Vestibular nucleus projections to nucleus tractus solitarius and the dorsal motor nucleus of the vagus nerve: potential substrates for vestibulo-autonomic interactions

Experimental Brain Research volume 98, pages200–212(1994)Cite this article

Abstract

Autonomic effects of vestibular stimulation are important components of phenomena as diverse as acute vestibular dysfunction and motion sickness. How ever, the organization of neural circuits mediating these responses is poorly understood. This study presents evidence for direct vestibular nucleus projections to brain stem regions that mediate autonomic function. One group of albino rabbits received injections of Phaseolus vulgaris leucoagglutinin into the vestibular nuclei. The tracer was visualized immunocytochemically with standard techniques. Anterogradely labeled axons from the caudal medial vestibular nucleus (cMVN) and inferior vestibular nucleus (IVN) could be traced bilaterally to nucleus tractus solitarius (NTS). Fewer axons ended near the somata of neurons in the dorsal motor nucleus of the vagus nerve (DMX). A second group of rabbits received pressure or iontophoretic injections of cholera toxin B-HRP or Fluoro-Gold into a region including NTS and DMX. Retrogradely labeled neurons were observed bilaterally in the caudal half of cMVN and ipsilaterally in IVN. The labeled somata were small and they tended to occupy the center of cMVN in transverse sections. These previously unreported vestibular nucleus projections to NTS and DMX are a potential substrate for vestibular influences on autonomic function. In particular, they may contribute to both cardiovascular control during head movements (e.g., orthostatic reflexes) and autonomic manifestions of vestibular dysfunction, motion sickness and exposure to altered gravitational environments.

This is a preview of subscription content, log in to check access.

Access options

Buy single article

Instant access to the full article PDF.

US$ 39.95

Tax calculation will be finalised during checkout.

References

  1. Akert K, Gernandt BE (1962) Neurophysiological study of vestibular and limbic influences upon vagal outflow Electroenceph Clin Neurophysiol 14:904–914.

    Google Scholar 

  2. Baloh R (1984) Dizziness, hearing loss and tinnitus: the essentials of neurotology. Davis, Philadelphia.

    Google Scholar 

  3. Barraco RA, El-Ridi MR (1989) Cardiorespiratory responses following electrical stimulation of caudal sites in the rat medulla. Brain Res Bull 23:299–310.

    Google Scholar 

  4. Blessing WW (1990) Distribution of glutamate decarboxylase containing neurons in rabbit medulla oblongata with attention to intramedullary and spinal projections. Neuroscience 37:171–185.

    Google Scholar 

  5. Blessing WW, Goodchild AK, Dampney RAL, Chalmers JP (1981) Cell groups in the lower brain stem of the rabbit projecting to the spinal cord, with special reference to cate cholamine-containing neurons. Brain Res 221:35–55.

    Google Scholar 

  6. Carleton SC, Carpenter MB (1984) Distribution of primary vestibular fibers in the brainstem and cerebellum of the monkey. Brain Res 294:281–298.

    Google Scholar 

  7. Cobbold AF, Meghirian D, Sherry JH (1968) Vestibular evoked activity in autonomic outflows. Arch Ital Biol 106:113–123.

    Google Scholar 

  8. Doba N, Reis DJ (1974) Role of the cerebellum and vestibular apparatus in regulation of orthostatic reflexes in the cat. Circ Res 34:9–18.

    Google Scholar 

  9. Donaghue S, Garcia M, Jordan D, Spyer KM (1982a) Identification and brain-stem projections of aortic baroreceptor afferent neurones in nodose ganglia of cats and rabbits. J Physiol (Lond) 322:337–352.

    Google Scholar 

  10. Donaghue S, Garcia M, Jordan D, Spyer KM (1982b) The brainstem projections of pulmonary stretch afferent neurones in cats and rabbits. J Physiol (Lond) 322:353–36.

    Google Scholar 

  11. Donaghue S, Felder RB, Jordan D, Spyer KM (1984) The central projections of carotid baroreceptors and chemoreceptors in the cat: a neurophysiological study. J Physiol (Lond) 347:397–409.

    Google Scholar 

  12. Elisevich K, Ciriello J (1988) Vestibular nucleus inputs to paramedian reticulospinal neurons in the cat. Neurosci Lett 91:1–6.

    Google Scholar 

  13. Elisevich KV, Hrycyshyn AW, Flumerfelt BA (1985) Cerebellar, medullary and spinal afferent connections of the paramedian reticular nucleus in the cat. Brain Res 332:267–282.

    Google Scholar 

  14. Feldman JL, Ellenberger HH (1988) Central coordination of respiratory and cardiovascular control in mammals. Ann Rev Physiol 50:593–606.

    Google Scholar 

  15. Goodhill V (1979) Ear diseases: deafness and dizziness. Harper and Row, Hagerstown, pp 224–225.

    Google Scholar 

  16. Henry RT, Connor JD, Balaban CD (1989) Nodulus-uvula depressor response: central GABA-mediate inhibition of αadrenergic outflow. Am J Physiol 256 (Heart Circ Physiol 25): H1601-H1608.

    Google Scholar 

  17. Hu S, Stern RM, Vasey MW, Koch K (1989) Motion sickness and gastric myoelectric activity as a function of speed of rotation of a circular vection drum. Aviat Space Environ Med 60:411–414.

    Google Scholar 

  18. Hudson LC (1986) The origins of innervation of the canine caudal pharyngeal muscles: an HRP study. Brain Res 374:413–418.

    Google Scholar 

  19. Igarashi M, Himi T, Ishii M, Patel S (1988) Studies on R-R intervals and salivation in visual-vestibular conflict sickness. In: Igarashi M, Nute K (eds) Proceedings of the symposium on vestibular organs and altered force environment, NASA/ Space Biomedical Research Institute, USRA/Division of Space Biomedicine, Houston, pp 57–60.

    Google Scholar 

  20. Kalia M (1981) Anatomical organization of central respiratory neurons. Ann Rev Physiol 43:105–120.

    Google Scholar 

  21. Kalia M, Mesulam M-M (1980) Brain stem 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.

    Google Scholar 

  22. Kasper J, Schor RH, Wilson VJ (1988) Response of vestibular neurons to head rotations in vertical planes. I. Response to vestibular stimulation. J Neurophysiol 60:1753–1764.

    Google Scholar 

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

    Google Scholar 

  24. Lin RH, Lin AMY, Su CK, Kuo JS, Chai CY (1989) Presence of perikarya for vasopressor actions in both the dorsolateral and ventrolateral regions of medulla oblongata in swine. Neurosci Res Comm 5:125–133.

    Google Scholar 

  25. Loewy AD (1990) Central autonomic pathways. In: Loewy AD, Spyer KM (eds) Central regulation of autonomic function. Oxford University Press, New York, pp 88–103.

    Google Scholar 

  26. Loewy AD, Burton H (1978) Nuclei of the solitary tract: efferent projections to the lower brain stem and spinal cord of the cat. J Comp Neural 181:421–449.

    Google Scholar 

  27. McLean, IW Nakane PK (1974) Periodate-lysine-paraformaldehyde fixative for immunoelectron microscopy. J Histochem Cytochem 22:1077–1083.

    CAS  PubMed  Google Scholar 

  28. Meesen H, Olszewski J (1949) A cytoarchitectonic atlas of the rhombencephalon of the rabbit. S. Karger, New York.

    Google Scholar 

  29. Meghirian D Manning JW (1967) Input-output relations of the vestibular system. Arch Ital Biol 105:15–30.

    Google Scholar 

  30. Mergner T, Pompeiano O, Corvaja N (1977) Vestibular projections to the nucleus intercalatus of Staderini ragged by retrograde transport of horseradish peroxidase. Neurosci Lett 6:309–313.

    Google Scholar 

  31. Money KE (1970) Motion sickness. Physiol Rev 50:1–39.

    Google Scholar 

  32. Moruzzi G (1940) Paleocerebellar inhibition of vasomotor and respiratory carotid sinus reflexes. J Neurophysiol 3:20–32.

    Google Scholar 

  33. Neuhuber WL, Zenker W (1989) Central distribution of cervical primary afferents in the rat, with emphasis on proprioceptive projections to vestibular, perihypoglossal and upper thoracic spinal nuclei. J Comp Neurol 280:231–253.

    CAS  PubMed  Google Scholar 

  34. Nisimaru N, Yamamoto Y (1977) Depressant action of the posterior lobe of the cerebellum upon renal sympathetic nerve activity. Brain Res 133:371–375.

    Google Scholar 

  35. Nisimaru N, Watanabe Y (1985) A depressant area in the lateral nodulus-uvula of the cerebellum for renal sympathetic nerve activity and systemic blood pressure in the rabbit. Neurosci Res 3:177–181.

    Google Scholar 

  36. Nisimaru N, Yamamoto M, Shimoyama I (1984) Inhibitory effects of cerebellar cortical stimulation on sympathetic nerve activity in rabbits. Jpn J Physiol 34:539–551.

    Google Scholar 

  37. Paton JFR, La Noce M, Sykes RM, Sebastiani L, Bagnoli P, Gherlarducci B, Bradley DJ (1991) Efferent connections of lobule IX of the posterior cerebellar cortex in the rabbit-some functional considerations. J Autonom Nerv Syst 36:209–224.

    Google Scholar 

  38. Peterson BW 1970 Distribution of neural responses to tilting within vestibular nuclei of the cat, J Neurophysiol 33:750–767.

    Google Scholar 

  39. Reason JT, Brand JJ (1975) Motion sickness. Academic Press, London.

    Google Scholar 

  40. Schor RH, Miller AD, Tomko DL (1984) Responses to head tilt in cat central vestibular neurons. I. Direction of maximum sensitivity. J Neurophysiol 51:136–146.

    Google Scholar 

  41. Siegborn J, Grant G (1983) Brainstem projections of different branches of the vestibular nerve. An experimental study by transganglionic transport of horseradish peroxidase in the cat. I. The horizontal ampullary and utricular nerves. Arch Ital Biol 121:237–248.

    Google Scholar 

  42. Siegborn J, Yingcharoen K, Grant G (1991) Brainstem projections of different branches of the vestibular nerve. An experimental study by transganglionic transport of horseradish peroxidase in the cat. II. The anterior and posterior ampullary nerves. Anat Embryol 184:291–299.

    Google Scholar 

  43. Spiegel EA (1936) Respiratory reactions upon vertical movements. Am J Physiol 117:349–354.

    Google Scholar 

  44. Spiegel EA (1946) Effect of labyrinthine reflexes on the vegetative nervous system. A review. Arch Otolaryngol 44:61–72.

    Google Scholar 

  45. Spiegel EA, Démétriades TD (1922) Beiträge zum Studium des vegetativen Nervensystems. III. Mitteilung. Der Einfluss des Vestibularappates auf das Gefäßsystem. Pfluger's Arch Ges Physiol 196:188–199.

    Google Scholar 

  46. Spiegel EA, Démétriades TD (1924) Der zentrale Mechanismus der vestibulären Blutdrucksenkung und ihre Bedeutung für die Entstehung des Labyrinthschwindels. Pfluger's Arch Ges Physiol 205:328–337.

    Google Scholar 

  47. Spiegel EA, Sommer I (1944) Vestibular mechanisms. In: Glasser O (eds) Medical Physics. Year Book, Chicago, pp 1638–1655.

    Google Scholar 

  48. Spyer KM (1990) The central organization of reflex circulatory control. In: Loewy AD, Spyer KM (eds) Central regulation of autonomic function. Oxford University Press, New York, pp 168–188.

    Google Scholar 

  49. Stechison MT, Saint-Cyr JA, Spence SJ (1985) Projections from the nuclei prepositus hypoglossi and intercalatus to the superior colliculus in the cat: an anatomical study using WGA HRP. Exp Brain Res 59:139–150.

    Google Scholar 

  50. Tang PC, Gernandt BE (1969) Autonomic responses to vestibular stimulation. Exp Neurol 24:558–578.

    Google Scholar 

  51. Uchino Y, Kudo N, Tsuda K, Iwamura Y (1970) Vestibular inhibition of sympathetic nerve activities. Brain Res 22:195–206.

    Google Scholar 

  52. Wallach JH, Loewy AD (1980) Projections of the aortic nerve to the nucleus tractus solitarius in the rabbit. Brain Res 188:247–251.

    Google Scholar 

  53. Yates BJ (1992) Vestibular influences on the sympathetic nervous system. Brain Res Rev 17:51–59.

    Google Scholar 

  54. Yates BJ, Yamagata Y (1990) Convergence of cardiovascular and vestibular inputs on neurons in the medullary paramedian reticular formation. Brain Res 513:166–170.

    Google Scholar 

  55. Yates BJ, Yamagata Y, Bolton PS (1991) The ventrolateral medulla of the cat mediates vestibulosympathetic reflexes. Brain Res 552:265–272.

    Google Scholar 

  56. Yates BJ, Goto T, Bolton PS (1993a) Responses of neurons in the rostral ventrolateral medulla of the cat to natural vestibular stimulation. Brain Res. 601:255–264.

    Google Scholar 

  57. Yates BJ, Jakus J, Miller AD (1993b) Vestibular effects on respiratory outflow in the decerebrate cat. Brain Res 629:209–217.

    Google Scholar 

Download references

Author information

Affiliations

  1. Department of Otolaryngology, University of Pittsburgh, The Eye and Ear Institute, 203 Lothrop Street, 15213, Pittsburgh, PA, USA

    Carey D. Balaban & Gennady Beryozkin

Authors
  1. Carey D. Balaban
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gennady Beryozkin
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Balaban, C.D., Beryozkin, G. Vestibular nucleus projections to nucleus tractus solitarius and the dorsal motor nucleus of the vagus nerve: potential substrates for vestibulo-autonomic interactions. Exp Brain Res 98, 200–212 (1994). https://doi.org/10.1007/BF00228409

Download citation

Key words

  • Vestibular nuclei
  • Autonomic nervous system
  • Nucleus tractus solitarius
  • Dorsal motor vagal nucleus
  • Rabbit