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

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

Abstract

The vestibular system sends projections to brainstem autonomic nuclei that modulate heart rate and blood pressure in response to changes in head and body position with regard to gravity. Consistent with this, binaural sinusoidally modulated galvanic vestibular stimulation (sGVS) in humans causes vasoconstriction in the legs, while low frequency (0.02-0.04 Hz) sGVS causes a rapid drop in heart rate and blood pressure in anesthetized rats. We have hypothesized that these responses occur through activation of vestibulo-sympathetic pathways. In the present study, c-Fos protein expression was examined in neurons of the vestibular nuclei and rostral ventrolateral medullary region (RVLM) that were activated by low frequency sGVS. We found c-Fos-labeled neurons in the spinal, medial, and superior vestibular nuclei (SpVN, MVN, and SVN, respectively) and the parasolitary nucleus. The highest density of c-Fos-positive vestibular nuclear neurons was observed in MVN, where immunolabeled cells were present throughout the rostro-caudal extent of the nucleus. c-Fos expression was concentrated in the parvocellular region and largely absent from magnocellular MVN. c-Fos-labeled cells were scattered throughout caudal SpVN, and the immunostained neurons in SVN were restricted to a discrete wedge-shaped area immediately lateral to the IVth ventricle. Immunofluorescence localization of c-Fos and glutamate revealed that approximately one third of the c-Fos-labeled vestibular neurons showed intense glutamate-like immunofluorescence, far in excess of the stain reflecting the metabolic pool of cytoplasmic glutamate. In the RVLM, which receives a direct projection from the vestibular nuclei and sends efferents to preganglionic sympathetic neurons in the spinal cord, we observed an approximately threefold increase in c-Fos labeling in the sGVS-activated rats. We conclude that localization of c-Fos protein following sGVS is a reliable marker for sGVS-activated neurons of the vestibulo-sympathetic pathway.

Keywords: blood pressure; heart rate; orthostatic hypotension; otolith organs; rostral ventrolateral medulla; sympathetic nervous system; vasovagal syncope; vestibular nuclei.

Figures

Figure 1
Figure 1
Changes in (A) blood pressure (BP) and (B) heart rate (HR) in response to sinusoidal galvanic vestibular stimulation (sGVS) at 0.1 Hz, 2 mA (C). BP fell from 100 to 90 mmHg and HR decreased from 5.5 to 5.1 beats/s. The calibration for BP was taken from an implanted intra-aortic sensor (red trace). Although the changes in BP from the PPG (blue trace) were uncalibrated, the waveforms obtained from PPG and intra-aortic sensors follow similar time courses. Changes in HR, which were calculated from the systolic changes in BP, were the same for the intra-aortic sensor and for PPG. See Section “Materials and Methods” for a further description of processing of the PPG. These results verify that changes in BP and HR can be detected and quantified using PPG data.
Figure 2
Figure 2
Representative vibratome sections through the vestibular nuclei from two sGVS-stimulated (A,B) and two mock (non)stimulated (C,D) rats processed for immunoperoxidase/diaminobenzidine staining of c-Fos protein. c-Fos-immunoreactive neuronal nuclei are apparent in the spinal and medial vestibular nuclei (SpVN, MVN), as well as nucleus tractus solitarius (NTS), of the stimulated animals. Sections from the mock-stimulated animals contained c-Fos-labeled cells in NTS, but rarely in the vestibular nuclei. Scale bar in (D) is for all panels.
Figure 3
Figure 3
A vibratome section through the caudal vestibular nuclei from an sGVS-stimulated rat, stained with anti-c-Fos antibody pre-incubated with a peptide blocker and then further processed for immunoperoxidase/diaminobenzidine staining. Signal was negligible in such control sections, and in those in which primary and/or secondary reagents were omitted from the processing protocol.
Figure 4
Figure 4
A schematic representation of the distribution of c-Fos-positive cells in the vestibular nuclear complex of one rat following sGVS (see Materials and Methods for details) is shown on the left side of the atlas sections (modified from Paxinos and Watson, 1998). The highest overall density of immunostained neurons was present in the medial vestibular nucleus (MVN). These cells were localized almost exclusively in the parvocellular region (MVNpc) and caudal MVN. Immunopositive neurons were present throughout the caudal half of the spinal vestibular nucleus (SpVN), and there was a small dense cluster of immunopositive neurons in the superior vestibular nucleus (SVN). Only labeling in the vestibular nuclei is plotted on this schematic. Approximate Bregma coordinates from the published atlas are indicated to the left. Abbreviations: 6, abducens nucleus; 8vn, vestibular nerve; 8n, vestibulo-cochlear nerve; das, dorsal acoustic stria; DC, dorsal cochlear nucleus; DMSp5, dorsomedial spinal trigeminal nucleus (dorsal D and ventral V subdivisions); DPGi, dorsal paragigantocellular nucleus; ECu, external cuneate nucleus; Gi, nucleus reticularis gigantocellularis; GiA, n. reticularis gigantocellularis, alpha nucleus; icp, inferior cerebellar peduncle; IRt, intermediate reticular nucleus; IS, inferior salivatory nucleus; LVe, lateral vestibular nucleus; lvs, lateral vestibulo-spinal tract; mlf, medial longitudinal fasciculus; MVeMC, medial vestibular nucleus, magnocellular division; MVePC, medial vestibular nucleus, parvocellular division; Pa6, paraabducens nucleus; PCRtA, parvicellular reticular nucleus; pd, predorsal bundle; Pr, prepositus nucleus; py, pyramids; RMg, raphé magnus; RVL, rostral ventrolateral medulla; scp, superior cerebellar peduncle; SGe, supragenual nucleus; sol, solitary tract; Sol, solitary nucleus (ventrolateral VL, rostrolateral RL, and medial M subdivisions); sp5, spinal trigeminal tract (oral O and interstitial I subdivisions); Sp5I, spinal trigeminal nucleus, pars interpolaris; SpVe, spinal (inferior) vestibular nucleus; SuVe, superior vestibular nucleus; ts, tectospinal tract; VCP, ventral cochlear nucleus, posterior division; VeCb, vestibulocerebellar nucleus; Y, Y-group.
Figure 5
Figure 5
Neurons in MVN activated by sGVS, visualized in vibratome sections processed for c-Fos immunoperoxidase/diaminobenzidine staining. The panels illustrate six rostro-caudal levels of the MVN from the same sGVS-stimulated rat. The images were obtained using the same microscopy and imaging conditions, and were subject to the same adjustments of brightness and contrast (see Materials and Methods). In all panels, the midline is to the left. A dense cluster of immunopositive cells is present in the rostral pole of MVNpc (A,B). The few activated neurons in MVNmc (A–D) are small diameter cells; none of the larger diameter neurons of this region were c-Fos-positive. c-Fos-stained cells were scattered throughout the caudal spinal vestibular nucleus (B–F). Approximate Bregma levels are indicated in the upper right of each panel. Abbreviations: MVN, medial vestibular nucleus; MVNmc, medial vestibular nucleus, magnocellular division; MVNpc, medial vestibular nucleus, parvocellular division; NTS, nucleus tractus solitarius; SpVN, spinal vestibular nucleus. Scale bar in (F) represents 100 μm, and is for all panels.
Figure 6
Figure 6
Multiple-label immunofluorescence visualization of c-Fos (green), glutamate (red), and DAPI nuclear stain (blue) in the vestibular nuclei of three different rats stimulated by sGVS. (A) A low magnification overview of rostral medial vestibular nucleus, where there is a discrete cluster of c-Fos immunopositive cells. (B) A cluster of sGVS-activated neurons in SpVN. (C) sGVS-activated neurons in the caudal MVN and SpVN and a dorsoventrally oriented column of labeled cells in the parasolitary nucleus. This panel has an irrelevant primary antibody control overlay, in order to better visualize the anatomical landmarks. Scale bars: 200 μm in (A), 50 μm in (B,C). Abbreviations: MVN, medial vestibular nucleus; MVNpc, medial vestibular nucleus, parvocellular division; NTS, nucleus tractus solitarius; SpVN, spinal vestibular nucleus; SVN, superior vestibular nucleus.
Figure 7
Figure 7
Multiple-label immunofluorescence visualization of c-Fos (green), glutamate (red), and DAPI nuclear stain (blue) in the vestibular nuclei of sGVS-stimulated rats. Three morphological types of vestibular nuclear neurons are activated by sGVS: globular (A,B), multipolar (C), and fusiform (D). The same three morphological cell types send direct projections from the vestibular nuclei to the RVLM (Holstein et al., 2011a). Approximately one third of the c-Fos-positive neurons showed intense glutamate immunofluorescence (C,D). Scale bars in all panels are 20 μm.
Figure 8
Figure 8
Multiple-label immunofluorescence visualization of c-Fos (green), glutamate (red), tyrosine hydroxylase (magenta), and DAPI nuclear stain (blue) in the RVLM of sGVS-stimulated rats. Most, but not all, of the sGVS-activated neurons in RVLM are intensely immunoreactive for tyrosine hydroxylase. The two cells indicated by white arrows in (A) are also intensely glutamate-immunofluorescent, whereas the two c-Fos-positive cells in (B) are not. Scale bars in both panels represent 20 μm.
Figure 9
Figure 9
Schematic diagram of the major cell groups mediating vestibulo-autonomic (red) and baroreflex pathways (green). Although there are vestibular projections to NTS and to CVLM, little convergence of this pathway with baroreflex signals occurs prior to processing in the RVLM. Regions receiving significant convergent baroreflex and vestibulo-sympathetic reflex inputs are indicated in yellow. See text for details. Abbreviations: CVLM, caudal ventrolateral medullary region; IML, intermediolateral cell column; NTS, solitary nucleus; RVLM, rostral ventrolateral medulla; VNC, vestibular nuclear complex.

References

    1. Abe C., Tanaka K., Awazu C., Morita H. (2008). Strong galvanic vestibular stimulation obscures arterial pressure response to gravitational change in conscious rats. J. Appl. Physiol. 104, 34–4010.1152/japplphysiol.00454.2007
    1. Abe C., Tanaka K., Awazu C., Morita H. (2009). Galvanic vestibular stimulation counteracts hypergravity-induced plastic alteration of vestibulo-cardiovascular reflex in rats. J. Appl. Physiol. 107, 1089–109410.1152/japplphysiol.00400.2009
    1. Armstrong D. M., Ross C. A., Pickel V. M., Joh T. H., Reis D. J. (1982). Distribution of dopamine-, noradrenaline-, and adrenaline-containing cell bodies in the rat medulla oblongata: Demonstration by the immunocytochemical localization of catecholamine biosynthetic enzymes. J. Comp. Neurol. 212, 173–18710.1002/cne.902120207
    1. Baizer J. S., Corwin W. L., Baker J. F. (2010). Otolith stimulation induces c-Fos expression in vestibular and precerebellar nuclei in cats and squirrel monkeys. Brain Res. 1351, 64–7310.1016/j.brainres.2010.05.087
    1. Balaban C. D., 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, 200–21210.1007/BF00228409
    1. Balaban C. D., Yates B. J. (2004). “Vestibulo-autonomic interactions: a teleological perspective,” in The Vestibular System, eds Highstein S. H., Fay R. R., Popper A. N. (Wein: Springer; ), 286–342
    1. Barmack N. H. (2003). Central vestibular system: vestibular nuclei and posterior cerebellum. Brain Res. Bull. 60, 511–54110.1016/S0361-9230(03)00055-8
    1. Bent L. R., Bolton P. S., Macefield V. G. (2006). Modulation of muscle sympathetic bursts by sinusoidal galvanic vestibular stimulation in human subjects. Exp. Brain Res. 174, 701–71110.1007/s00221-006-0515-6
    1. Bourassa E. A., Sved A. F., Speth R. C. (2009). Angiotensin modulation of rostral ventrolateral medulla (RVLM) in cardiovascular regulation. Mol. Cell. Endocrinol. 302, 167–17510.1016/j.mce.2008.10.039
    1. Bradbury S., Eggleston C. (1925). Postural hypotension. A report of three cases. Am. Heart J. 1, 73–8610.1016/S0002-8703(25)90007-5
    1. Büttner-Ennever J. A. (1992). “Patterns of connectivity in the vestibular nuclei,” in Sensing and Controlling Motion: Vestibular and Sensorimotor Function, eds Cohen B., Tomko D., Guedry F. (New York: New York Academy of Sciences; ), 363–378
    1. Büttner-Ennever J. A., Gerrits N. M. (2004). “Vestibular system,” in The Human Nervous System, 2 Edn, eds Paxinos G., Mai J. K. (London: Elsevier Academic Press; ), 1212–1240
    1. Cai Y.-L., Ma W.-L., Li M., Guo J.-S., Li Y.-Q., Wang L.-G., Wang W.-Z. (2007). Glutamatergic vestibular neurons express Fos after vestibular stimulation and project to the NTS and the PBN in rats. Neurosci. Lett. 417, 132–13710.1016/j.neulet.2007.01.079
    1. Cai Y.-L., Want J.-Q., Chen X.-M., Li H.-X., Li M., Guo J.-S. (2010). Decreased Fos protein expression in rat caudal vestibular nucleus is associated with motion sickness habituation. Neurosci. Lett. 480, 87–9110.1016/j.neulet.2010.06.011
    1. Card J. P., Sved J. C., Craig B., Raizada M., Vazquez J., 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, 840–85910.1002/cne.21140
    1. Carleton S. C., Carpenter M. B. (1983). Afferent and efferent connections of the medial, inferior and lateral vestibular nuclei in the cat and monkey. Brain Res. 278, 29–5110.1016/0006-8993(83)90223-8
    1. Carleton S. C., Carpenter M. B. (1984). Distribution of primary vestibular fibres in the brainstem and cerebellum of the monkey. Brain Res. 294, 281–29810.1016/0006-8993(84)91040-0
    1. Chan R. K., 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, 433–46010.1002/cne.903480309
    1. Chen L.-W., Lai C.-H., Law H.-Y., Yung K. K. L., Chan Y.-S. (2003). Quantitative study of the coexpression of Fos and N-methyl-D aspartate (NMDA) receptor subunits in otolith-related vestibular nuclear neurons of rats. J. Comp. Neurol. 460, 292–30110.1002/cne.10657
    1. Cirelli C., Pompeiano M., D’ascanio P., Arrighi P., Pompeiano O. (1996). c-Fos expression in the rat brain after unilateral labyrintectomy and its relation to the uncompensated and compensated stages. Neuroscience 70, 515–54610.1016/0306-4522(95)00369-X
    1. Cohen B., Martinelli G. P., Ogorodnikov D., Xiang Y., Raphan T., Holstein G. R., Yakushin S. B. (2011). Sinusoidal galvanic vestibular stimulation (sGVS) induces a vasovagal response in the rat. Exp. Brain Res. 210, 45–5510.1007/s00221-011-2604-4
    1. Courjon J. H., Precht W., 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, 41–4810.1007/BF00236200
    1. Cui J., Iwase S., Mano T., Katayama N., Mori S. (1999). Sympathetic response to horizontal linear acceleration in humans. J. Gravit. Physiol. 6, 65–66
    1. Cui J., Mukai C., Iwase S., Sawasaki N., Kitazawa H., Mano T., Sugiyama Y., Wada Y. (1997). Response to vestibular stimulation of sympathetic outflow to muscle in humans. J. Auton. Nerv. Syst. 66, 154–16210.1016/S0165-1838(97)00077-5
    1. Curran T., Morgan J. I. (1995). Fos: an immediate-early transcription factor in neurons. J. Neurobiol. 26, 403–41210.1002/neu.480260312
    1. Curthoys I. S. (2010). A critical review of the neurophysiological evidence underlying clinical vestibular testing using sound, vibration and galvanic stimuli. Clin. Neurophysiol 121, 132–14410.1016/j.clinph.2009.09.027
    1. Dampney R. A. L., Polson J. W., Potts P. D., Hirooka Y., Horiuchi J. (2003). Functional organization of brain pathways subserving the baroreceptor reflex: studies in conscious animals using immediate early gene expression. Cell. Mol. Neurobiol. 23, 597–61610.1023/A:1025080314925
    1. Darlington C. L., Lawlor P., Smith P. F., 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, 173–17610.1016/0006-8993(96)00889-X
    1. Dragunow M., Faull R. (1989). The use of c-fos as a metabolic marker in neuronal pathway tracing. J. Neurosci. Methods 29, 261–26510.1016/0165-0270(89)90150-7
    1. Durchdewald M., Angel P., Hess J. (2009). The transcription factor Fos: a Janus-type regulator in health and disease. Histol. Histopathol. 24, 1451–1461
    1. Epema A. H., Gerrits N. M., Voogd J. (1988). Commissural and intrinsic connections of the vestibular nuclei in the rabbit: a retrograde labeling study. Exp. Brain Res. 71, 129–14610.1007/BF00247528
    1. Fuller P. M., Jones T. A., Jones S. M., Fuller C. A. (2004). Evidence for macular gravity receptor modulation of hypothalamic, limbic and autonomic nuclei. Neuroscience 129, 461–47110.1016/j.neuroscience.2004.05.059
    1. Gacek R. R. (1978). Location of commissural neurons in the vestibular nuclei of the cat. Exp. Neurol. 59, 479–49110.1016/0014-4886(78)90239-X
    1. Goldberg J. M., Smith C. E., Fernandez C. (1984). Relation between discharge regularity and responses to externally applied galvanic currents in vestibular nerve afferents of the squirrel monkey. J. Neurophysiol. 51, 1236–1256
    1. Goodchild A. K., Moon E. A. (2009). Maps of cardiovascular and respiratory regions of rat ventral medulla: focus on the caudal medulla. J. Chem. Neuroanat. 38, 209–22110.1016/j.jchemneu.2009.06.002
    1. Grewal T., James C., Macefield V. G. (2009). Frequency-dependent modulation of muscle sympathetic nerve activity by sinusoidal galvanic vestibular stimulation in human subjects. Exp. Brain Res. 197, 379–38610.1007/s00221-009-1926-y
    1. Gustave Dit Duflo S., Gestreau C., Lacour M. (2000). Fos expression in the rat brain after exposure to gravito-inertial force changes. Brain Res. 861, 333–34410.1016/S0006-8993(00)02044-8
    1. Gustave Dit Duflo S., Gestreau C., Tighilet B., Lacour M. (1999). Fos expression in the cat brainstem after unilateral vestibular neurectomy. Brain Res. 824, 1–1710.1016/S0006-8993(99)01172-5
    1. Herdegen T., 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, 370–49010.1016/S0165-0173(98)00018-6
    1. Highstein S. M., Holstein G. R. (2006). “The anatomy of the vestibular nuclei,” in Neuroanatomy of the Oculomotor System, ed. Büttner-Ennever J. A. (Amsterdam: Elsevier; ), 157–203
    1. Holstein G. R. (2012). “The vestibular system,” in The Human Nervous System, 3rd Edn, eds Mai J., Paxinos G. (London: Elsevier; ), 1239–1269
    1. Holstein G. R., Friedrich V. L. J., Kang T., Kukielka E., Martinelli G. P. (2011a). Direct projections from the caudal vestibular nuclei to the ventrolateral medulla in the rat. Neuroscience 175, 104–11710.1016/j.neuroscience.2010.12.011
    1. Holstein G. R., Martinelli G. P., Friedrich V. L. J. (2011b). Anatomical observations of the caudal vestibulo-sympathetic pathway. J. Vestib. Res. 21, 49–62
    1. Holstein G. R., Martinelli G. P., Cohen B. (1999). The ultrastructure of GABA-immunoreactive vestibular commissural neurons related to velocity storage in the monkey. Neuroscience 93, 171–18110.1016/S0306-4522(99)00142-6
    1. Holstein G. R., Martinelli G. P., Henderson S. C., Friedrich V. L. J., Rabbitt R. D., Highstein S. M. (2004). Gamma-aminobutyric acid is present in a spatially discrete subpopulation of hair cells in the crista ampullaris of the toadfish, Opsanus tau. J. Comp. Neurol. 471, 1–1010.1002/cne.11025
    1. Hughes P., 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
    1. Illing R.-B., Michler S. A., Kraus K. S., Laszig R. (2002). Transcription factor modulation and expression in the rat auditory brainstem following electrical intracochlear stimulation. Exp. Neurol. 175, 226–24410.1006/exnr.2002.7895
    1. Imholtz B. P., Wieling W., Langewouters G. J., Van Montfrans G. A. (1991). Continuous finger arterial pressure: utility in the cardiovascular laboratory. Clin. Auton. Res. 1, 43–5310.1007/BF01826057
    1. James C., Macefield V. G. (2010). Competitive interactions between vestibular and cardiac rhythms in the modulation of muscle sympathetic nerve activity. Auton. Neurosci. 158, 127–13110.1016/j.autneu.2010.07.005
    1. James C., Statis A., 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, 291–29810.1007/s00221-009-2131-8
    1. Kaufman G. D. (2005). Fos expression in the vestibular brainstem: what one marker can tell us about the network. Brain Res. Rev. 50, 200–21110.1016/j.brainresrev.2005.06.001
    1. Kaufman G. D., Anderson J. H., Beitz A. J. (1991). Activation of a specific vestibulo-olivary pathway by centripetal acceleration in rat. Brain Res. 562, 311–31710.1016/0006-8993(91)90637-B
    1. Kaufman G. D., Anderson J. H., Beitz A. J. (1992a). Brainstem Fos expression following acute unilateral labyrinthectomy in the rat. Neuroreport 3, 929–83210.1097/00001756-199208000-00011
    1. Kaufman G. D., Anderson J. H., Beitz A. J. (1992b). Fos-defined activity in rat brainstem following centripetal acceleration. J. Neurosci. 12, 4489–4500
    1. Kaufman G. D., Anderson J. H., 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
    1. Kaufman G. D., Perachio A. A. (1994). Translabyrinthine electrical stimulation for the induction of immediate-early genes in the gerbil brainstem. Brain Res. 646, 345–35010.1016/0006-8993(94)90104-X
    1. Kaufman G. D., Shinder M. E., Perachio A. A. (1999). Correlation of Fos expression and circling asymmetry during gerbil vestibular compensation. Brain Res. 817, 246–25510.1016/S0006-8993(98)01284-0
    1. Kaufmann H., Biaggioni I., Voustianiouk A., Diedrich A., Costa F., Clarke R., Gizzi M., Raphan T., Cohen B. (2002). Vestibular control of sympathetic activity. An otolith-sympathetic reflex in humans. Exp. Brain Res. 143, 463–46910.1007/s00221-002-1002-3
    1. Kevetter G. A., Perachio A. A. (1986). Distribution of vestibular afferents that innervate the sacculus and posterior canal in the gerbil. J. Comp. Neurol. 254, 410–42410.1002/cne.902540312
    1. Kim M. S., Jin B. K., Chun S. W., Lee M. Y., Lee S. H., Kim J. H., 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, 147–15010.1016/S0304-3940(97)00550-8
    1. Kim M. S., Kim J. H., Jin Y. Z., Kry D., 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, 9–1210.1016/S0304-3940(01)02422-3
    1. Kitahara T., Saika T., Takeda N., Kiyama H., Kubo T. (1995). Changes in Fos and Jun expression in the rat brainstem in the process of vestibular compensation. Acta Otolaryngol. Suppl. 520, 401–40410.3109/00016489509125282
    1. Kitahara T., Takeda M., Saika T., Kubo T., Kiyama H. (1997). 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. Lett. 76, 571–580
    1. Kovács K. J. (2008). Measurement of immediate-early gene activation-c-fos and beyond. J. Neuroendocrinol. 20, 665–67210.1111/j.1365-2826.2008.01734.x
    1. Lai C.-H., Tse Y.-C., Shum D. K. Y., Yung K. K. L., Chan Y.-S. (2004). Fos expression in otolith-related brainstem neurons of postnatal rats following off-vertical axis rotation. J. Comp. Neurol. 470, 282–29610.1002/cne.11048
    1. Lai S.-K., Lai C.-H., Tse Y.-C., Yung K. K. L., Shum D. K. Y., 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, 2157–217210.1111/j.1460-9568.2008.06523.x
    1. Lai S.-K., Lai C.-H., Yung K. K. L., Shum D. K. Y., Chan Y.-S. (2006). Maturation of otolith-related brainstem neurons in the detection of vertical linear acceleration in rats. Eur. J. Neurosci. 23, 2431–244610.1111/j.1460-9568.2006.04762.x
    1. Lau L. D., Sparto P. J., Furman J. M., Redfern M. S. (2003). The steady-state postural responses to continuous sinusoidal galvanic stimulation. Gait Posture 18, 64–7210.1016/S0966-6362(02)00195-9
    1. Li Y.-W., Dampney R. A. L. (1994). Expression of Fos-like protein in brain following sustained hypertension and hypotension in conscious rabbits. Neuroscience 61, 613–63410.1016/0306-4522(94)90066-3
    1. MacDougall H. G., Brizuela A. E., Burgess A. M., Curthoys I. S., Halmagyi G. M. (2005). Patient and normal three-dimensional eye-movement reesponses to maintained (DC) surface galvanic vestibular stimulation. Otol. Neurotol. 26, 500–51110.1097/01.mao.0000169766.08421.ef
    1. Marshburn T. H., Kaufman G. D., Purcell I. M., 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, 51–5810.1016/S0006-8993(97)00030-9
    1. Mitsacos A., Reisine H., Highstein S. M. (1983a). The superior vestibular nucleus: an intracellular HRP study in the cat. I. Vestibulo-ocular neurons. J. Comp. Neurol. 215, 78–9110.1002/cne.902150108
    1. Mitsacos A., Reisine H., Highstein S. M. (1983b). The superior vestibular nucleus: an intracellular HRP study in the cat. II. Non-vestibulo-ocular neurons. J. Comp. Neurol. 215, 92–10710.1002/cne.902150108
    1. Morgan J. I., Curran T. (1989). Stimulus-transcription coupling in neurons: role of cellular immediate-early genes. Trends Neurosci. 12, 459–46210.1016/0166-2236(89)90096-9
    1. Morgan J. I., Curran T. (1991). Stimulus-transcription coupling in the nervous system: involvement of the inducible proto-oncogenes fos and jun. Ann. Rev. Neurosci. 14, 421–45110.1146/annurev.ne.14.030191.002225
    1. Morrison S. F. (2003). Glutamate transmission in the rostral ventrolateral medullary sympathetic premotor pathway. Cell. Mol. Neurobiol. 23, 761–77210.1023/A:1025005020376
    1. Newlands S. D., Purcell I. M., Kevetter G. A., Perachio A. A. (2002). Central projections of the utricular nerve in the gerbil. J. Comp. Neurol. 452, 11–2310.1002/cne.10350
    1. Newlands S. D., Vrabec J. T., Purcell I. M., Stewart C. M., Zimmerman B. E., Perachio A. A. (2003). Central projections of the saccular and utricular nerves in macaques. J. Comp. Neurol. 466, 31–4710.1002/cne.10876
    1. Paxinos G., Carrive P., Wang H., Wang P.-Y. (1999). Chemoarchitectonic Atlas of The Rat Brainstem. San Diego: Academic Press
    1. Paxinos G., Watson C. (1998). The Rat Brain in Stereotaxic Coordinates. San Diego: Academic Press
    1. Peterson B. W., Fukushima K., Hirai N., Schor R. H., Wilson V. J. (1980). Responses of vestibulospinal and reticulospinal neurons to sinusoidal vestibular stimulation. J. Neurophysiol. 43, 1236–1250
    1. Pompeiano O., D’ascanio P., Centini C., Pompeiano M., Balaban E. (2002). Gene expression in rat vestibular and reticular structures during and after space flight. Neuroscience 114, 135–15510.1016/S0306-4522(02)00202-6
    1. Porter J. D., Balaban C. D. (1997). Connections between the vestibular nuclei and regions that mediate autonomic function in the rat. J. Vestib. Res. 7, 63–7610.1016/S0957-4271(96)00138-3
    1. Ray C. A., Carter J. R. (2003). Review: vestibular activation of sympathetic nerve activity. Acta Physiol. Scand. 177, 313–31910.1046/j.1365-201X.2003.01084.x
    1. Saxon D. W., Anderson J. H., Beitz A. J. (2001). Transtympanic tetrodotoxin alters the VOR and Fos labeling in the vestibular complex. Neuroreport 12, 3051–305510.1097/00001756-200110080-00014
    1. Shinder M. E., Perachio A. A., 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, 79–9310.1016/j.brainres.2005.05.029
    1. Shinder M. E., Perachio A. A., Kaufman G. D. (2005b). VOR and Fos response during acute vestibular compensation in the Mongolian gerbil in darkness and in light. Brain Res. 1038, 183–19710.1016/j.brainres.2005.01.043
    1. Shinder M. E., Ramanathan M., 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
    1. Stornetta R. L. (2009). Neurochemistry of bulbospinal presympathetic neurons of the medulla oblongata. J. Chem. Neuroanat. 38, 222–23010.1016/j.jchemneu.2009.07.005
    1. Tse Y.-C., Lai C.-H., Lai S.-K., Liu J. X., Yung K. K., Shum D. K., 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, 343–36410.1002/cne.21688
    1. Voustianiouk A., Diedrich A., Ogorodnikov D., Macdougall H. G., Raphan T., Biaggioni I., Cohen B., Kaufmann H. (2004). Vestibular nerve stimulation modulates muscle sympathetic nerve activity in humans. Clin. Auton. Res. 14, 335
    1. Voustianiouk A., Kaufmann H., Diedrich A., Raphan T., Biaggioni I., Macdougall H., Ogorodnikov D., Cohen B. (2006). Electrical activation of the human vestibulo-sympathetic reflex. Exp. Brain Res. 171, 251–26110.1007/s00221-005-0266-9
    1. Watson S. R., Brizuela A. E., Curthoys I. S., Colebatch J. G., Macdougall H. G., Halmagyi G. M. (1998). Maintained ocular torsion produced by bilateral and unilateral galvanic (DC) vestibular stimulation in humans. Exp. Brain Res. 122, 453–45810.1007/s002210050533
    1. Yates B. J., Aoki M., Burchill P., Bronstein A. M., Gresty M. A. (1999). Cardiovascular responses elicited by linear acceleration in humans. Exp. Brain Res. 125, 476–48410.1007/s002210050705
    1. Yates B. J., Bronstein A. M. (2005). The effects of vestibular system lesions on autonomic regulation: observations, mechanisms, and clinical implications. J. Vestib. Res. 15, 119–129
    1. Yates B. J., Grélot L., Kerman I. A., Balaban C. D., Jakus J., Miller A. D. (1994). Organization of vestibular inputs to nucleus tractus solitarius and adjacent structures in cat brain stem. Am. J. Physiol. 267, R974–R983
    1. Yates B. J., Miller A. D. (1994). Properties of sympathetic reflexes elicited by natural vestibular stimulation: implications for cardiovascular control. J. Neurophysiol. 71, 2087–2092
    1. Zhang F. X., Lai C. H., Tse Y. C., Shum D. K. Y., Chan Y. S. (2005). Expression of Trk receptors in otolith-related neurons in the vestibular nucleus of rats. Brain Res. 1062, 92–10010.1016/j.brainres.2005.09.025

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