Activation of Vestibular Neurons Projecting to Autonomic Brain Stem Nuclei Following Acute Hypotension in Rats

  • Choi, Myoung-Ae (Department of Physiology, Wonkwang University School of Medicine and Vestibulocochlear Research Center at Wonkwang University) ;
  • Wang, Won-Ki (Department of Physiology, Wonkwang University School of Medicine and Vestibulocochlear Research Center at Wonkwang University) ;
  • Choi, Dong-Ok (Department of Physiology, Wonkwang University School of Medicine and Vestibulocochlear Research Center at Wonkwang University) ;
  • Kim, Min-Sun (Department of Physiology, Wonkwang University School of Medicine and Vestibulocochlear Research Center at Wonkwang University) ;
  • Park, Byung-Rim (Department of Physiology, Wonkwang University School of Medicine and Vestibulocochlear Research Center at Wonkwang University)
  • Published : 2004.06.21

Abstract

The purpose of the present study was to elucidate the possible involvement of the medial vestibular nucleus (MVN) and inferior vestibular nucleus (IVN) following acute hypotension in the vestibuloautonomic reflex through vestibulosolitary or vestibuloventrolateral projections. Acute hypotension-induced cFos expression was assessed in combination with retrograde cholera toxin B subunit (CTb) tract tracing. After injection of CTb into the solitary region, CTb-labeled neurons were located prominently around the lateral borders of the caudal MVN and medial border of the IVN. The superior vestibular nucleus also had a scattered distribution of CTb-labeled neurons. After injection of CTb toxin into the unilateral VLM, the distributions of CTb-labeled neurons in the MVN and IVN were similar to that observed after injection into the solitary region, although there were fewer CTb-labeled neurons. In the caudal MVN, about 38% and 13% of CTb-labeled neurons were double-labeled for cFos after injection of CTb into the solitary region and the VLM, respectively. In the IVN, 14% and 7% of CTb-labeled neurons were double-labeled for cFos after injection of CTb into the solitary region and the VLM, respectively. Therefore, the present study suggests that acute arterial hypotension may result in activation of vestibulosolitary pathways that mediate behavioral and visceral reflexes, and vestibuloventrolateral medullary pathways that indirectly mediate vestibulosympathetic responses.

Keywords

References

  1. Altschuler SM, Bao X, Bieger D, Hopkisn DA, MIselis RR. Viscerotopic representation of the upper alimentary tract in the rat: sensory ganglia and nuclei of the soliatry and spinal trigeminal tracts. J Comp Neurol 283: 248-268, 1989 https://doi.org/10.1002/cne.902830207
  2. Andrews JC, Hoover LA, Lee RS, Honrubia V. Vertigo in the hyperviscosity syndrome. Otolaryngol Head Neck Surg 98: 144- 149, 1998
  3. Baer MR, Stein RS, Dessypris EN. Chronic lymphocytic leukemia with hyperleukocytosis: the hyperviscosity syndrome. Cancer 56: 2865-2869, 1985a https://doi.org/10.1002/1097-0142(19851215)56:12<2865::AID-CNCR2820561225>3.0.CO;2-6
  4. Balaban CD. Vestibular autonomic regulation: including motion sickness and the mechanism of vomiting. Curr Opin Neurol 12: 29-33, 1999 https://doi.org/10.1097/00019052-199902000-00005
  5. Balaban CD. Vestibular nucleus projections to the parabrachial nucleus in rabbits: implications for vestibular influences on the autonomic nervous system. Exp Brain Res 108: 367-381, 1996
  6. Balaban CD, Porter JD. Neuroanatomic substrates for vestibuloautonomic interactions. J Vestibular Res 8: 7-16, 1998 https://doi.org/10.1016/S0957-4271(97)00037-2
  7. Balaban CD, 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
  8. Baurle J, Helmchen C, Grusser-Cornehls U. Diverse effects of Purkinje cell loss on deep cerebellar and vestibular nuclei neurons in Purkinje cell degeneration mutant mice: a possible compensatory mechanism. J Comp Neurol 384: 580-596, 1997 https://doi.org/10.1002/(SICI)1096-9861(19970811)384:4<580::AID-CNE7>3.0.CO;2-Z
  9. Berger AJ. Distribution of carotid sinus nerve afferent fibers to solitary tract nuclei of the cat using transganlionic transport of horseadish peroxide. Neurosci Lett 14: 153-158, 1979 https://doi.org/10.1016/0304-3940(79)96140-8
  10. Blessing WW, Reis DJ. Inhibitory cardiovascular function of neurons in the caudal ventrolateral medulla of the rabbit: relationship to the area containing A1 noradrenergic cells. Brain Res 253: 161-171, 1982 https://doi.org/10.1016/0006-8993(82)90683-7
  11. Chalmers J, Arnolda L, Kapoor V, Llewellyn-Smith I, Minson J, Pilowsky P. Amino acid neurotransmitters in the central control of blood pressure and experimental hypertension. J Hypertension 10: 27-37, 1992 https://doi.org/10.1097/00004872-199212007-00002
  12. Chan RK, Sawchenko PE. Spatially and temporally differentiated patterns of c-fos expression in brainstem catecholaminergic cell groups induced by cardiovascular challenges in the rat. J Comp Neurol 348: 433-460, 1994 https://doi.org/10.1002/cne.903480309
  13. Cirelli C, Pompeiano M, D'ascanio P, Arrighi OP, Pompeiano. c-fos expression in the rat brain after unilateral labyrinthectomy and its relation to the uncompensated and compensated. Neurosci 70: 515-546, 1996 https://doi.org/10.1016/0306-4522(95)00369-X
  14. De Zeeuw CI, Berrebi AS. Postsynaptic targets of Purkinje cell terminals in the cerebellar and vestibular nuclei of the rat. Eur J Neurosci 7: 2322-2333, 1995 https://doi.org/10.1111/j.1460-9568.1995.tb00653.x
  15. Ericson H, Blomqvist A. Tracing of neuronal connections with cholera toxin subunit B: light and electron microscopic immunohistochemistry using monoclonal antibodies. J Neurosci Meth 24: 225-235, 1988 https://doi.org/10.1016/0165-0270(88)90167-7
  16. Feldman JL. Neurophysiology of breathing in mammals. In: Handbook of Physiology, The Nervous System. Vol 4, Intrinsic Regulatory Systems of the Brain. Bethesda, American Physiological Society, 1986, pp 463-524
  17. Hardy SGP, Horecky JG, Presley KG. Projections of the caudal ventrolateral medulla to the thoracic spinal cord in the rat. Anat Rec 250: 95-102, 1998
  18. Horiuchi J, Potts PD, Polson JW, Dampney RA. Distribution of neurons projecting to the rostral ventrolateral medullary pressor region that are activated by sustained hypotension. Neuroscience 89: 1319-1329, 1999 https://doi.org/10.1016/S0306-4522(98)00399-6
  19. Kalia M, Mesulam MM. Brain stem projection of sensory and motor components of the vagus complex in the cat, II Laryngeal, tracheobronchial, pulmonary, cardiac and gastrointestianl branches, J Comp Neurol 193: 467-508, 1980 https://doi.org/10.1002/cne.901930211
  20. Kaufman GD, Perachio AA. Translabyrinth electrical stimulation for the induction of immediate-early genes in the gerbil brainstem. Brain Res 646: 345-350, 1994 https://doi.org/10.1016/0006-8993(94)90104-X
  21. Kaufman GD, Anderson JH, Beitz AJ. Fos-defined activity in rat brainstem following centripetal acceleration. J Neurosci 12: 4489 -4500, 1992
  22. Kikuchi S, Kaga K,Yamasoba T, Higo R, O'uchi T, Tokumaru A. Slow blood flow of the vertebrobasilar system in patients with dizziness and vertigo. Acta Otolaryngol 113: 257-260, 1993. https://doi.org/10.3109/00016489309135804
  23. Kim MS, Kim JH, Kry D, Choi MA, Choi DO, Cho BG, Jin YZ, Lee SH, Park BR. Effects of acute hypotension on expression of cFos-like protein in the vestibular nuclei of rats. Brain Res 962: 111-121, 2003 https://doi.org/10.1016/S0006-8993(02)03977-X
  24. Kim MS, Kim JH, Jin YZ, Kry D, Park BR. Temporal changes of cFos-like protein expression in medial vestibular nuclei following arsanilate-induced unilateral labyrinthectomy in rats. Neurosci Lett 319:9-12, 2002 https://doi.org/10.1016/S0304-3940(01)02422-3
  25. Kitahara T, Takeda N, Saika T, Kubo T, Kiyama H. Role of the flocculus in the development of vestibular compensation: immunohistochemical studies with retrograde tracing and flocculectomy using Fos expression as a marker in the rat brainstem. Neurosci 76:571-580, 1997 https://doi.org/10.1016/S0306-4522(96)00374-0
  26. Llewellyn-Smith IJ, Pilowsky P, Minson JB. Retrograde tracers for light and electron microscopy. In: Experimental Neuroanatomy, edited by JP Bolam. London, IRL Press, 1992, pp 31-59
  27. Loewy AD. Central autonomic pathways. In: Central Regulation of Autonomic Functions, edited by AD Loewy and KM Spyer. New York: Oxford Univ Press, 1990, pp 88-103
  28. Luppi PH, Fort P, Jouvet M. Iontophoretic application of unconjugated cholera toxin B subunit (CTb) combined with immunohistochemistry of neurochemical substances: a method for transmitter identification of retrogradely labeled neurons. Brain Res 534: 209-224, 1990 https://doi.org/10.1016/0006-8993(90)90131-T
  29. Matsunaga T, Sano M, Yamamoto K, Kubo T. Vestibular neuronal function during ischemia. Response of vestibular neurons to vertebral and carotid artery occlusion in rabbits. Adv Otorhinolaryngol 25: 184-191, 1979
  30. Money KE. Motion sickness. Physiol Rev 50: 1-39, 1970 https://doi.org/10.1152/physrev.1970.50.1.1
  31. Morgan JI, Curran T. Stimulus-transcription coupling in the nervous system: Involvement of the inducible proto-oncogenes Fos and Jun. Annu Rev Neurosci 14: 421-451, 1991 https://doi.org/10.1146/annurev.ne.14.030191.002225
  32. Nario K, Matsunaga T, Inui H, Murai T, Miyahara H. ABR findings, electrocochleograms and caloric tests in vertebrobasilar ischemic rats. Acta Otolaryngol Suppl 528: 63-66, 1997
  33. Park BR, Kim MS, Kim JH, Jin YZ. Effects of acute hypotension on neuronal activity in the medial vestibular nuclei of rats. Neuroreport 12: 3821-3824, 2001 https://doi.org/10.1097/00001756-200112040-00044
  34. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates, New York, Academic Press, 1997
  35. Porter JD, Balaban CD. Connections between the vestibular nuclei and brain stem regions that mediate autonomic function in the rat. J Vestibular Res 7: 63-76, 1997 https://doi.org/10.1016/S0957-4271(96)00138-3
  36. Pujol R, Puel JL, D'aldin CG, Eybalin M. Pathophysiology of the glutamatergic synapses in the cochlea. Acta Otolaryngol 113: 330-334, 1993. https://doi.org/10.3109/00016489309135819
  37. Pyner S, Coote JH. Rostroventrolateral medulla neurons preferentially project to target-specified sympathetic preganglionic neurons. Neuroscience 83: 617-631, 1998 https://doi.org/10.1016/S0306-4522(97)00355-2
  38. Ruggiero DA, Mtui EP, Otake K, Anwar M. Vestibular afferents to the dorsal vagal complex: substrate for vestibular-autonomic interactions in the rat. Brain Res 743: 294-302, 1996 https://doi.org/10.1016/S0006-8993(96)01099-2
  39. Steinbacher BC Jr, Yates BJ. Processing of vestibular and other inputs by the caudal ventrolateral medullary reticular formation. Am J Physiol 271: R1070-1077, 1996
  40. Stocker SD, Steinbacher BC Jr, Balaban CD, Yates BJ. Connections of the caudal ventrolateral medullary reticular formation in the cat brainstem. Exp Brain Res 116: 270-282, 1997 https://doi.org/10.1007/PL00005755
  41. Yamamoto K, Kubo T, Matsunaga T. Effects of asymmetric vertebral blood flow upon the vestibulo-ocular reflex of the rabbit. Arch Otorhinolaryngol 241: 195-202, 1985 https://doi.org/10.1007/BF00454354
  42. Yates BJ, Miller AD. Properties of sympathetic reflexes elicited by natural vestibular stimulation: implications for cardiovascular control. J Neurophysiol 71: 2087-2092, 1994 https://doi.org/10.1152/jn.1994.71.6.2087
  43. Yates BJ. Vestibular influences on cardiovascular control. In: Vestibular autonomic regulation, edited by BJ Yates and AD Miller, New York, CRC Press, 1996, pp 97-111
  44. Yates BJ, Balaban CD, Miller AD, Endo K, Yamaguchi Y. Vestibular inputs to the lateral tegmental field of the cat: potential role in autonomic control. Brain Res 689: 197-206, 1995 https://doi.org/10.1016/0006-8993(95)00569-C
  45. Yates BJ, Goto T, Bolton PS. Responses of neurons in the rostral ventrolateral medulla of the cat to natural vestibular stimulation. Brain Res 601: 255-264, 1993 https://doi.org/10.1016/0006-8993(93)91718-8
  46. Yates BJ, Goto T, Kerman I, Bolton PS. Responses of caudal medullary raphe neurons to natural vestibular stimulation. J Neurophysiol 70: 938-946, 1993 https://doi.org/10.1152/jn.1993.70.3.938
  47. Yates BJ, Yamagata Y, Bolton PS. The ventrolateral medulla of the cat mediates vestibulosympathetic reflexes. Brain Res 552: 265-272, 1991 https://doi.org/10.1016/0006-8993(91)90091-9
  48. Zagon A, Smith AD. Monosynaptic projections from the rostral ventrolateral medulla oblongata to identified sympathetic preganglionic neurons. Neuroscience, 54: 729-743, 1993 https://doi.org/10.1016/0306-4522(93)90243-9