Asymmetric gene expression in the brain during acute compensation to unilateral vestibular labyrinthectomy in the Mongolian gerbil

Journal of Vestibular Research: Equilibrium and Orientation

Volumn 16, Issue 4-5, 2006, Pages 147-169

  Shinder, Michael E ^a   Ramanathan Jr Jr , Murugappan ^b   Kaufman, Galen D ^a,c  

^a University of Texas Medical Branch School of Medicine   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

Cerebellum; Flocculus; Gene expression; Labyrinthectomy; Plasticity; Vestibular

Indexed keywords

4 AMINOBUTYRIC ACID; DOPAMINE 3 RECEPTOR STIMULATING AGENT; GLUTAMIC ACID; GLYCINE; N METHYL DEXTRO ASPARTIC ACID; NEUROTRANSMITTER; PROTEIN SUBUNIT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; BRAIN STEM; CELL STIMULATION; CEREBELLUM; CLUSTER ANALYSIS; COMPUTER PROGRAM; CONTROLLED STUDY; DNA MICROARRAY; FEMALE; GENE EXPRESSION; GENE TARGETING; GERBIL; HYBRIDIZATION; LABYRINTHECTOMY; MALE; MOLECULAR DYNAMICS; MOUSE; NERVE CELL; NEUROBIOLOGY; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SPECIES COMPARISON; SYNTENY; VESTIBULAR DISORDER; VESTIBULE;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BRAIN; DENERVATION; EAR, INNER; FUNCTIONAL LATERALITY; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION PROFILING; GERBILLINAE; MICE; N-METHYLASPARTATE; NERVE TISSUE PROTEINS; NEURAL PATHWAYS; PROTEIN ARRAY ANALYSIS; RATS; RECOVERY OF FUNCTION; RNA; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY; VESTIBULE;

EID: 34249899668     PISSN: 09574271     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (71)

1. H.J. Adler, I.A. Belyantseva, R.C. Jr. Merritt, G.I. Frolenkov, G.W. Dougherty and B. Kachar, Expression of prestin, a membrane motor protein, in the mammalian auditory and vestibular periphery, Hear Res 184 (2003), 27-40.
2. M. Aoki, Y. Ito and H. Miyata, Prevention of vestibular deafferentation-induced spontaneous nystagmus with pretreatment of Ca2+ channel/N-methyl-D-aspartic acid receptor antagonists in guinea pigs, Acta Otolaryngol 118 (1998), 554-556.
3. C.D. Balaban and G.G. Romero, A role of climbing fibers in regulation of flocculonodular lobe protein Kinase C expression during vestibular compensation, Brain Research 804 (1998), 253-265.
4. A.B. Belousov and A.N. van den Pol, Dopamine inhibition: enhancement of GABA activity and potassium channel activation in hypothalamic and arcuate nucleus neurons, J Neurophysiol 78 (1997), 674-688.
5. M. Brudno, A. Poliakov, A. Salamov, G.M. Cooper, A. Sidow, E.M. Rubin, V. Solovyev, S. Batzoglou and I. Dubchak, Automated whole-genome multiple alignment of rat, mouse, and human, Genome Res 14 (2004), 685-692.
6. A.F. Cartwright, I.S. Curthoys and D.P. Gilchrist, Testable predictions from realistic neural network simulations of vestibular compensation: integrating the behavioral and physiological data, Biol Cybern 81 (1999), 73-87.
7. B. Chih, H. Engelman and P. Scheiffele, Control of excitatory and inhibitory synapse formation by neuroligins, Science 307 (2005), 1324-1328.
8. C. Cirelli, M. Pompeiano, P. D'ascanio and O. Pompeiano, Early c-fos expression in the rat vestibular and olivocerebellar systems after unilateral labyrinthectomy, Arch Ital Biol 131 (1993), 71-74.
9. C. Cirelli, M. Pompeiano, P. D'ascanio, P. Arrighi and O. Pompeiano, C-fos expression in the rat brain after unilateral labyrinthectomy and its relation to the uncompensated and compensated stages, Neuroscience 70 (1996), 515-546.
10. M.O. Collins, L. Yu, M.P. Coba, H. Husi, I. Campuzano, W.P. Blackstock, J.S. Choudhary and S.G. Grant, Proteomic analysis of in vivo phosphorylated synaptic proteins, J Biol Chem 280 (2005), 5972-5982.
11. J.J. Crouch and B.A. Schulte, Identification and cloning of site C splice variants of plasma membrane Ca-ATPase in the gerbil cochlea, Hear Res 101 (1996), 55-61.
12. I.S. Curthoys and G.M. Halmagyi, Vestibular compensation, Adv Otorhinolaryngol 55 (1999), 82-110.
13. C.L. Darlington and P.F. Smith, Pre-treatment with a Ca2+ channel antagonist facilitates vestibular compensation, Neuroreport 3 (1992), 143-145.
14. C.L. Darlington and P.F. Smith, Molecular mechanisms of recovery from vestibular damage in mammals: recent advances, Prog Neurobiol 62 (2000), 313-325.
15. F. Drago, L. Nardo, L. Rampello and R. Raffaele, Vestibular compensation in aged rats with unilateral labyrinthectomy treated with dopaminergic drugs, Pharmacological Research 33 (1996), 135-140.
16. L. Eleore, I. Vassias, I. Bernat, P.P. Vidal and C. de Waele, An in situ hybridization and immunofluorescence study of GABA(A) and GABA(B) receptors in the vestibular nuclei of the intact and unilaterally labyrinthectomized rat, Exp Brain Res 160 (2005), 166-179.
17. L. Eleore, I. Vassias, P.P. Vidal and C. de Waele, An in situ hybridization and immunofluorescence study of glycinergic receptors and gephyrin in the vestibular nuclei of the intact and unilaterally labyrinthectomized rat, Exp Brain Res 154 (2004), 333-344.
18. U. Fisch, The vestibular response following unilateral vestibular neurectomy, Acta Otolaryngol 76 (1973), 229-238.
19. N. Furuya and T. Koizumi, Neurotransmitters of vestibular commissural inhibition in the cat, Acta Otolaryngol 118 (1998), 64-69.
20. M.L. Garcia and E.E. Strehler, Plasma membrane calcium ATPases as critical regulators of calcium homeostasis during neuronal cell function, Front Biosci 4 (1999), D869-D882.
21. C.M. Gliddon, C.L. Darlington and P.F. Smith, GABAergic systems in the vestibular nucleus and their contribution to vestibular compensation, Prog Neurobiol 75 (2005), 53-81.
22. C.M. Gliddon, C.L. Darlington and P.F. Smith, GABA(A) receptor subunit expression in the guinea pig vestibular nucleus complex during the development of vestibular compensation, Exp Brain Res 166 (2005), 71-77.
23. J. Goossens, H. Daniel, A. Rancillac, J. van der Steen, J. Oberdick, F. Crepel, C.I. De Zeeuw and M.A. Frens, Expression of protein kinase C inhibitor blocks cerebellar long-term depression without affecting Purkinje cell excitability in alert mice, J Neurosci 21 (2001), 5813-5823.
24. M.M. Goto, G.G. Romero and C.D. Balaban, Transient changes in flocculonodular lobe protein kinase C expression during vestibular compensation, J Neurosci 17 (1997), 4367-4381.
25. C. Guilding and M.B. Dutia, Early and late changes in vestibular neuronal excitability after deafferentation, Neuroreport 16 (2005), 1415-1418.
26. S. Gustave Dit Duflo, C. Gestreau, B. Tighilet and M. Lacour, Fos expression in the cat brainstem after unilateral vestibular neurectomy, Brain Res 824 (1999), 1-17.
27. K.L. Hoe, I. Armando, G. Baiardi, T. Sreenath, A. Kulkarni, A. Martinez and J.M. Saavedra, Molecular cloning, characterization, and distribution of the gerbil angiotensin II AT2 receptor, Am J Physiol Regul Integr Comp Physiol 285 (2003), R1373-R1383.
28. A. Horii, C. Masumura, P.F. Smith, C.L. Darlington, T. Kitahara, A. Uno, K. Mitani and T. Kubo, Microarray analysis of gene expression in the rat vestibular nucleus complex following unilateral vestibular deafferentation, J Neurochem 91 (2004), 975-982.
29. A.R. Johnston, A. Him and M.B. Dutia, Differential regulation of GABA(A) and GABA(B) receptors during vestibular compensation, Neuroreport 12 (2001), 597-600.
30. G.D. Kaufman, J.H. Anderson and A.J. Beitz, Brainstem Fos expression following acute unilateral labyrinthectomy in the rat, Neuroreport 3 (1992), 829-832.
31. G.D. Kaufman, J.H. Anderson and A.J. Beitz, 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 (1993), 117-127.
32. G.D. Kaufman, M.E. Shinder and A.A. Perachio, Correlation of Fos expression and behavioral turning during gerbil vestibular compensation, Brain Res 817 (1999), 246-255.
33. G.D. Kaufman, M. Ramanathan and M.E. Shinder, Microarray analysis of vestibular compensation in the gerbil, Soc Neurosci Abstr 703.12, New Orleans, LA, 2003.
34. G.D. Kaufman, Fos expression in the vestibular system: What one marker can tell us about the network, Brain Research Reviews 50 (2005), 200-211.
35. A.E. Kelley, M.E. Andrzejewski, A.E. Baldwin, P.J. Hernandez and W.E. Pratt, Glutamate-mediated plasticity in corticostriatal networks: role in adaptive motor learning, Ann NY Acad Sci 1003 (2003), 159-168.
36. D.R. Kerr, A.J. Sansom, P.F. Smith and C.L. Darlington, Comparison of protein kinase activity and protein phosphorylation in the medial vestibular nucleus and prepositus hypoglossi in labyrinthine-intact and labyrinthectomized guinea pigs, J Vestib Res 10 (2000), 107-117.
37. M.S. Kim, J.H. Kim, Y.Z. Jin, D. Kry and B.R. Park, Temporal changes of cFos-like protein expression in medial vestibular nuclei following arsanilate-induced unilateral labyrinthectomy in rats, Neurosci Lett 319 (2002), 9-12.
38. T. Kitahara, T. Saika, N. Takeda, H. Kiyama and T. Kubo, Changes in Fos and Jun expression in the rat brainstem in the process of vestibular compensation, Acta Oto-Laryngol Suppl (Stockh) 520 (1995), 401-404.
39. T. Kitahara, N. Takeda, T. Saika, T. Kubo and H. Kiyama, Effects of MK801 on Fos expression in the rat brainstem after unilateral labyrinthectomy, Brain Res 700 (1995), 182-190.
40. T. Kitahara, N. Takesa and T. Kubo, Nitric oxide in the flocculus works the inhibitory neural circuits after unilateral labyrinthectomy, Brain Res 815 (1999), 405-409.
41. T. Kitahara, M. Fukushima, N. Takeda, T. Saika and T. Kubo, Effects of pre-flocculectomy on Fos expression and NMDA receptor-mediated neural circuits in the central vestibular system after unilateral labyrinthectomy, Acta Otolaryngol 120 (2000), 866-871.
42. H.Y. Li, T.G. Godfrey, D.A. Godfrey and A.M. Rubin, Quantitative changes of amino acid distributions in the rat vestibular nuclear complex after unilateral vestibular ganglionectomy, Journal of Neurochemistry 66 (1996), 1550-1564.
43. X.Y. Li, T. Hashimoto, W. Tokuyama, Y. Miyashita and H. Okuno, Spatiotemporal dynamics of brain-derived neurotrophic factor mRNA induction in the vestibulo-olivary network during vestibular compensation, J Neurosci 21 (2001), 2738-2748.
44. G. Liu, A.E. Loraine, R. Shigeta, M. Cline, J. Cheng, V. Vaimeekam, S. Sun, D. Kulp and M.A. Siani-Rose, NetAffx: Affymetrix probesets and annotations, Nucleic Acids Res 31 (2003), 82-86.
45. D.J. Lockhart, H. Dong, M.C. Byrne, M.T. Follettie, M.V. Gallo, M.S. Chee, M Mittmann, C. Wang, M. Kobayashi, H. Horton and E.L. Brown, Expression monitoring by hybridization to high-density oligonucleotide arrays, Nat Biotechnol 14 (1996), 1675-1680.
46. A.K. Magnusson, S. Lindstrom and R. Tham, GABA(B) receptors contribute to vestibular compensation after unilateral labyrinthectomy in pigmented rats, Exp Brain Res 134 (2000), 32-41.
47. M. Miles and R. Kerns, Analysis and Interpretation of Microarray Data, in: The Bioinformatics of Brains: From Genes and Proteins to Behaviors, R.W. Williams, ed., Society for Neuroscience, Washington, DC, 2003, pp. 41-49.
48. A.B. Nelson, C.M. Krispel, C. Sekirnjak and S. Du Lac, Long-lasting increases in intrinsic excitability triggered by inhibition, Neuron 40 (2003), 609-620.
49. S.D. Newlands, S. Dara and G.D. Kaufman, VOR compensation after unilateral canal plugging or labyrinthectomy in the gerbil, The Laryngoscope 115 (2005), 191-204.
50. S.D. Newlands and A.A. Perachio, Compensation of horizontal canal related activity in the medial vestibular nucleus following unilateral labyrinth ablation in the decerebrate gerbil II. Type II neurons, Exp Brain Res 82 (1990), 373-383.
51. E. Passarge, B. Horsthemke and R.A. Farber, Incorrect use of the term synteny, Nat Genet 23 (1999), 387.
52. L. Petrosini and M.E. Dell'Anna, Vestibular compensation is affected by treatment with dopamine active agents, Arch Ital Biol 131 (1993), 159-171.
53. K.J. Rennie, T. Weng and M.J. Correia, Effects of KCNQ channel blockers on K(+) currents in vestibular hair cells, Am J Physiol Cell Physiol 280 (2001), C473-C480.
54. I.M. Reti, L.B. Minor and J.M. Baraban, Prominent expression of Narp in central vestibular pathways: selective effect of labyrinth ablation, Eur J Neurosci 16 (2002), 1949-1958.
55. A.J. Sansom, C.L. Darlington and P.F. Smith, Pretreatment with MK-801 reduces spontaneous nystagmus following unilateral labyrinthectomy, Eur J Pharmacol 220 (1992), 123-129.
56. A.J. Sansom, V.A. Brent, P.E. Jarvie, C.L. Darlington, P.F. Smith, R. Laverty and J.A.P. Rostas, In vitro phosphorylation of medial vestibular nucleus and prepositus hypoglossi proteins during behavioral recovery from unilateral vestibular deafferentation in the guinea pig, Brain Res 778 (1997), 166-177.
57. C. Sekirnjak and S. Du Lac, Intrinsic firing dynamics of vestibular nucleus neurons, J Neurosci 22 (2002), 2083-2095.
58. M.E. Shinder, A.A. Perachio and G.D. Kaufman, VOR and Fos response during acute vestibular compensation in the Mongolian gerbil in darkness and in light, Brain Res 1038 (2005), 183-197.
59. M.R. Smith, A.B. Nelson and S. Du Lac, Regulation of firing response gain by calcium-dependent mechanisms in vestibular nucleus neurons, J Neurophysiol 87 (2002), 2031-2042.
60. P.F. Smith and I.S. Curthoys, Neuronal activity in the contralateral medial vestibular nucleus of the guinea pig following unilateral labyrinthectomy, Brain Res 444 (1988), 295-307.
61. P.F. Smith and C.L. Darlington, The NMDA antagonists MK801 and CPP disrupt compensation for unilateral labyrinthectomy in the guinea pig, Neurosci Lett 94 (1988), 309-313.
62. J.S. Stahl, Eye movements of the murine P/Q calcium channel mutant rocker, and the impact of aging, J Neurophysiol 91 (2004), 2066-2078.
63. H. Straka, N. Vibert, P.P. Vidal, L.E. Moore and M.B. Dutia, Intrinsic membrane properties of vertebrate vestibular neurons: Function, development and plasticity, Prog Neurobiol 76 (2005), 349-392.
64. E. Tolu, O. Mameli, M.A. Caria and F. Melis, Improvement of vestibular plasticity in the guinea pig with a calcium entry blocker, Acta Otolaryngol Suppl 460 (1988), 72-79.
65. N. Vibert, N. Serafin, O. Crambes, P.P. Vidal and M. Muhlethaler, Dopaminergic agonists have both presynaptic and postsynaptic effects on the guinea-pig's medial vestibular nucleus neurons, Eur J Neurosci 7 (1995), 555-562.
66. N. Vibert, N. Serafin, P.P. Vidal and M. Muhlethaler, Direct and indirect effects of muscimol on medial vestibular nucleus neurones in guinea-pig brainstem slices, Exp Brain Res 104 (1995), 351-356.
67. N. Vibert, M. Serafin, C. de Waele, A. Babalian, M. Muhlethaler and P.P Vidal, Modulatory effects of monomines on central vestibular neurons: possible functional implications, in: Neurochemistry of the Vestibular System, A.J. Beitz and J.H. Anderson, eds, CRCPress, NewYork, 2000, pp. 163-181.
68. J.R. Wickens, J.N. Reynolds and B.L. Hyland, Neural mechanisms of reward-related motor learning, Curr Opin Neurobiol 13 (2003), 685-690.
69. D. Xu, C. Hope, R. Reddy, R.W. Cho, L. Guo, A. Lanaham, R.S. Petralia, R.J. Wenthold, R.T. O'brien and P. Worley, Narp and NP1 form heterocomplexes that function in developmental and activity-dependent synaptic plasticity, Neuron 39 (2003), 513-528.
70. R. Zhang, J. Ashton, A. Horii, C.L. Darlington and P.F. Smith, Immunocytochemical and stereological analysis of GABA(B) receptor subunit expression in the rat vestibular nucleus following unilateral vestibular deafferentation, Brain Res 1037 (2005), 107-113.
71. Y.D. Zhou, T.J. Turner and K. Dunlap, Enhanced G protein-dependent modulation of excitatory synaptic transmission in the cerebellum of the Ca2+ channel-mutant mouse, tottering, J Physiol 547 (2003), 497-507.