Fos expression in neurons of the rat vestibulo-autonomic pathway activated by sinusoidal galvanic vestibular stimulation

Frontiers in Neurology

Volumn FEB, Issue , 2012, Pages

  Holstein, Gay R ^a   Friedrich, Victor L ^a   Martinelli, Giorgio P ^a   Ogorodnikov, Dmitri ^a   Yakushin, Sergei B ^a   Cohen, Bernard ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Blood pressure; Heart rate; Orthostatic hypotension; Otolith organs; Rostral ventrolateral medulla; Sympathetic nervous system; Vasovagal syncope; Vestibular nuclei

Indexed keywords

EID: 84864283735     PISSN: None     EISSN: 16642295     Source Type: Journal    
DOI: 10.3389/fneur.2012.00004     Document Type: Article

References (98)

1. Abe, C., Tanaka, K., Awazu, C., and Morita, H. (2008). Strong galvanic vestibular stimulation obscures arterial pressure response to gravitational change in conscious rats. J. Appl. Physiol. 104, 34-40.
2. Abe, C., Tanaka, K., Awazu, C., and Morita, H. (2009). Galvanic vestibular stimulation counteracts hypergravity-induced plastic alteration of vestibulo-cardiovascular reflex in rats. J. Appl. Physiol. 107, 1089-1094.
3. Armstrong, D. M., Ross, C. A., Pickel, V. M., Joh, T. H., and Reis, D. J. (1982). Distribution of dopamine-, noradrenaline-, and adrenaline-containing cell bodies in the rat medulla oblongata: Demonstration by the immunocytochem-ical localization of catecholamine biosynthetic enzymes. J. Comp. Neurol. 212, 173-187.
4. Baizer, J. S., Corwin, W. L., and Baker, J. F. (2010). Otolith stimulation induces c-Fos expression in vestibular and precerebellar nuclei in cats and squirrel monkeys. Brain Res. 1351, 64-73.
5. Balaban, C. D., and Beryozkin, G. (1994). Vestibular nucleus projections to nucleus tractus solitarius and the dorsal motor nucleus of the vagus nerve: potential substrates for vestibular-autonomic interactions. Exp. Brain Res. 98, 200-212.
6. Balaban, C. D., and Yates, B. J. (2004). "Vestibulo -autonomic interactions: a teleological perspective," in The Vestibular System, eds S. H. High-stein, R. R. Fay, and A. N. Popper (Wein: Springer), 286-342.
7. Barmack,N.H. (2003). Central vestibular system: vestibular nuclei and posterior cerebellum. Brain Res. Bull. 60, 511-541.
8. Bent, L. R., Bolton, P. S., and Mace-field, V. G. (2006). Modulation of muscle sympathetic bursts by sinusoidal galvanic vestibular stimulation in human subjects. Exp. Brain Res. 174,701-711.
9. Bourassa, E. A., Sved, A. F., and Speth, R. C. (2009). Angiotensin modulation of rostral ventrolateral medulla (RVLM) in cardiovascular regulation. Mol. Cell. Endocrinol. 302, 167-175.
10. Bradbury, S., and Eggleston, C. (1925). Postural hypotension. A report of three cases. Am. Heart J. 1, 73-86.
11. Büttner-Ennever, J. A. (1992). "Patterns of connectivity in the vestibular nuclei," in Sensing and Controlling Motion: Vestibular and Senso-rimotor Function, eds B. Cohen, D. Tomko, and F. Guedry (New York: New York Academy of Sciences), 363-378.
12. Büttner-Ennever, J. A., and Gerrits, N. M. (2004). "Vestibular system," in The Human Nervous System, 2 Edn, eds G. Paxinos and J. K. Mai (London: Elsevier Academic Press), 1212-1240.
13. Cai, Y.-L., Ma, W.-L., Li, M., Guo, J.-S., Li,Y.-Q.,Wang,L.-G.,andWang,W.-Z. (2007). Glutamatergic vestibular neurons express Fos after vestibular stimulation and project to the NTS and the PBN in rats. Neurosci. Lett. 417, 132-137.
14. Cai, Y.-L., Want, J.-Q., Chen, X.-M., Li, H.-X., Li, M., and Guo, J.-S. (2010). Decreased Fos protein expression in rat caudal vestibular nucleus is associated with motion sickness habitu-ation. Neurosci. Lett. 480, 87-91.
15. Card, J. P., Sved, J. C., Craig, B., Raizada, M., Vazquez, J., and Sved, A. F. (2006). Efferent projections of rat rostroventrolateral medulla C1 catecholamine neurons: Implications for the central control of cardiovascular regulation. J. Comp. Neurol. 499, 840-859.
16. Carleton, S. C., and Carpenter, M. B. (1983). Afferent and efferent connections of the medial, inferior and lateral vestibular nuclei in the cat and monkey. Brain Res. 278, 29-51.
17. Carleton, S. C., and Carpenter, M. B. (1984). Distribution of primary vestibular fibres in the brainstem and cerebellum of the monkey. Brain Res. 294,281-298.
18. Chan, R. K., and Sawchenko, P. E. (1994). Spatially and temporally differentiated patterns of c-for expression in brainstem catecholaminergic cell groups induced by cardiovascular challenges in the rat. J. Comp. Neurol. 348,433-460.
19. Chen, L.-W., Lai, C.-H., Law, H.-Y., Yung, K. K. L., and Chan, Y.-S. (2003). Quantitative study of the coexpression of Fos and N-methyl-D aspartate (NMDA) receptor sub-units in otolith-related vestibular nuclear neurons of rats. J. Comp. Neurol. 460,292-301.
20. Cirelli, C., Pompeiano, M., D'ascanio, P., Arrighi, P., and Pompeiano, O. (1996). c-Fos expression in the rat brain after unilateral labyrintectomy and its relation to the uncompen-sated and compensated stages. Neu-roscience 70, 515-546.
21. Cohen, B., Martinelli, G. P., Ogorod-nikov, D., Xiang, Y., Raphan, T., Hol-stein, G. R., and Yakushin, S. B. (2011). Sinusoidal galvanic vestibular stimulation (sGVS) induces a vasovagal response in the rat. Exp. Brain Res. 210,45-55.
22. Courjon, J. H., Precht, W., and Sirkin, D. W. (1987). Vestibular nerve and nuclei unit responses and eye movement responses to repetitive galvanic stimulation of the labyrinth in the rat. Exp. Brain Res. 66, 41-48.
23. Cui, J., Iwase, S., Mano, T., Katayama, N., and Mori, S. (1999). Sympathetic response to horizontal linear acceleration in humans. J. Gravit. Physiol. 6, 65-66.
24. Cui, J., Mukai, C., Iwase, S., Sawasaki, N., Kitazawa, H., Mano, T., Sugiyama, Y., and Wada, Y. (1997). Response to vestibular stimulation of sympathetic outflow to muscle in humans. J. Auton. Nerv. Syst. 66, 154-162.
25. Curran, T., and Morgan, J. I. (1995). Fos: an immediate-early transcription factor in neurons. J. Neurobiol. 26,403-412.
26. Curthoys, I. S. (2010). A critical review of the neurophysiological evidence underlying clinical vestibular testing using sound, vibration and galvanic stimuli. Clin. Neurophysiol 121, 132-144.
27. Dampney, R. A. L., Polson, J. W., Potts, P. D., Hirooka, Y., and Hori-uchi, J. (2003). Functional organization of brain pathways subserving the baroreceptor reflex: studies in conscious animals using immediate early gene expression. Cell. Mol. Neurobiol. 23,597-616.
28. Darlington, C. L., Lawlor, P., Smith, P. F., and Dragunow, M. (1996). Temporal relationship between the expression of Fos, Jun and Krox-24 in the guinea pig vestibular nuclei during the development of vestibular compensation for unilateral vestibular deafferentation. Brain Res. 735, 173-176.
29. Dragunow, M., and Faull, R. (1989). The use of c-fos as a metabolic marker in neuronal pathway tracing. J. Neurosci. Methods 29, 261-265.
30. Durchdewald, M., Angel, P., and Hess, J. (2009). The transcription factor Fos: a Janus-type regulator in health and disease. Histol. Histopathol. 24, 1451-1461.
31. Epema,A. H., Gerrits,N. M.,andVoogd, J. (1988). Commissural and intrinsic connections of the vestibular nuclei in the rabbit: a retrograde labeling study. Exp. Brain Res. 71, 129-146.
32. Fuller, P. M., Jones, T. A., Jones, S. M., and Fuller, C. A. (2004). Evidence for macular gravity receptor modulation of hypothalamic, limbic and autonomic nuclei. Neuroscience 129, 461-471.
33. Gacek, R. R. (1978). Location of commissural neurons in the vestibular nuclei of the cat. Exp. Neurol. 59, 479-491.
34. Goldberg, J. M., Smith, C. E., and Fernandez, C. (1984). Relation between discharge regularity andresponses to externally applied galvanic currents in vestibular nerve afferents of the squirrel monkey. J. Neurophysiol. 51, 1236-1256.
35. Goodchild, A. K., and Moon, E. A. (2009). Maps of cardiovascular and respiratory regions of rat ventral medulla: focus on the caudal medulla. J. Chem. Neuroanat. 38, 209-221.
36. Grewal, T., James, C., and Mace-field, V. G. (2009). Frequency-dependent modulation of muscle sympathetic nerve activity by sinusoidal galvanic vestibular stimulation in human subjects. Exp. Brain Res. 197, 379-386.
37. Gustave Dit Duflo, S., Gestreau, C., and Lacour, M. (2000). Fos expression in the rat brain after exposure to gravito-inertial force changes. Brain Res. 861, 333-344.
38. Gustave Dit Duflo, S., Gestreau, C., Tighilet, B., and Lacour, M. (1999). Fos expression in the cat brainstem after unilateral vestibular neurec-tomy. Brain Res. 824, 1-17.
39. Herdegen, T., and Leah, J. D. (1998). Inducible and constitutive transcription factors in the mammalian nervous system: control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins. Brain Res. Rev. 28,370-490.
40. Highstein, S. M., and Holstein, G. R. (2006). "The anatomy of the vestibular nuclei," in Neuroanatomy of the Oculomotor System, ed. J. A. Büttner-Ennever (Amsterdam: Else-vier), 157-203.
41. Holstein, G. R. (2012). "The vestibular system," in The Human Nervous System, 3rd Edn, eds J. Mai and G. Pax-inos (London: Elsevier), 1239-1269.
42. Holstein, G. R., Friedrich, V. L. J., Kang, T., Kukielka, E., and Martinelli, G. P. (2011a). Direct projections from the caudal vestibular nuclei to the ven-trolateral medulla in the rat. Neuroscience 175, 104-117.
43. Holstein, G. R., Martinelli, G. P., and Friedrich, V. L. J. (2011b). Anatomical observations of the caudal vestibulo-sympathetic pathway. J. Vestib. Res. 21,49-62.
44. Holstein, G. R., Martinelli, G. P., and Cohen,B. (1999). The ultrastructure of GABA-immunoreactive vestibular commissural neurons related to velocity storage in the monkey. Neuroscience 93, 171-181.
45. Holstein, G. R., Martinelli, G. P., Henderson, S. C., Friedrich, V. L. J., Rabbitt, R. D., and Highstein, S. M. (2004). Gamma-aminobutyric acid is present in a spatially discrete sub-population of hair cells in the crista ampullaris of the toadfish, Opsanus tau. J. Comp. Neurol. 471, 1-10.
46. Hughes, P., and Dragunow, M. (1995). Induction of immediate-early genes and the control of neurotransmitter-regulated gene expression within the nervous system. Pharmacol. Rev. 47, 133-175.
47. Illing, R.-B., Michler, S. A., Kraus, K. S., and Laszig, R. (2002). Transcription factor modulation and expression in the rat auditory brainstem following electrical intracochlear stimulation. Exp. Neurol. 175,226-244.
48. Imholtz, B. P., Wieling, W., Lange-wouters, G. J., and Van Montfrans, G. A. (1991). Continuous finger arterial pressure: utility in the cardiovascular laboratory. Clin. Auton. Res. 1, 43-53.
49. James, C., and Macefield, V. G. (2010). Competitive interactions between vestibular and cardiac rhythms in the modulation of muscle sympathetic nerve activity. Auton. Neurosci. 158, 127-131.
50. James, C., Statis, A., and Macefield, V. G. (2010). Vestibular and pulse-related modulation of skin sympathetic nerve activity during sinusoidal galvanic vestibular stimulation in human subjects. Exp. Brain Res. 202,291-298.
51. Kaufman, G. D. (2005). Fos expression in the vestibular brainstem: what one marker can tell us about the network. Brain Res. Rev. 50, 200-211.
52. Kaufman, G. D., Anderson, J. H., and Beitz, A. J. (1991). Activation of a specific vestibulo-olivary pathway by centripetal acceleration in rat. Brain Res. 562, 311-317.
53. Kaufman, G. D., Anderson, J. H., and Beitz, A. J. (1992a). Brainstem Fos expression following acute unilateral labyrinthectomy in the rat. Neurore-port 3, 929-832.
54. Kaufman, G. D., Anderson, J. H., and Beitz, A. J. (1992b). Fos-defined activity in rat brainstem following centripetal acceleration. J. Neurosci. 12,4489-4500.
55. Kaufman, G. D., Anderson, J. H., and Beitz, A. J. (1993). Otolith-brainstem connectivity - evidence for differential neural activation by vestibular hair cells based on quantification of FOS expression in unilateral labyrinthectomized rats. J. Neurophysiol. 70,117-127.
56. Kaufman, G. D., and Perachio, A. A. (1994). Translabyrinthine electrical stimulation for the induction of immediate-early genes in the gerbil brainstem. Brain Res. 646, 345-350.
57. Kaufman, G. D., Shinder, M. E., and Perachio, A. A. (1999). Correlation of Fos expression and circling asymmetry during gerbil vestibular compensation. Brain Res. 817, 246-255.
58. Kaufmann, H., Biaggioni, I., Voustian-iouk, A., Diedrich, A., Costa, F., Clarke, R., Gizzi, M., Raphan, T., and Cohen, B. (2002). Vestibular control of sympathetic activity. An otolith-sympathetic reflex in humans. Exp. Brain Res. 143, 463-469.
59. Kevetter, G. A., and Perachio, A. A. (1986). Distribution of vestibular afferents that innervate the sacculus and posterior canal in the gerbil. J. Comp. Neurol. 254,410-424.
60. Kim, M. S., Jin, B. K., Chun, S. W., Lee, M. Y., Lee, S. H., Kim, J. H., and Park, B. R. (1997). Effect of MK801 on cFos-like protein expression in the medial vestibular nucleus at early stage of vestibular compensation in uvulonodulectomized rats. Neurosci. Lett. 231,147-150.
61. Kim, M. S., Kim, J. H., Jin, Y Z., Kry, D., and Park, B. R. (2002). Temporal changes of cFos-like protein expression in medial vestibular nuclei following arsanilate-induced unilateral labyrinthectomy in rats. Neurosci. Lett. 319,9-12.
62. Kitahara, T., Saika, T., Takeda, N., Kiyama, H., and Kubo, T. (1995). Changes in Fos and Jun expression in the rat brainstem in the process of vestibular compensation. Acta Oto-laryngol. Suppl. 520, 401-404.
63. Kitahara, T., Takeda, M., Saika, T., Kubo, T., and Kiyama, H. (1997). Role of the flocculus in the development of vestibular compensation: immunohistochemical studies with retrograde tracing and flocculec-tomy using Fos expression as a marker in the rat brainstem. Neurosci. Lett. 76, 571-580.
64. Kovács, K. J. (2008). Measurement of immediate-early gene activation-c-fos and beyond. J. Neuroendocrinol. 20,665-672.
65. Lai, C.-H., Tse, Y.-C., Shum, D. K. Y., Yung, K. K. L., and Chan, Y.-S. (2004). Fos expression in otolith-related brainstem neurons of postnatal rats following off-vertical axis rotation. J. Comp. Neurol. 470, 282-296.
66. Lai, S.-K., Lai, C.-H., Tse, Y.-C., Yung, K. K. L., Shum, D. K. Y., and Chan, Y.-S. (2008). Developmental maturation of ionotropic glutamate receptor subunits in rat vestibular nuclear neurons responsive to vertical linear acceleration. Eur. J. Neurosci. 28, 2157-2172.
67. Lai, S.-K., Lai, C.-H., Yung, K. K. L., Shum, D. K. Y., and Chan, Y.-S. (2006). Maturation of otolith-related brainstem neurons in the detection of vertical linear acceleration in rats. Eur. J. Neurosci. 23, 2431-2446.
68. Lau, L. D., Sparto, P. J., Furman, J. M., and Redfern, M. S. (2003). The steady-state postural responses to continuous sinusoidal galvanic stimulation. Gait Posture 18, 64-72.
69. Li, Y.-W., and Dampney, R. A. L. (1994). Expression of Fos-like protein in brain following sustained hypertension and hypotension in conscious rabbits. Neuroscience 61, 613-634.
70. MacDougall, H. G., Brizuela, A. E., Burgess, A. M., Curthoys, I. S., and Halmagyi, G. M. (2005). Patient and normal three-dimensional eye-movement reesponses to maintained (DC) surface galvanic vestibular stimulation. Otol Neurotol. 26, 500-511.
71. Marshburn, T. H., Kaufman, G. D., Pur-cell, I. M., and Perachio, A. A. (1997). Saccule contribution to immediate early gene induction in the gerbil brainstem with posterior canal galvanic or hypergravity stimulation. Brain Res. 761,51-58.
72. Mitsacos, A., Reisine, H., and High-stein, S. M. (1983a). The superior vestibular nucleus: an intracellular HRP study in the cat. I. Vestibulo-ocular neurons. J. Comp. Neurol. 215,78-91.
73. Mitsacos, A., Reisine, H., and Highstein, S. M. (1983b). The superior vestibular nucleus: an intracellular HRP study in the cat. II. Non-vestibulo-ocular neurons. J. Comp. Neurol. 215,92-107.
74. Morgan, J. I., and Curran, T. (1989). Stimulus-transcription coupling in neurons: role of cellular immediate-early genes. Trends Neurosci. 12, 459-462.
75. Morgan, J. I., and Curran, T. (1991). Stimulus-transcription coupling in the nervous system: involvement of the inducible proto-oncogenes fos and jun. Ann. Rev. Neurosci. 14, 421-451.
76. Morrison,S.F. (2003). Glutamate transmission in the rostral ventrolat-eral medullary sympathetic premo-tor pathway. Cell. Mol Neurobiol. 23, 761-772.
77. Newlands, S. D., Purcell, I. M., Kevet-ter, G. A., and Perachio, A. A. (2002). Central projections of the utricular nerve in the gerbil. J. Comp. Neurol. 452,11-23.
78. Newlands, S. D., Vrabec, J. T., Purcell, I. M., Stewart, C. M., Zimmerman, B. E., and Perachio, A. A. (2003). Central projections of the saccular and utricular nerves in macaques. J. Comp. Neurol. 466, 31-47.
79. Paxinos, G., Carrive, P., Wang, H., and Wang, P.-Y. (1999). Chemoarchitec-tonic Atlas of The Rat Brainstem. San Diego: Academic Press.
80. Paxinos, G., and Watson, C. (1998). The Rat Brain in Stereotaxic Coordinates. San Diego: Academic Press.
81. Peterson, B. W., Fukushima, K., Hirai, N., Schor, R. H., and Wilson, V. J. (1980). Responses of vestibulospinal and reticulospinal neurons to sinusoidal vestibular stimulation. J. Neurophysiol. 43, 1236-1250.
82. Pompeiano, O., D'ascanio, P., Centini, C., Pompeiano, M., and Balaban, E. (2002). Gene expression in rat vestibular and reticular structures during and after space flight. Neuroscience 114, 135-155.
83. Porter, J. D., and Balaban, C. D. (1997). Connections between the vestibular nuclei and regions that mediate autonomic function in the rat. J. Vestib. Res. 7, 63-76.
84. Ray, C. A., and Carter, J. R. (2003). Review: vestibular activation of sympathetic nerve activity. Acta Physiol. Scand. 177,313-319.
85. Saxon, D. W., Anderson, J. H., and Beitz, A. J. (2001). Transtympanic tetrodotoxin alters the VOR and Fos labeling in the vestibular complex. Neuroreport 12, 3051-3055.
86. Shinder, M. E., Perachio, A. A., and Kaufman, G. D. (2005a). Fos responses to short-term adaptation of the horizontal vestibuloocular reflex before and after vestibular compensation in the Mongolian gerbil. Brain Res. 1050, 79-93.
87. Shinder, M. E., Perachio, A. A., and Kaufman, G. D. (2005b). VOR and Fos response during acute vestibular compensation in the Mongolian gerbil in darkness and in light. Brain Res. 1038, 183-197.
88. Shinder, M. E., Ramanathan, M., and Kaufman, G. D. (2006). Asymmetric gene expression in the brain during acute compensation to unilateral vestibular labyrinthectomy in the Mongolian gerbil. J. Vestib. Res. 16, 147-169.
89. Stornetta, R. L. (2009). Neurochemistry of bulbospinal presympathetic neurons of the medulla oblongata. J. Chem. Neuroanat. 38, 222-230.
90. Tse, Y.-C., Lai, C.-H., Lai, S.-K., Liu, J. X., Yung, K. K., Shum, D. K., and Chan, Y.-S. (2008). Developmental expression of NMDA and AMPA receptor subunits in vestibular nuclear neurons that encode gravity-related horizontal orientations.J. Comp.Neurol. 508, 343-364.
91. Voustianiouk, A., Diedrich, A., Ogorod-nikov, D., Macdougall, H. G., Raphan, T., Biaggioni, I., Cohen, B., and Kaufmann, H. (2004). Vestibular nerve stimulation modulates muscle sympathetic nerve activity in humans. Clin. Auton. Res. 14,335.
92. Voustianiouk, A., Kaufmann, H., Diedrich, A., Raphan, T., Biaggioni, I., Macdougall, H., Ogorodnikov, D., and Cohen, B. (2006). Electrical activation of the human vestibulo-sympathetic reflex. Exp. Brain Res. 171,251-261.
93. Watson, S. R., Brizuela, A. E., Curthoys, I. S., Colebatch, J. G., Macdougall, H. G., and Halmagyi, G. M. (1998). Maintained ocular torsion produced by bilateral and unilateral galvanic (DC) vestibular stimulation in humans. Exp. Brain Res. 122, 453-458.
94. Yates, B. J., Aoki, M., Burchill, P., Bronstein, A. M., and Gresty, M. A. (1999). Cardiovascular responses elicited by linear acceleration in humans. Exp. Brain Res. 125, 476-484.
95. Yates, B. J., and Bronstein, A. M. (2005). The effects of vestibular system lesions on autonomic regulation: observations, mechanisms, and clinical implications. J. Vestib. Res. 15, 119-129.
96. Yates, B. J., Grélot, L., Kerman, I. A., Balaban, C. D., Jakus, J., and Miller, A. D. (1994). Organization of vestibular inputs to nucleus tractus soli-tarius and adjacent structures in cat brain stem. Am. J. Physiol. 267, R974-R983.
97. Yates, B. J., and Miller, A. D. (1994). Properties of sympathetic reflexes elicited by natural vestibular stimulation: implications for cardiovascular control. J. Neurophysiol. 71, 2087-2092.
98. Zhang, F. X., Lai, C. H., Tse, Y. C., Shum, D. K. Y., and Chan, Y. S. (2005). Expression of Trk receptors in otolith-related neurons in the vestibular nucleus of rats. Brain Res. 1062,92-100.