Swallowing-related Perihypoglossal Neurons Projecting to Hypoglossal Motoneurons in the Cat

Abstract

Although previous studies have examined the functional role of the neurons in the area ventrolateral to the hypoglossal nucleus (perihypoglossal neurons) in the trigemino-hypoglossal reflex, no convincing evidence for the direct connection from the perihypoglossal neurons to the hypoglossal motoneurons has yet been provided. In addition, the role of the perihypoglossal neurons in swallowing has not been studied. The purpose of this study was to investigate (1) the input-output relationship of the perihypoglossal neurons and (2) whether the afferent feedback was essential for their swallowing-related activity in chloralose-anesthetized cats. Before and after the cats were paralyzed, single-unit activities were recorded extracellularly from 30 perihypoglossal neurons during swallowing elicited by electrical stimulation of the superior laryngeal nerve. These perihypoglossal neurons responded with spike potentials after short latencies to stimulation of the inferior alveolar and hypoglossal nerves. The neurons also responded with spike potentials to single shocks applied to the superior laryngeal nerve, but were activated transiently at the initial phase of repetitive stimulation of the nerve and kept silent until the occurrence of swallowing before and after the animal was paralyzed. They showed burst activities in coincidence with swallowing. Averaging of intracellular potentials of a hypoglossal motoneuron by simultaneously recorded extracellular spikes of a perihypoglossal neuron revealed monosynaptic inhibitory post-synaptic potentials. We conclude that, in the region ventrolateral to the hypoglossal nucleus, there are neurons which relay trigeminal, hypoglossal, and vagal afferents. Furthermore, some of these perihypoglossal neurons are inhibitory hypoglossal premotor neurons that are involved in the central programming of swallowing.

Keywords

perihypoglossal neuron hypoglossal motoneuron superior laryngeal nerve swallowing cat.

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References

Amri M. , Car A. , Roman C. (1990). Axonal branching of medullary swallowing neurons projecting on the trigeminal and hypoglossal motor nuclei: demonstration by electrophysiological and fluorescent double labeling techniques. Exp Brain Res 81:384-390.

Borke RC , Nau ME (1985). The ultrastructual identification of reticulo-hypoglossal axon terminals anterogradely labeled with horseradish peroxidase. Brain Res 337:127-132.

Borke RC , Nau ME , Ringler RL Jr (1983). Brain stem afferents of hypoglossal neurons in the rat. Brain Res 269:47-55.

Cajal SR (1909). Histologie du systeme nerveux de l'homme et des vertebres. Vol. 1. Paris: Maloine .

DiNardo LA , Travers JB (1994). Hypoglossal neural activity during ingestion and rejection in the awake rat. J Neurophysiol 72:1181-1191.

Grillner S. , Hongo T. , Lund S. ( 1970). The vestibulospinal tract. Effects on alpha-motoneurones in the lumbosacral spinal cord in the cat. Exp Brain Res 10:94-120.

Hanson J. , Widen L. (1970). Afferent fibres in the hypoglossal nerve of the cat. Acta Physiol Scand 79:24-36.

Hartwich-Young R. , Nelson JS , Sparks DL (1990). The perihypoglossal projection to the superior colliculus in the rhesus monkey. Visual Neurosci 4:29-42.

Higo S. , Kawano J. , Matsuyama T. , Kawamura S. (1992). Differential projections to the superior collicular layers from the perihypoglossal nuclei in the cat. Brain Res 599:19-28.

10.

Hongo T. , Jankowska E. , Lundberg A. (1972). The rubrospinal tract. IV. Effects on interneurons . Exp Brain Res 15:54-78.

11.

Jankowska E. , Roberts WJ (1972a). An electrophysiological demonstration of the axonal projections of single spinal interneurones in the cat. J Physiol (Lond) 222:597-622.

12.

Jankowska E. , Roberts WJ (1972b). Synaptic actions of single interneurones mediating reciprocal la inhibition of motoneurones. J Physiol (Lond) 222:623-642.

13.

Jean A. ( 1972a). Localization et activite des neurones deglutiteurs bulbaires . J Physiol (Paris) 64:227-268.

14.

Jean A. ( 1972b). Effet de lesions localisees du bulbe rachidien sur le stade oesophagien de la deglutition. J Physiol (Paris) 64:507-516.

15.

Jean A. ( 1984). Control of the central swallowing program by inputs from the peripheral receptors. A review. J Autonom Nerv Syst 10:225-233.

16.

Jean A. ( 1990). Brainstem control of swallowing: localization and organization of the central pattern generator for swallowing. In: Neurophysiology of the jaws and teeth. Taylor A , editor. London: Macmillan Press, pp. 294-321.

17.

Kotchabhakdi N. , Hoddevik GH , Walberg F. (1978). Cerebellar projections from the perihypoglossal nuclei: an experimental study with the method of retrograde axonal transport of horseradish peroxidase. Exp Brain Res 31 :13-29.

18.

Lindquist C. , Martensson A. (1969). Reflex responses induced by stimulation of hypoglossal afferents. Acta Physiol Scand 77:234-240.

19.

Lowe AA ( 1978). Excitatory and inhibitory inputs to hypoglossal motoneurons and adjacent reticular formation neurons in cats. Exp Neurol 62:30-47.

20.

Miller AJ (1972). Significance of sensory inflow to the swallowing reflex. Brain Res 43:147-159.

21.

Miller AJ (1982). Deglutition. Physiol Rev 62:129-184.

22.

Morimoto T. , Kawamura Y. (1972). Inhibitory postsynaptic potentials of hypoglossal motoneurons of the cat. Exp Neurol 37:188-198.

23.

Nakamura Y. , Goldberg LJ , Mizuno N. , Clemente CD (1970). Masseteric reflex inhibition induced by afferent impulses in the hypoglossal nerve. Brain Res 18:241-255.

24.

Ono T. , Ishiwata Y. , Inaba N. , Kuroda T. , Nakamura Y. (1994). Hypoglossal premotor neurons with rhythmical inspiratory-related activity in the cat: localization and projection to the phrenic nucleus. Exp Brain Res 98:1-12.

25.

Sumino R. , Nakamura Y. (1974). Synaptic potentials of hypoglossal motoneurons and a common inhibitory interneuron in the trigemino-hypoglossal reflex. Brain Res 73:439-454.

26.

Takada M. , Itoh K. , Yasui Y. , Mitani A. , Nomura S. , Mizuno N. (1984). Distribution of premotor neurons for the hypoglossal nucleus in the cat. Neurosci Lett 52:141-146.

27.

Tomomune N. , Takata M. (1988). Excitatory and inhibitory postsynaptic potentials in cat hypoglossal motoneurons during swallowing. Exp Brain Res 71:262-272.

28.

Travers JB , Norgren R. (1983). Afferent projections to the oral motor nuclei in the rat. J Comp Neurol 220:280-298.

29.

Walberg F. , Dietrichs E. , Nordby T. (1985). On the projections from the vestibular and perihypoglossal nuclei to the spinal trigeminal and lateral reticular nuclei in the cat. Brain Res 333:123-130.

30.

Zapata P. , Torrealba G. (1988). Reflex effects evoked by stimulation of hypoglossal afferent fibers. Brain Res 445:19-29.

31.

Zimny R. , Grottel K. (1995). Non-reciprocal connections between the perihypoglossal nuclei and the cerebellar paramedian lobule in rabbits and their relationship to the climbing fiber zones. Brain Behav Evol 46:339-353.