle Flanigan, Richard B. Levine, Jesse Wealing |
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Rok vydání: | 2019 |
Předmět: |
Male
Hypoglossal Nerve Patch-Clamp Techniques Physiology Musculoskeletal Physiological Phenomena Tongue muscles Biology Membrane Potentials Rats Sprague-Dawley 03 medical and health sciences 0302 clinical medicine Tongue medicine Animals Muscle Skeletal 030304 developmental biology Motor Neurons 0303 health sciences Medulla Oblongata Rapid Report General Neuroscience Anatomy Electrophysiological Phenomena Rats medicine.anatomical_structure Animals Newborn Female Nucleus 030217 neurology & neurosurgery |
Zdroj: | J Neurophysiol |
ISSN: | 1522-1598 |
Popis: | 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 utero to terrestrial life. To address this, we studied XIIMNs that innervate intrinsic and extrinsic tongue muscles, because 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 ventrally. 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). We also found that the appearance of net outward currents in GG XIIMNs occurred at more hyperpolarized membrane potentials than IL XIIMNs, consistent with lower excitability in GG XIIMNs. These observations document muscle-specific functional specializations among XIIMNs. NEW & NOTEWORTHY The hypoglossal motor nucleus contains motoneurons responsible for innervating one of seven different muscles with notably different biomechanics and patterns of use. Whether or not motoneurons innervating the different muscles also have unique functional properties (e.g., spiking behavior, synaptic physiology) is poorly understood. In this work we show that neonatal hypoglossal motoneurons innervating muscles that shape the tongue (intrinsic longitudinal muscles) have different electrical properties than those innervating the genioglossus, which controls tongue position. |
Databáze: | OpenAIRE |
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