Lesions of the vestibular system disrupt hippocampal theta rhythm in the rat

Journal of Neurophysiology

Volumn 96, Issue 1, 2006, Pages 4-14

  Russell, Noah A ^a   Horii, Arata ^a,b   Smith, Paul F ^a   Darlington, Cynthia L ^a   Bilkey, David K ^a,c  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b OSAKA UNIVERSITY MEDICAL SCHOOL   (Japan)

^c UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

CORTICOSTERONE;

ACCELERATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN REGION; CONTROLLED STUDY; CORRELATION ANALYSIS; CORTICOSTEROID BLOOD LEVEL; ELECTROENCEPHALOGRAM; HIPPOCAMPUS; HIPPOCAMPUS THETA RHYTHM; HISTOLOGY; MALE; MEMORY; MOVEMENT (PHYSIOLOGY); NERVE CELL; NERVE CONDUCTION; NERVE LESION; NONHUMAN; POWER SPECTRUM; PRIORITY JOURNAL; PROPRIOCEPTION; RAT; SPATIAL DISCRIMINATION; VESTIBULAR SYSTEM; VOLUNTARY MOVEMENT;

ANIMALS; CORTICOSTERONE; HIPPOCAMPUS; MALE; MEMORY DISORDERS; NEURONS, AFFERENT; PROPRIOCEPTION; RATS; RATS, SPRAGUE-DAWLEY; SPACE PERCEPTION; SPATIAL BEHAVIOR; THETA RHYTHM; TIME FACTORS; VESTIBULAR DISEASES; VESTIBULE;

EID: 33745761926     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00953.2005     Document Type: Article

References (86)

1. Andersen MB, Zimmer J, and Sams-Dodd F. Postischemic hyperactivity in the Mongolian gerbil correlates with loss of hippocampal neurons. Behav Neurosci 111: 1205-1216, 1997.
2. Arnolds DE, Lopes da Silva FH, Boeijinga P, Kamp A, and Aitink W. Hippocampal EEG and motor activity in the cat: The role of eye movements and body acceleration. Behav Brain Res 12: 121-135, 1984.
3. Bannerman DM, Gilmour G, Norman G, Lemaire M, Iversen SD, and Rawlins JN. The time course of the hyperactivity that follows lesions or temporary inactivation of the fimbria-fornix. Behav Brain Res 120: 1-11, 2001.
4. Basile AS, Brichta AM, Harris BD, Morse D, Coling D, and Skolnick P. Dizocilpine attenuates streptomycin-induced vestibulotoxicity in rats. Neurosci Lett 265: 71-74, 1999.
5. Bilkey DK and Clearwater JM. The dynamic nature of spatial encoding in the hippocampus Behav Neurosci 119: 1533-1545, 2005.
6. Bilkey DK and Goddard GV. Medial septal facilitation of hippocampal granule cell activity is mediated by inhibition of inhibitory interneurones. Brain Res 361: 99-106, 1985.
7. Bilkey DK and Muir GM. A low cost, high precision microdrive for extracellular unit recording in behaving animals. J Neurosci Methods 92: 87-90, 1999.
8. Bilkey DK, Russell NA, and Colombo M. A lightweight microdrive for single unit recording in freely moving rats and pigeons. Methods 30: 152-158, 2003.
9. Bland BH. The physiology and pharmacology of the hippocampal formation theta rhythms. Prog Neurobiol 26: 1-54, 1986.
10. Bland BH and Colom LV. Extrinsic and intrinsic properties underlying oscillation and synchrony in limbic cortex. Prog Neurobiol 41: 157-208, 1993.
11. Brandt T, Schautzer F, Hamilton DA, Bruning R, Markowitsch HJ, Kalla R, Darlington CL, Smith PF, and Strupp M. Vestibular loss causes hippocampal atrophy and impaired spatial memory in humans. Brain 128: 2732-2741, 2005.
12. Brazhnik E, Borgnis R, Muller RU, and Fox SE. The effects on place cells of local scopolamine dialysis are mimicked by a mixture of two specific muscarinic antagonists. J Neurosci. 24: 9313-9323, 2004.
13. Brazhnik ES, Muller RU, and Fox SE. Muscarinic blockade slows and degrades the location-specific firing of hippocampal pyramidal cells. J Neurosci 23: 611-621, 2003.
14. Bures J, Fenton AA, Kaminsky Y, and Zinyuk L. Place cells and place navigation. Proc Natl Acad Sci USA 94: 343-350, 1997.
15. Buzsaki G. Theta oscillations in the hippocampus. Neuron 33: 325-340, 2002.
16. Buzsaki G, Czopf J, Kondakor I, and Kellenyi L. Laminar distribution of hippocampal rhythmic slow activity (RSA) in the behaving rat: current-source density analysis, effects of urethane and atropine. Brain Res 365: 125-137, 1986.
17. Campos-Torres. A, Touret M, Vidal PP, and de Waele C. The differential response of astrocytes within the vestibular and cochlear nuclei following unilateral labyrinthectomy or vestibular afferent activity blockade by transtympanic tetrodotoxin injection in the rat. Neuroscience 130: 853-865, 2005.
18. Cuthbert PC, Gilchrist DP, Hicks SL, MacDougall HG, and Curthoys IS. Electrophysiological evidence for vestibular activation of the guinea pig hippocampus. Neuroreport 11: 1443-1447, 2000.
19. Czurko A, Hirase H, Csicsvari J, and Buzsaki G. Sustained activation of hippocampal pyramidal cells by "space clamping" in a running wheel. Eur J Neurosci 11: 344-52, 1999.
20. Deboer T. Electroencephalogram theta frequency changes in parallel with euthermic brain temperature. Brain Res 930: 212-215, 2002.
21. Decker MW, Curzon P, and Brioni JD. Influence of separate and combined septal and amygdala lesions on memory, acoustic startle, anxiety, and locomotor activity in rats. Neurobiol Learn Mem 64: 156-168, 1995.
22. Fox SE, Wolfson S, and Ranck JB Jr. Hippocampal theta rhythm and the firing of neurons in walking and urethane anesthetized rats. Exp Brain Res 62: 495-508, 1986.
23. Frederickson CJ, Frederickson MH, Lewis C, Howell GA, Smylie C, and Wright CG. Hippocampal EEG in normal mice and in mice with congenital vestibular defects. Behav Neural Biol 34: 121-131, 1982.
24. Freund TF and Antal M. GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 336: 170-173, 1988.
25. Freund TF and Buzsaki G. Interneurons of the hippocampus. Hippocampus 6: 347-470, 1996.
26. Fukushima M, Kitahara T, Takeda N, Saika T, Uno A, and Kubo T. Role of cholinergic mossy fibers in medial vestibular and prepositus hypoglossal nuclei in vestibular compensation. Neuroscience 102: 159-166, 2001.
27. Fuller PM, Jones TA, Jones SM, and Fuller CA. Neurovestibular modulation of circadian and homeostatic regulation: vestibulohypothalamic connection? Proc Natl Acad Sci USA 99: 15723-15728, 2002.
28. Gavrilov VV, Wiener SI, and Berthoz A. Enhanced hippocampal theta EEG during whole body rotations in awake restrained rats. Neurosci Lett 197: 239-241, 1995.
29. Gavrilov VV, Wiener SI, and Berthoz A. Whole-body rotations enhance hippocampal theta rhythmic slow activity in awake rats passively transported on a mobile robot. Ann NY Acad Sci 781: 385-398, 1996.
30. Gerhardt SC and Boast CA. Motor activity changes following cerebral ischemia in gerbils are correlated with the degree of neuronal degeneration in hippocampus. Behav Neurosci 102: 301-328, 1988.
31. Gliddon C, Darlington CL, and Smith PF. Activation of the hypothalamic-pituitary-adrenal axis in the guinea pig following unilateral labyrinthectomy. Brain Res 964: 306-310, 2003.
32. Gray JA and McNaughton N. The Neuropsychology of Anxiety: An Enquiry Into the Functions of the Septo-Hippocampal System (2nd ed.). Oxford, UK: Oxford Univ. Press, 2001.
33. Hayakawa T, Ito H, and Zyo K. Neuroanatomical study of afferent projections to the supramammillary nucleus of the rat. Anat Embryol 188: 139-148, 1993.
34. Horii A, Kitahara T, Smith PF, Darlington CL, Masmumura C, and Kubo T. Effects of unilateral labyrinthectomy on GAD, GAT1 and GABA receptor gene expression in the vestibular nucleus in rat. Neuroreport 14: 2359-2364, 2003.
35. Horii A, Masumura C, Smith PF, Darlington CL, Kitahara T, Uno A, Mitani K, and Kubo T. Microarray analysis of gene expression in the rat vestibular nucleus complex following unilateral vestibular deafferentation. J Neurochem 91: 975-982, 2004a.
36. Horii A, Russell NA, Smith PF, Darlington CL, and Bilkey DK. Vestibular influences on CA1 neurons in the rat hippocampus: an electrophysiological study in vivo. Exp Brain Res 155: 245-250, 2004b.
37. Horii A, Takeda N, Mochizuki T, Okakura-Mochizuki K, Yamamoto Y, and Yamatodani A. Effects of vestibular stimulation on acetylcholine release from rat hippocampus: an in vivo microdialysis study. J Neurophysiol 72: 605-611, 1994.
38. Huxter J, Burgess N, and O'Keefe J. Independent rate and temporal coding in hippocampal pyramidal cells. Nature 425: 828-832, 2003.
39. Jacob RG and Furman JM. Psychiatric consequences of vestibular dysfunction. Curr Opin Neurol 14: 41-46, 2001.
40. Kirk IJ and McNaughton N. Supramammillary cell firing and hippocampal rhythmical slow activity. Neuroreport 2: 723-725, 1991.
41. Kitahara T, Takeda N, Saika T, Kubo T, and Kiyama H. Effects of MK801 on Fos expression in the rat brainstem after unilateral labyrinthectomy. Brain Res 700: 182-190, 1995.
42. Lee MG, Chrobak JJ, Sik A, Wiley RG, and Buzsaki G. Hippocampal theta activity following selective lesion of the septal cholinergic system. Neuroscience 62: 1033-1047, 1994.
43. Leung LS. Pharmacology of theta phase shift in the hippocampal CA1 region of freely moving rats. Electroencephalogr Clin Neurol 58: 457-466, 1984a.
44. Leung LS. Theta rhythm during REM sleep and waking: correlations between power, phase and frequency. Electroencephalogr Clin Neurol 58: 553-564, 1984b.
45. Leung LW. Model of gradual phase shift of theta rhythm in the rat. J Neurophysiol 52: 1051-1065, 1984.
46. Leung LW, Lopes da Silva FH, and Wadman WJ. Spectral characteristics of the hippocampal EEG in the freely moving rat. Electroencephalogr Clin Neurol 54: 203-219, 1982.
47. Leutgeb S and Mizumori SJY. Excitotoxic septal lesions result in spatial memory deficits and altered flexibility of hippocampal single-unit representations. J Neurosci 19: 6661-6672, 1999.
48. Lindsay L, Liu P, Gliddon C, Zheng Y, Smith PF, and Darlington CL. Cytosolic glucocorticoid receptor expression in the vestibular nucleus and hippocampus following unilateral vestibular deafferentation. Exp Brain Res 162: 309-314, 2005.
49. Maclennan K, Zheng Y, Sheard P, Williams S, Darlington CL, and Smith PF. Adrenalectomy-induced cell death in the dentate gyrus: further characterization using TUNEL and effects of the Ginkgo biloba extract, EGb 761, and ginkgolide B. Hippocampus 13: 170-183, 2003.
50. Matyas F, Freund TF, and Gulyas AI. Convergence of excitatory and inhibitory inputs onto CCK-containing basket cells in the CA1 area of the rat hippocampus. Eur J Neurosci 19: 1243-1256, 2004.
51. McNaughton BL, Barnes CA, Gerrard JL, Gothard K, Jung MW, Knierim JJ, Kudrimoti H, Qin Y, Skaggs WE, Suster M, and Weaver KL. Deciphering the hippocampal polyglot: the hippocampus as a path integration system. J Exp Biol 199: 173-185, 1996.
52. McNaughton BL, Barnes CA, and O'Keefe J. The contributions of position, direction and velocity to single unit activity in the hippocampus of freely moving rats. Exp Brain Res 52: 41-49, 1983.
53. Mizumori SJ, Barnes CA, and McNaughton BL. Reversible inactivation of the medial septum: Selective effects on the spontaneous unit activity of different hippocampal cell types. Brain Res 500: 99-106, 1989.
54. Muir GM and Bilkey DK. Theta- and movement velocity-related firing of hippocampal neurons is disrupted by lesions centered on the perirhinal cortex. Hippocampus 13: 93-108, 2003.
55. Murakami DM, Erkman L, Hermanson O, Rosenfeld MG, and Fuller CA. Evidence for vestibular regulation of autonomic functions in a mouse genetic model. Proc Natl Acad Sci USA 99: 17078-17082, 2002.
56. Nerad L and Bilkey DK. Ten- to 12-Hz EEG oscillation in the rat hippocampus and rhinal cortex that is modulated by environmental familiarity. J Neurophysiol 93: 1246-1254, 2005.
57. Oddie SD and Bland BH. Hippocampal formation theta activity and movement selection. Neurosci Biobehav Rev 22: 221-231, 1998.
58. O'Keefe J and Recce ML. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3: 317-330, 1993.
59. Pan WX and McNaughton N. The medial supramammillary nucleus, spatial learning and the frequency of hippocampal theta activity. Brain Res 764: 101-108, 1997.
60. Raphan T and Cohen B. The vestibulo-ocular reflexes in three dimensions. Exp Brain Res 145: 1-27, 2002.
61. Ris L and Godaux E. Neuronal activity in the vestibular nuclei after contralateral or bilateral labyrinthectomy in the alert guinea pig. J Neurophys 80: 2352-2367, 1998.
62. Russell NA, Horii A, Smith PF, Darlington CL, and Bilkey DK. The long-term effects of permanent vestibular lesions on hippocampal spatial firing. J Neurosci 23: 6490-6498, 2003a.
63. Russell NA, Horii A, Smith PF, Darlington CL, and Bilkey DK. Bilateral peripheral vestibular lesions produce long-term changes in spatial learning in the rat. J Vestib Res 13: 9-16, 2003b.
64. Russell NA, Liu P, Darlington CL, Bilkey DK, Horii A, and Smith PF. Hippocampal Neural Firing Rate Correlations with Velocity, Acceleration, Angular Velocity and Angular Acceleration in Rats with Vestibular Lesions. Proc Intl Australasian Winter Conf Brain Res 2001.
65. Schaeppi U, Krinke G, FitzGerald RE, and Classen W. Impaired tunnel-maze behavior in rats with sensory lesions: vestibular and auditory systems. Neurotoxicology 12: 445-454, 1991.
66. Schautzer F, Hamilton D, Kalla R, Strupp M, and Brandt T. Spatial memory deficits in patients with chronic bilateral vestibular failure. Ann NY Acad Sci 1004: 316-324, 2003.
67. Semba K, Reiner PB, McGeer EG, and Fibiger HC. Brainstem afferents to the magnocellular basal forebrain studied by axonal transport, immunohistochemistry, and electrophysiology in the rat. J Comp Neurol 267: 433-453, 1988.
68. Sharp PE, Blair HT, Etkin D, and Tzanetos DB. Influences of vestibular and visual motion information on the spatial firing patterns of hippocampal place cells. J Neurosci 15: 173-189, 1995.
69. Shoham S, Chen YC, DeVietti TL, and Teitelbaum P. Deafferentation of the vestibular organ: effects on atropine-resistant EEG in rats. Psychobiol 17: 307-314, 1989.
70. Skaggs WE, McNaughton BL, Wilson MA, and Barnes CA. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6: 149-172, 1996.
71. Smith PF. Vestibular-hippocampal interactions. Hippocampus 7: 465-471, 1997.
72. Smith PF and Curthoys IS. Mechanisms of recovery following unilateral labyrinthectomy: a review. Brain Res Brain Res Rev 14: 155-180, 1989.
73. Smith PF, Zheng Y, Horii A, and Darlington CL. Does vestibular damage cause cognitive dysfunction in humans? J Vestib Res 15: 1-9, 2005.
74. Stackman RW, Clark AS, and Taube JS. Hippocampal spatial representations require vestibular input. Hippocampus 12: 291-303, 2002.
75. Stackman RW and Taube JS. Firing properties of head direction cells in the rat anterior thalamic nucleus: dependence on vestibular input. J Neurosci 17: 4349-4358, 1997.
76. Taube JS, Goodridge JP, Golob EJ, Dudchenko PA, and Stackman RW. Processing the head direction cell signal: a review and commentary. Brain Res Bull 40: 477-486, 1996.
77. Terrazas A, Krause M, Lipa P, Gothard KM, Barnes CA, and McNaughton BL. Self-motion and the hippocampal spatial metric. J Neurosci 25: 8085-8096, 2005.
78. Toth K, Freund TF, and Miles R. Disinhibition of rat hippocampal pyramidal cells by GABAergic afferents from the septum. J Physiol 500: 463-474, 1997.
79. Vann SD and Aggleton JP. The mammillary bodies: two memory systems in one? Nat Rev Neurosci. 5: 35-44, 2004.
80. Vertes RP, Hoover WB, and Viana Di Prisco G. Theta rhythm of the hippocampus: subcortical control and functional significance. Behav Cogn Neurosci Rev. 3: 173-200, 2004.
81. Vertes RP and Kocsis B. Brainstem-diencephalo-septohippocampal systems controlling the theta rhythm of the hippocampus. Neuroscience 81: 893-926, 1997.
82. Wallace DG, Hines DJ, Pellis SM, and Whishaw IQ. Vestibular information is required for dead reckoning in the rat. J Neurosci 22: 10009-10017, 2002.
83. Whishaw IQ. Place learning in hippocampal rats and the path integration hypothesis. Neurosci Biobehav Rev 22: 209-220, 1998.
84. Wyble BP, Hyman JM, Rossi CA, and Hasselmo ME. Analysis of theta power in hippocampal EEG during bar pressing and running behavior in rats during distinct behavioral contexts. Hippocampus. 14: 662-674, 2004.
85. Wylie DR, Glover RG, and Aitchison JD. Optic flow input to the hippocampal formation from the accessory optic system. J Neurosci 19: 5514-5527, 1999.
86. Zhang R, Smith PF, and Darlington CL. An immunocytochemical and stereological study of glucocortioid receptors in the rat medical vestibular nucleus and effects of unilateral labyrinthectomy. Acta Otolaryngol 125: 1258-1264, 2005.