Fos Expression in Otolith-Related Brainstem Neurons of Postnatal Rats following off-Vertical Axis Rotation

Journal of Comparative Neurology

Volumn 470, Issue 3, 2004, Pages 282-296

  Lai, Chun Hong ^a   Tse, Yiu Chung ^a   Shum, Daisy K Y ^a   Yung, Ken K L ^b   Chan, Ying Shing ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b HONG KONG BAPTIST UNIVERSITY   (Hong Kong)

Author keywords

Brainstem nuclei; C fos; Development; Immunohistochemistry; Utricle; Vestibular nuclei

Indexed keywords

PROTEIN FOS;

ANIMAL EXPERIMENT; ARTICLE; BRAIN STEM; CONTROLLED STUDY; FEMALE; GIGANTOCELLULAR RETICULAR NUCLEUS; GRAVITY; HAIR CELL; HEAD MOVEMENT; HYPOGLOSSAL NUCLEUS; MALE; NONHUMAN; OTOLITH; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; ROTATION; SENSORIMOTOR FUNCTION; VESTIBULAR NUCLEUS;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BRAIN STEM; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; NEURONS; OTOLITHIC MEMBRANE; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY; ROTATION;

EID: 0742270444     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.11048     Document Type: Article

References (99)

1. Abercrombie M. 1946. Estimation of nuclear population from microtome sections. Anat Rec 94:239-247.
2. Altman J, Bayer SA. 1980. Development of the brain stem in the rat. III. Thymidine-radiographic study of the time of origin of neurons of the vestibular and auditory nuclei of the upper medulla. J Comp Neurol 194:877-904.
3. Angelaki DE. 1992. Detection of rotating gravity signals. Biol Cybern 67:523-533.
4. Angelaki DE, Hess BJM. 1996. Three-diensional organization of otolith-ocular reflexes in rhesus monkeys. II. Inertial detection of angular velocity. J Neurophysiol 75:2425-2440.
5. Angelaki DE, Bush GA, Perachio AA. 1993. Two-dimensional spatiotemporal coding of linear acceleration in vestibular nuclei neurons. J Neurosci 13:1403-1417.
6. Angelaki DE, McHenry MQ, Dickman JD, Hess BJ. 1999. Computation of inertial motion: neural strategies to resolve ambiguous otolith information. J Neurosci 19:316-327.
7. Baloh RW, Halmagyi GM. 1996. Disorders of the vestibular system. New York: Oxford.
8. Barmack NH. 1996. GABAergic pathways convey vestibular information to the beta nucleus and dorsomedial cell column of the inferior olive. Ann N Y Acad Sci 781:541-552.
9. 2-induced c-fos expression in medullary neurons during early development. Respir Physiol 117:13-28.
10. Bentivoglio M, Macchi G, Rossini P, Tempesta E. 1978. Brain stem neurons projecting to neocortex: a HRP study in the cat. Exp Brain Res 31:489-498.
11. Bolton PS, Goto T, Schor RH, Wilson VJ, Yamagata Y, Yates BJ. 1992. Response of pontomedullary reticulospinal neurons to vestibular stimuli in vertical planes. Role in vertical vestibulospinal reflexes of the decerebrate cat. J Neurophysiol 67:639-647.
12. Bush GA, Perachio AA, Angelaki DE. 1993. Encoding of head acceleration in vestibular neurons. I. Spatiotemporal response properties to linear acceleration. J Neurophysiol 69:2039-2055.
13. Buttner-Ennever JA. 1999. A review of otolith pathways to brainstem and cerebellum. Ann N Y Acad Sci 871:51-64.
14. Cannon SC, Robinson DA. 1987. Loss of the neural integrator of the oculomotor system from brain stem lesions in monkey. J Neurophysiol 57:1383-1409.
15. Chan RK, Sawchenko PE. 1994. Spatially and temporally differentiated patterns of c-fos expression in brain stem catecholaminergic cell groups induced by cardiovascular challenges in the rat. J Comp Neurol 348:433-460.
16. Chan YS. 1997. The coding of head orientations in neurons of bilateral vestibular nuclei of cats after unilateral labyrinthectomy: response to off-vertical axis rotation. Exp Brain Res 114:293-303.
17. Chan YS, Hwang JC, Cheung YM. 1979. Vestibular function of saccule in cats as indicated by the response of Deiters' nucleus to static tilts. Exp Brain Res 35:591-594.
18. Chan YS, Cheung YM, Hwang JC. 1985. Effect of tilt on the response of neuronal activity within the cat vestibular nuclei during slow and constant velocity rotation. Brain Res 345:271-278.
19. Chan YS, Chen CW, Lai CH. 1996. Response of medial medullary reticular neurons to otolith stimulation during bidirectional off-vertical axis rotation of the cat. Brain Res 732:159-168.
20. Chan YS, Shum DK, Lai CH. 1999. Neuronal response sensitivity to bidirectional off-vertical axis rotations: a dimension of imbalance in the lateral vestibular nuclei of cats after unilateral labyrinthectomy. Neuroscience 94:831-843.
21. Chan YS, Lai CH, Shum DK. 2002. Bilateral otolith contribution to spatial coding in the vestibular system. J Biomed Sci 9:574-586.
22. Chan YS, Chen CW, Lai CH, Shum DK, Yung KK, Zhang FX. 2003a. Receptors of glutamate and neurotrophin in vestibule neuronal functions. J Biomed Sci 10:577-587.
23. Chan YS, Lai CH, Shum DK. 2003b. Response properties of Y group neurons to crossed otolith inputs in the cat. Neuroreport 14:729-733.
24. Chen LW, Yung KK, Chan YS. 2000. Co-localization of NMDA receptors and AMPA receptors in the neurons of vestibular nuclei of rats. Brain Res 884:87-97.
25. Chen LW, Lai CH, Law HY, Yung KK, Chan YS. 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 460:292-301.
26. Chen X, Herbert J. 1995. Regional changes in c-fos expression in the basal forebrain and brainstem during adaptation to repeated stress: correlations with cardiovascular, hypothermic and endocrine responses. Neuroscience 64:675-685.
27. Cheron G, Godaux E, Laune JM, Vanderkelen B. 1988. Lesions in the cat prepositus complex: effects on the vestibulo-ocular reflex and saccades. J Physiol 372:75-94.
28. Cirelli C, Pompeiano M, D'Ascanio P, Arrighi P, Pompeiano O. 1996. c-fos Expression in the rat brain after unilateral labyrinthectomy and its relation to the uncompensated and compensated stages. Neuroscience 70:515-546.
29. Clarac F, Vinay L, Cazalets JR, Fady JC, Jamon M. 1998. Role of gravity in the development of posture and locomotion in the neonatal rat. Brain Res Rev 28:35-43.
30. Coggeshall RE, Lekan HA. 1996. Methods for determining numbers of cells or synapses: a case for more uniform standards of review. J Comp Neurol 364:6-15.
31. Cohen B, Suzuki JI, Raphan T. 1983. Role of the otolith organs in generation of horizontal nystagmus: effects of selective labyrinthine lesions. Brain Res 276:159-164.
32. Cole AJ, Saffen DW, Baraban JM, Worley PF. 1989. Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature 340:474-476.
33. Cullinan WE, Herman JP, Battaglia DF, Akil H, Watson SJ. 1995. Pattern and time course of immediate early gene expression in rat brain following acute stress. Neuroscience 64:477-505.
34. Curthoys IS. 1979. The development of function of horizontal semicircular canal primary neurons in the rat. Brain Res 167:41-52.
35. Darlington CL, Lawlor P, Smith PF, 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.
36. de Waele C, Muhlethaler M, Vidal PP. 1995. Neurochemistry of the central vestibular pathways. Brain Res Rev 20:24-46.
37. Dechesne CJ, Mbiene P, Sans A. 1986. Postnatal development of vestibular receptor surfaces in the rat. Acta Otolaryngol 101:11-18.
38. Dent GW, Smith MA, Levine S. 2001. Stress-induced alterations in locus coeruleus gene expression during ontogeny. Brain Res Dev Brain Res 127:23-30.
39. Endo K, Thomson DB, Wilson VJ, Yamaguchi T, Yates BJ. 1995. Vertical vestibular input to and projections from the caudal parts of the vestibular nuclei of the decerebrate cat. J Neurophysiol 74:428-436.
40. Fagerson MH, Barmack NH. 1995. Responses to vertical vestibular stimulation of neurons in the nucleus reticularis gigantocellularis in rabbits. J Neurophysiol 73:2378-2391.
41. Fernandez C, Goldberg JM. 1976. Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. II. Directional selectivity and force response relations. J Neurophysiol 39:996-1008.
42. Furman JM, Schor RH, Kamerer DB. 1993. Off-vertical axis rotational responses in patients with unilateral peripheral vestibular lesions. Ann Otol Rhinol Laryngol 102:137-143.
43. Gacek RR. 1969. The course and central termination of first order neurons supplying vestibular end organs in the cat. Acta Otolaryngol Suppl 254:1-66.
44. Graybiel AM, Moratalla R, Robertson HA. 1990. Amphetamine and cocaine induce drug-specific activation of the c-fos gene in strisome-matrix compartments and limbic subdivisions of the striatum. Proc Natl Acad Sci USA 87:6912-6916.
45. Gubits RM, Smith TM, Farihurst JL, Yu H. 1989. Adrenergic receptors mediate changes in c-fos mRNA levels in the brain. Brain Res Mol Brain Res 6:39-45.
46. Gustave Dit Duflo S, Gestreau C, Tighilet B, Lacour M. 1999. Fos expression in the cat brainstem after unilateral vestibular neurectomy. Brain Res 824:1-17.
47. Heinsen H. 1978. Postnatal quantitative changes in the cerebellar uvula of albino rats. Anat Embryol 154:285-304.
48. Herrera DG, Robertson HA. 1990. N-methyl-D-aspartate receptors mediate activation of the c-fos proto-oncogene in a model of brain injury. Neuroscience 35:273-281.
49. Hess BJM, Dieringer N. 1990. Spatial organization of the maculo-ocular reflex of the rat: responses during off-vertical axis rotation. Eur J Neurosci 2:909-919.
50. Horii A, Takeda N, Morita M, Kubo T, Matsunaga T. 1993. Motion sickness induced by sinusoidal linear acceleration in rats. Acta Otolaryngol Suppl 501:31-33.
51. Horn EM, Kramer JM, Waldrop TG. 2000. Development of hypoxia-induced Fos expression in rat caudal hypothalamic neurons. Neuroscience 99:711-720.
52. Houser GR, Barber RP, Vaughn JE. 1984. Immunocytochemical localization of glutamic acid decarboxylase in the dorsal lateral vestibule nucleus: evidence for an intrinsic and extrinsic GABAergic innervation. Neurosci Lett 47:213-220.
53. Imagawa M, Isu N, Sasaki M, Endo K, Ikegami H, Uchino Y. 1995. Axonal projections of utricular afferents to the vestibular nuclei and the abducens nucleus in cats. Neurosci Lett 186:87-90.
54. Janusonis S, Fite K. 2001. Diurnal variation of c-fos expression in subdivisions of the dorsal raphe nucleus of the Mongolian gerbil (Meriones unguiculatus). J Comp Neurol 440:31-42.
55. Karhunen E. 1973. Postnatal development of the lateral vestibular nucleus (Deiter's nucleus) of the rat. Acta Otolaryngol Suppl 313:1-87.
56. 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.
57. Kaufman GD, Anderson JH, Beitz AJ. 1992a. Brain stem Fos expression following unilateral labyrinthectomy in the rat. Neuroreport 3:829-832.
58. Kaufman GD, Anderson JH, Beitz AJ. 1992b. Fos-defined activity in rat brainstem following centripetal acceleration. J Neurosci 12:4489-4500.
59. Kaufman GD, Anderson JH, Beitz AJ. 1993. Otolith-brain stem 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.
60. Kaufman GD, Shinder ME, Perachio AA. 1999. Correlation of Fos expression and circling asymmetry during gerbil vestibular compensation. Brain Res 817:246-255.
61. Lacour M, Gustave Dit Duflo S, Gestreau C. 2000. Fos expression in the rat brain after exposure to gravito-inertial force changes. Brain Res 861:333-344.
62. Lai CH, Chan YS. 1995. Properties of otolith-related vestibular nuclear neurons in response to bidirectional off-vertical axis rotation of the rat. Brain Res 693:39-50.
63. Lai CH, Chan YS. 1996. Spontaneous activity of otolith-related vestibular nuclear neurons in the decrerebrate rat. Brain Res 739:322-329.
64. Lai CH, Chan YS. 2001. Spontaneous discharge and response characteristics of central otolith neurons of rats during postnatal development. Neuroscience 103:275-288.
65. Lai CH, Chan YS. 2002. Development of the vestibular system. Neuroembryology 1:61-71.
66. Lannou J, Precht W, Cazin C. 1979. The postnatal development of functional properties of central vestibular neurons in the rat. Brain Res 7:219-232.
67. Laouris Y, Kalli-Laouri J, Schwartze P. 1990. The postnatal development of the air-righting reaction in albino rats. Quantitative analysis of normal development and the effect of preventing neck-torso-pelvis rotations. Behav Brain Res 37:37-44.
68. Leong SK, Shieh JY, Wong WC. 1984. Localizing spinal cord-projecting neurons in adult albino rats. J Comp Neurol 228:1-17.
69. Lerea LS, Butler LS, McNamara JO. 1992. NMDA and non-NMDA receptor-mediated increase of c-fos mRNA in dentate gyrus neurons involves calcium influx via different routes. J Neurosci 12:2973-2981.
70. Lysakowski A. 1999. Development of synaptic innervation in the rodent utricle. Ann N Y Acad Sci 871:422-425.
71. Manzoni D, Andre P, Pompeiano O. 1995. Responses of purkinje cells in the cerebellar anterior vermis to off-vertical axis rotation. Pfluegers Arch 431:141-154.
72. Mariani J, Changeux JP. 1981. Ontogenesis of olivocerebellar relationships. I. Studies by intracellular recordings of the multiple innervation of Purkinje cells by climbing fibers in the developing rat cerebellum. J Neurosci 1:696-702.
73. Marshburn TH, Kaufman GD, Purcell IM, Perachio AA. 1997. Saccule contribution to immediate early gene induction in the gerbil brainstem with posterior canal galvanic or hypergravity stimulation. J Comp Neurol 377:509-519.
74. Mason CA, Christakos S, Catalano SM. 1990. Early climbing fiber interactions with Purkinje cells in the postnatal mouse cerebellum. J Comp Neurol 297:77-90.
75. Mayne R. 1974. A systems concept of the vestibular organs. In: Kornhuber HH, editor. Handbook of sensory physiology, vol 6/2. New York: Springer. p 439-580.
76. Moratalla R, Elibol B, Vallejo M, Graybiel AM. 1996. Network-level changes in expression of inducible Fos-Jun proteins in the striatum during chronic cocaine treatment and withdrawal. Neuron 17:147-156.
77. Morgan J, Curran T. 1986. Role of ion flux in the control of c-fos expression. Nature 322:552-555.
78. Morgan J, Curran T. 1991. Stimulus-transcription-coupling in the nervous system: involvement of the inducible proto-oncogenes fos and jun. Annu Rev Neurosci 14:421-451.
79. Morris RJ, Beech JN, Heizmann CW. 1988. Two distinct phases and mechanisms of axonal growth shown by primary vestibular fibres in the brain, demonstrated by parvalbumin immunohistochemistry. Neuroscience 27:571-596.
80. Paige GD, Tomko DL. 1991. Eye movement responses to linear head motion in the squirrel monkey. I. Basic characteristics. J Neurophysiol 65:1170-1182.
81. Paxinos G, Watson C. 1998. The rat brain in stereotaxic coordinates. San Diego: Academic Press.
82. Paxinos G, Ashwell KWS, Tork I. 1994. Atlas of the developing rat nervous system. San Diego: Academic Press.
83. Peterson BW, Fukushima K, Hirai N, Schor RH, Wilson VJ. 1980. Responses of vestibulospinal and reticulospinal neurons to sinusoidal vestibular stimulation. J Neurophysiol 43:1236-1250.
84. Pompeiano O, Manzoni D, Barnes CD. 1991. Responses of locus coeruleus neurons to labyrinth and neck stimulation. Prog Brain Res 88:411-434.
85. Reisine H, Raphan T. 1992. Neural basis for eye velocity generation in the vestibular nuclei of alert monkeys during off-vertical axis rotation. Exp Brain Res 92:209-226.
86. Ris L, Godaux E. 1998. Neuronal activity in the vestibular nuclei after contralateral or bilateral labyrinthectomy in the alert guinea pig. J Neurophysiol 80:2352-2367.
87. Ris L, de Waele C, Serafin M, Vidal PP, Godaux E. 1995. Neuronal activity in the ipsilateral vestibular nucleus following unilateral labyrinthectomy in the alert guinea pig. J Neurophysiol 74:2087-2099.
88. Rossiter CD, Hayden NL, Stocker SD, Yates BJ. 1996. Changes in outflow to respiratory pump muscles produced by natural vestibular stimulation. J Neurophysiol 76:3274-3284.
89. Rubertone JA, Mehler WR, Cox GE. 1983. The intrinsic organization of the vestibular complex: evidence for internuclear connectivity. Brain Res 263:137-141.
90. Sagar SM, Sharp FR, Curran T. 1988. Expression of c-fos protein in brain: metabolic mapping at the cellular level. Science 240:1328-1331.
91. Saper CB. 1996. Any way you cut it: a new journal policy for the use of unbiased counting methods. J Comp Neurol 364:5.
92. Schoenfeld NM, Leathem JH, Rabji J. 1980. Maturation of adrenal stress responsiveness in the rat. Neuroendocrinology 31:101-105.
93. Schor RH, Miller AD, Timerick SJB, Tomko DL. 1985. Responses to head tilt in cat central vestibular neurons. I. Frequency dependence of neuronal response vectors. J Neurophysiol 53:1444-1452.
94. Sheng M, Greenberg ME. 1990. The regulation and function of c-fos and other immediate early genes in the nervous system. Neuron 4:477-485.
95. Shu SY, Ju G, Fan LZ. 1988. The glucose oxidase-DAB-nickel method in peroxidase histochemistry of the nervous system. Neurosci Lett 85:169-171.
96. Telford L, Seidman SH, Paige GD. 1997. Dynamics of squirrel monkey linear vestibuloocular reflex and interactions with fixation distance. J Neurophysiol 78:1775-1790.
97. Wenzel W, Fritschy JM, Mohler H, Benke D. 1997. NMDA receptor heterogeneity during postnatal development of the rat brain: differential expression of the NR2A, NR2B, and NR2C subunit proteins. J Neurochem 68:469-478.
98. Wood SJ. 2002. Human otolith-ocular reflexes during off-vertical axis rotation: effect of frequency on tilt-translation ambiguity and motion sickness. Neurosci Lett 323:41-44.
99. Yates BJ, Miller AD. 1994. Properties of sympathetic reflexes elicited by natural vestibular stimulation: implications for cardiovascular control. J Neurophysiol 71:2087-2092.