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Neuronal activity in nucleus ambiguus during deglutition and vocalization in conscious monkeys

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Abstract

Extracellular recordings were made from the nucleus ambiguus in three conscious Macaca nemestrina monkeys during spontaneous vocalizations and swallows. The temporal relationship of neuronal activity to swallowing was inferred through correlation with the thyroarytenoid electromyographic (EMG) activity. Videofluoroscopic analysis of a fourth monkey during swallows of barium-impregnated fruit juice established the temporal relationship between swallowing and thyroarytenoid EMG activity. Of 691 cells recorded from the nucleus ambiguus and its adjacent area, the neuronal activity of 80 cells showed modulation during swallowing. Sixty-two cells were classified as “active” cells, with increased activity in relation to swallowing, while 18 cells were classified as “suppressed” cells, with tonic activity that reduced with swallowing. A continuum of latency was seen between the onset of modulation of these cells and the onset of swallowing, from “early” before the swallow to “late” after the swallow onset with most of the cells (44 cells) showing modulation near the onset of the swallow. A majority (37) of the 62 active swallowing-related cells also discharged with vocalization, but they demonstrated a lower discharge frequency and a longer burst duration during swallowing. Of the 18 suppressed swallowing-related cells, 11 cells discharged phasically with the respiratory cycle and may be a part of the ventral medullary respiratory center. This chronic awake primate model would preserve the many sensory inputs that may modify the oropharyngeal swallow and may better approximate human physiology.

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References

  1. Amri M, Car A (1988) Projection from the medullary swallowing center to the hypoglossal motor nucleus: a neuroanatomical and electrophysiological study in sheep. Brain Res 441:119–126

  2. Amri M, Car A, Jean A (1984) Medullary control of the pontine swallowing neurones in sheep. Exp Brain Res 55:105–110

  3. 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

  4. Bieger D, Hopkins DA (1987) Viscerotopic representation of the upper alimentary tract in the medulla oblongata in the rat: The nucleus ambiguus. J Comp Neurol 262:546–562

  5. Cohen MI (1981) Central determinants of respiratory rhythm. Annu Rev Physiol 43:91–104

  6. Doty RW, Bosma JF (1956) An electrophysiological analysis of reflex deglutition. J Neurophysiol 19:44–60

  7. Falempin M, Rousseau JP (1984) Activity of lingual, laryngeal and oesophageal receptors in conscious sheep. J Physiol (Lond) 347:47–58

  8. Hukuhara T, Okada H (1956) Effects of deglutition upon spike discharges of neurons in the respiratory center. Jpn J Physiol 6:162–166

  9. Jean A (1984a) Brainstem organization of the swallowing network. Brain Behav Evol 25:109–116

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

  11. Jean A (1990) Brainstem control of swallowing: localization and organization of the central generator for swallowing. In: Taylor A (ed) Neurophysiology of the jaw and teeth. Macmillan, New York, pp 294–321

  12. Kalia M, Mesulam M (1980) Brainstem projections of sensory and motor components of the Vagus complex in the cat: II. Laryngeal, tracheobronchial, pulmonary, cardiac, and gastrointestinal branches. J Comp Neurol 193:467–508

  13. Kessler JP, Jean A (1985) Identification of the medullary swallowing regions in the rat. Exp Brain Res 57:256–263

  14. Larson CR (1991) On the relation of PAG neurons to laryngeal and respiratory muscles during vocalization in the monkey. Brain Res 552:77–86

  15. Larson CR, Yajima Y, Ko P Modification in activity of medullary respiratory-related neurons for vocalization and swallowing. J Neurophysiol (in press)

  16. Lawson EE, Richter DW, Czyzyk-Krzeska MF, Bischoff A, Rudesil RC (1991) Respiratory neuronal activity during apnea and other breathing patterns induced by laryngeal stimulation. J Appl Physiol 70:2742–2749

  17. Logemann J, Kahrilas PJ, Egelman J, Dodds W, Pauloski B (1989) Interactive computer program for biomechanical analysis of videoradiographic studies of swallowing. Am J Roentgenol 153:277–280

  18. Miller A (1993) The search for the central swallowing pathway: the quest for clarity. Dysphagia 8:185–194

  19. Nuñez-Abades P, Pasaro R, Bianchi A (1992) Study of the topographical distribution of different population of motoneurons within rat's nucleus ambiguus, by means of four different fluorochromes. Neurosci Lett 135:103–107

  20. Shaker R, Dodds W, Dantas R, Hogan W, Arndorfer R (1990) Coordination of deglutitive glottic closure with oropharyngeal swallowing. Gastroenterology 98:1478–1484

  21. Sumi T (1963) The activity of brain-stem respiratory neurons and spinal respiratory motoneurons during swallowing. J Neurophysiol 26:466–477

  22. West R, Larson CR (1993) Laryngeal and respiratory activity during vocalization in Macaque monkeys. J Voice 7:54–68

  23. Yajima Y, Hayashi Y (1983) Ambiguous motoneurons discharging synchronously with ultrasonic vocalization in rats. Exp Brain Res 50:359–366

  24. Yajima Y, Larson CR (1993) Multifunctional properties of ambiguous neurons identified electrophysiologically during vocalization in the awake monkey. J Neurophysiol 70:529–540

  25. Yoshida Y, Mitsumasu T, Hirano M, Kanaseki T (1985) Somatotopic representation of the laryngeal motoneurons in the medulla of monkeys. Acta Otolaryngol (Stockh) 100:299–303

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Chiao, G.Z., Larson, C.R., Yajima, Y. et al. Neuronal activity in nucleus ambiguus during deglutition and vocalization in conscious monkeys. Exp Brain Res 100, 29–38 (1994). https://doi.org/10.1007/BF00227276

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Key words

  • Nucleus ambiguus
  • Oropharyngeal swallow
  • Vocalization
  • Ventral medullary swallowing center
  • Larynx
  • Monkey