Abstract
Localization and projection to the phrenic (PH) nucleus were studied in a sample of premotor neurons that directly projected to hypoglossal motoneurons (XII Mns) and showed respiratory-related patterns of activity. The experiments were carried out in cats, under pentobarbital anesthesia. In the first part of the study, the retrograde double-labeling technique was used to reveal the existence of neurons projecting to both the XII and the PH nuclei. Injection of a fluorescent dye (fast blue, FB) into the XII nucleus and another (nuclear yellow, NY) into the PH nucleus retrogradely labeled, with either FB or NY, medullary reticular neurons mainly in the regions ventrolateral to the nucleus of the tractus solitarius (vl-NTS), ventrolateral to the hypoglossal nucleus (vl-XII), and dorsomedial to the nucleus ambiguus (dm-AMB) bilaterally. In addition, some neurons in these regions were labeled with both FB and NY. In the second part of the study, unitary activity was recorded extracellularly from medullary respiratory neurons. In the regions vl-NTS, vl-XII, and dm-AMB, inspiratory neurons were found which antidromically responded to stimulation of the XII nucleus. Some of them also responded antidromically to stimulation of the PH nucleus. Averaging of rectified and integrated XII and PH nerve discharges by spontaneous spikes of single inspiratory neurons in the vl-NTS and dm-AMB regions revealed a facilitation in either XII nerve discharge or both XII and PH nerve discharges after a short latency of monosynaptic range. It is concluded that in the vl-NTS and dm-AMB regions there are inspiratory neurons that are excitatory premotor neurons projecting to XII Mns showing the respiratory-related activity. Some of them have excitatory synaptic connections to XII and PH Mns via bifurcating axons.
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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
Arita H, Ochiishi M (1991) Opposing effects of 5-hydroxytryptamine on two types of medullary inspiratory neurons with distinct firing patterns. J Neurophysiol 66:285–292
Bentivoglio M, Kuypers HGJM, Catsman-Berrevoets CE (1980) Retrograde neuronal labeling by means of bisbenzimide and Nuclear Yellow (Hoechst S 769121). Measures to prevent diffusion on the tracers out of retrogradely labeled neurons. Neurosci Lett 18:19–24
Cohen MI (1979) Neurogenesis of respiratory rhythm in the mammal. Physiol Rev 59:1105–1173
Davies JGM, Kirkwood PA, Sears TA (1985a) The detection of monosynaptic connexions from inspiratory bulbospinal neurones to inspiratory motoneurons in the cat. J Physiol (Lond) 368:33–62
Davies JGM, Kirkwood PA, Sears TA (1985b) The distribution of monosynaptic connexions from inspiratory bulbospinal neurones to inspiratory motoneurons in the cat. J Physiol (Lond) 368:63–87
Dellow PG, Lund JP (1971) Evidence for central timing of rhythmical mastication. J Physiol (Lond) 215:1–13
Duggan AW, Lodge D, Biscoe TJ (1973) The inhibition of hypoglossal motoneurones by impulses in the glossopharyngeal nerve of the rat. Exp Brain Res 17:261–270
Ellenberger HH, Feldman JL, Goshgarian HG (1990) Ventral respiratory group projections to phrenic motoneurons: electron microscopic evidence for monosynaptic connections. J Comp Neurol 302:707–714
Ezure K, Manabe M (1989) Monosynaptic excitation of medullary inspiratory neurons by bulbospinal inspiratory neurons of the ventral respiratory group in the cat. Exp Brain Res 74:501–511
Feldman JL, Speck DF (1983) Interactions among inspiratory neurons in dorsal and ventral respiratory groups in cat medulla. J Neurophysiol 49:472–490
Holtman JR Jr (1988) Immunohistochemical localization of serotonin- and substance P-containing fibers around respiratory muscle motoneurons in the nucleus ambiguus of the cat. Neuroscience 26:169–178
Hunter IW, Porter R (1974) Glossopharyngeal influences on hypoglossal motoneurones in the cat. Brain Res 74:161–166
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
Jankowska E, Roberts WJ (1972b) Synaptic actions of single interneurones mediating reciprocal Ia inhibition of motoneurones. J Physiol (Lond) 222:623–642
Keizer K, Kuypers HGJM (1984) Distribution of corticospinal neurons with collaterals to the lower brain stem reticular formation in cat. Exp Brain Res 54:107–120
Keizer K, Kuypers HGJM (1989) Distribution of corticospinal neurons with collaterals to the lower brain stem reticular formation in monkey (Macaca fascicularis). Exp Brain Res 74:311–318
Killackey HP, Koralek KA, Chiaia NL, Rhoades RW (1989) Laminar and areal differences in the origin of the subcortical projection neurons of the rat somatosensory cortex. J Comp Neurol 282:428–445
Lalley PM (1986) Serotoninergic and non-serotoninergic responses of phrenic motoneurones to raphe stimulation in the cat. J Physiol (Lond) 380:373–385
Lowe AA (1981) The neural regulation of tongue movement. Prog Neurobiol 15:295–344
Lowe AA (1990) Neural control of tongue posture. In: Taylor A (ed) Neurophysiology of the jaws and teeth. Macmillan, London, pp 322–368
Lund JP, Dellow PG (1973) Rhythmical masticatory activity of hypoglossal motoneurons responding to an oral stimulus. Exp Neurol 40:243–246
Lunteren E van, Strohl KP (1986) The muscle of the upper airways. Clin Chest Med 7:171–188
Lunteren E van, Dick TE (1992) Intrinsic properties of pharyngeal and diaphragmatic respiratory motoneurons and muscles. J Appl Physiol 73:787–800
Manabe M, Ezure K (1988) Excitatory connection between inspiratory neurons of the ventral respiratory group. Nippon Seirigaku Zasshi 50:586
Manaker S, Tischler LJ, Morrison AR (1992) Raphespinal and reticulospinal axon collaterals to the hypoglossal nucleus in the rat. J Comp Neurol 322:68–78
Merrill EG, Lipski J (1987) Inputs to intercostal motoneurons from ventrolateral medullary respiratory neurons in the cat. J Neurophysiol 57:1837–1853
Miller AD, Ezure K, Suzuki I (1985) Control of abdominal muscles by brain stem respiratory neurons in the cat. J Neurophysiol 54:155–167
Morimoto T, Kawamura Y (1972) Inhibitory postsynaptic potentials of hypoglossal motoneurons of the cat. Exp Neurol 37:188–198
Morimoto T, Tanaka M, Kawamura Y (1972) Inhibiton of hypoglossal motoneurons by a masseteric nerve volley. Brain Res 43:285–288
Morin D, Hennequin S, Monteau R, Hilaire G (1990) Serotonergic influences on central respiratory activity: an in vitro study in the newborn rat. Brain Res 535:281–287
Onai T, Miura M (1986) Projections of supraspinal structures to the phrenic motor nucleus in cats studied by a horseradish peroxidase microinjection method. J Auton Nerv Syst 16:61–77
Ono T, Ishiwata Y, Kuroda T, Nakamura Y (1989) Respiratory neurons in medullary reticular formation directly project to hypoglossal nucleus (abstract). Jpn J Oral Biol 31:5
Otake K, Sasaki H, Ezure K, Manabe M (1989) Axonal trajectory and terminal distribution of inspiratory neurons of the dorsal respiratory group in the cat's medulla. J Comp Neurol 286:218–230
Peterson B, Maunz RA, Pitts HNG, Mackel RG (1975) Patterns of projection and branching of reticulospinal neurons. Exp Brain Res 23:333–351
Portillo F, Pásaro R (1988) Location of bulbospinal neurons and of laryngeal motoneurons within the nucleus ambiguus of the rat and cat by means of retrograde fluorescent labelling. J Anat 159:11–18
Rikard-Bell GC, Bystrzycka EK, Nail BS (1984) Brainstem projection to the phrenic nucleus: a HRP study in the cat. Brain Res Bull 12:469–477
Sasaki H, Otake K, Mannen H, Ezure K, Manabe M (1989) Morphology of augmenting inspiratory neurons of the ventral respiratory group in the cat. J Comp Neurol 282:157–168
Schwartz ML, Goldman-Rakic PS (1982) Single cortical neurones have axon collaterals to ipsilateral and contralateral cortex in fetal and adult primates. Nature 299:154–155
Shinoda Y, Arnold AP, Asanuma H (1976) Spinal branching of corticospinal axons in the cat. Exp Brain Res 26:215–234
Shinoda Y, Ghez C, Arnold AP (1977) Spinal branching of rubrospinal axons in the cat. Exp Brain Res 30:203–218
Sica AL, Cohen MI, Donnelly DF, Zhang H (1984) Hypoglossal motoneurons responses to pulmonary and superior laryngeal afferents inputs. Respir Physiol 56:339–357
Sumi T (1969) Synaptic potentials of hypoglossal motoneurons and their relation to reflex deglutition. Jpn J Physiol 19:68–79
Sumi T (1970a) Activity in single hypoglossal fibers during cortically induced swallowing and chewing in rabbits. Pflügers Arch 314:329–346
Sumi T (1970b) Changes of hypoglossal nerve activity during inhibition of chewing and swallowing by lingual nerve stimulation. Pflügers Arch 317:303–309
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
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
Takata M, Tomomune N (1986) Properties of postsynaptic potentials evoked in hypoglossal motoneurons by inferior alveolar nerve stimulation. Exp Neurol 93:117–127
Travers JB, Jackson LM (1992) Hypoglossal neural activity during licking and swallowing in the awake rat. J Neurophysiol 67:1171–1184
Withington-Wray DJ, Mifflin SW, Spyer KM (1988) Intracellular analysis of respiratory modulated hypoglossal motoneurons in the cat. Neuroscience 25:1041–1051
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Ono, T., Ishiwata, Y., Inaba, N. et al. Hypoglossal premotor neurons with rhythmical inspiratory-related activity in the cat: localization and projection to the phrenic nucleus. Exp Brain Res 98, 1–12 (1994). https://doi.org/10.1007/BF00229103
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DOI: https://doi.org/10.1007/BF00229103