Long-term effects of permanent vestibular lesions on hippocampal spatial firing

Journal of Neuroscience

Volumn 23, Issue 16, 2003, Pages 6490-6498

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

^a UNIVERSITY OF OTAGO   (New Zealand)

^b UNIVERSITY OF OTAGO   (New Zealand)

^c OSAKA UNIVERSITY MEDICAL SCHOOL   (Japan)

Author keywords

Compensation; Hippocampus; Labyrinthectomy; Navigation; Place cell; Place field; Self motion; Vestibular

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; CONTROLLED STUDY; HIPPOCAMPUS; LABYRINTHECTOMY; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; RIGHTING REFLEX; SPATIAL ORIENTATION; SPIKE WAVE; VESTIBULAR SYSTEM;

EID: 0041342032     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-16-06490.2003     Document Type: Article

References (50)

1. Bannerman DM, Gilmour G, Norman G, Lemaire M, Iversen SD, Rawlins JN (2001) The time course of the hyperactivity that follows lesions or temporary inactivation of the fimbria-fornix. Behav Brain Res 120:1-11.
2. Basile AS, Brichta AM, Harris BD, Morse D, Coling D, Skolnick P (1999) Dizocilpine attenuates streptomycin-induced vestibulotoxicity in rats. Neurosci Lett 265:71-74.
3. Berger TW, Rinaldi PC, Weisz DJ, Thompson RF (1983) Single-unit analysis of different hippocampal cell types during classical conditioning of rabbit nictitating membrane response. J Neurophysiol 50:1197-1219.
4. Bilkey DK, Muir GM (1999) A low cost, high precision subminiature microdrive for extracellular unit recording in behaving animals. J Neurosci Methods 92:87-90.
5. Bilkey DK, Russell NA, Colombo M (2003) A lightweight microdrive for single unit recording in freely moving rats and pigeons. Methods 30:152-158.
6. Curthoys IS, Halmagyi GM (1995) Vestibular compensation: a review of the oculomotor, neural, and clinical consequences of unilateral vestibular loss. J Vestib Res 5:67-107.
7. Cuthbert PC, Gilchrist DP, Hicks SL, MacDougall HG, Curthoys IS (2000) Electrophysiological evidence for vestibular activation of the guinea pig hippocampus. NeuroReport 11:1443-1447.
8. Deliagina TG, Popova LB, Grant G (1997) The role of tonic vestibular input for postural control in rats. Arch Ital Biol 135:239-261.
9. Dudchenko P, Goodridge JP, Taube JS (1997) The effects of disorientation on visual landmark control of head direction cell orientation. Exp Brain Res 115:375-380.
10. Fox SE, Ranck Jr JB (1981) Electrophysiological characteristics of hippocampal complex-spike cells and theta cells. Exp Brain Res 41:399 -410.
11. Freund TF, Buzsaki G (1996) Interneurons of the hippocampus. Hippocampus 6:347-470.
12. Fukushima M, Kitahara T, Takeda N, Saika T, Uno A, Kubo T (2001) Role of cholinergic mossy fibers in medial vestibular and prepositus hypoglossal nuclei in vestibular compensation. Neuroscience 102:159-166.
13. Gavrilov VV, Wiener SI, Berthoz A (1998) Discharge correlates of hippocampal complex spike neurons in behaving rats passively displaced on a mobile robot. Hippocampus 8:475-490.
14. Gilchrist DPD, Curthoys IS, Cartwright AD, Burgess AM, Topple AN, Halmagyi GM (1998) High acceleration impulsive rotations reveal severe long-term deficits of the horizontal vestibulo- ocular reflex in the guinea pig. Exp Brain Res 123:242-245.
15. Gothard KM, Hoffman KL, Battaglia FP, McNaughton BL (2001) Dentate gyrus and CA1 ensemble activity during spatial reference frame shifts in the presence and absence of visual input. J Neurosci 21:7284-7292.
16. Hayakawa T, Ito H, Zyo K (1993) Neuroanatomical study of afferent projections to the supramammillary nucleus of the rat. Anat Embryol 188:139-148.
17. Hill AJ, Best PJ (1981) Effects of deafness and blindness on the spatial correlates of hippocampal unit activity in the rat. Exp Neurol 74:204-217.
18. Jensen DW (1983) Survival of function in the deafferented vestibular nerve. Brain Res 273:175-178.
19. Kirk IJ, McNaughton N (1991) Supramammillary cell firing and hippocampal rhythmical slow activity. NeuroReport 2:723-725.
20. Kubie JL, Muller RU, Bostock E (1990) Spatial firing properties of hippocampal theta cells. J Neurosci 10:1110-1123.
21. Markus EJ, Barnes CA, McNaughton BL, Gladden VL, Skaggs WE (1994) Spatial information content and reliability of hippocampal CA1 neurons: effects of visual input. Hippocampus 4:410-421.
22. Markus EJ, Qin YL, Leonard B, Skaggs WE, McNaughton BL, Barnes CA (1995) Interactions between location and task affect the spatial and directional firing of hippocampal neurons. J Neurosci 15:7079-7094.
23. McNaughton BL, Barnes CA, O'Keefe J (1983) The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats. Exp Brain Res 52:41-49.
24. Muller RU, Kubie JL, Ranck Jr JB (1987) Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. J Neurosci 7:1935-1950.
25. O'Keefe J (1979) A review of the hippocampal place cells. Prog Neurobiol 13:419-439.
26. O'Keefe J, Dostrovsky J (1971) The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 34:171-175.
27. O'Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Oxford: Clarendon.
28. O'Mara SM, Rolls ET, Berthoz A, Kesner RP (1994) Neurons responding to whole-body motion in the primate hippocampus. J Neurosci 14:6511-6523.
29. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates, Ed 4. Orlando, FL: Academic.
30. Quirk GJ, Muller RU, Kubie JL (1990) The firing of hippocampal place cells in the dark depends on the rat's recent experience. J Neurosci 10:2008-2017.
31. 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.
32. Rossier J, Haeberli C, Schenk F (2000) Auditory cues support place navigation in rats when associated with a visual cue. Behav Brain Res 117:209-214.
33. Russell NA, Horii A, Liu P, Smith PF, Darlington CL, Bilkey DK (2000) Hippocampal place Fields have decreased stability in rats with bilateral vestibular labyrinthectomies. Soc Neurosci Abstr 26:173.4.
34. Save E, Cressant A, Thinus-Blanc C, Poucet B (1998) Spatial firing of hippocampal place cells in blind rats. J Neurosci 18:1818-1826.
35. Semba K, Reiner PB, McGeer EG, Fibiger HC (1988) Brainstem afferents to the magnocellular basal forebrain studied by axonal transport, immunohistochemistry, and electrophysiology in the rat. J Comp Neurol 267:433-453.
36. Shapiro ML, Tanila H, Eichenbaum H (1997) Cues that hippocampal place cells encode: dynamic and hierarchical representation of local and distal stimuli. Hippocampus 7:624-642.
37. Sharp PE, Blair HT, Etkin D, Tzanetos DB (1995) Influences of vestibular and visual motion information on the spatial firing patterns of hippocampal place cells. J Neurosci 15:173-189.
38. Skaggs WE, McNaughton BL, Gothard KM, Markus EJ (1993) An information-theoretic approach to deciphering the hippocampal code. In: Advances in neural information processing systems (Hanson SJ, Cowan JD, Giles CL, eds), pp 1030-1037. San Mateo, CA: Morgan Kaufmann.
39. Smith PF (1997) Vestibular-hippocampal interactions. Hippocampus 7:465-471.
40. Smith PF, Curthoys IS (1989) Mechanisms of recovery following unilateral labyrinthectomy: a review. Brain Res Brain Res Rev 14:155-180.
41. Stackman RW, Taube JS (1997) Firing properties of head direction cells in the rat anterior thalamic nucleus: dependence on vestibular input. J Neurosci 17:4349-4358.
42. Stackman RW, Clark AS, Taube JS (2002) Hippocampal spatial representations require vestibular input. Hippocampus 12:291-303.
43. Taube JS, Goodridge JP, Golob EJ, Dudchenko PA, Stackman RW (1996) Processing the head direction cell signal: a review and commentary. Brain Res Bull 40:477-486.
44. Vertes RP, Kocsis B (1997) Brainstem-diencephalo-septohippocampal systems controlling the theta rhythm of the hippocampus. Neuroscience 81:893-926.
45. Whishaw IQ (1998) Place learning in hippocampal rats and the path integration hypothesis. Neurosci Biobehav Rev 22:209-220.
46. Wiener SI, Korshunov VA, Garcia R, Berthoz A (1995) Inertial, substratal and landmark cue control of hippocampal CA1 place cell activity. Eur J Neurosci 7:2206-2219.
47. Wilson VJ, Melvill Jones G (1979) Mammalian vestibular physiology. New York: Plenum.
48. Wood ER, Dudchenko PA, Eichenbaum H (2001) Cellular correlates of behavior. Int Rev Neurobiol 45:293-312.
49. Wylie DR, Glover RG, Aitchison JD (1999) Optic flow input to the hippocampal formation from the accessory optic system. J Neurosci 19:5514-5527.
50. Zheng Y, Horii A, Appleton I, Darlington CL, Smith PF (2001) Damage to the vestibular inner ear causes long-term changes in neuronal nitric oxide synthase expression in the rat hippocampus. Neuroscience 105:1-5.