The effects of complete vestibular deafferentation on spatial memory and the hippocampus in the rat: The Dunedin experience

Multisensory Research

Volumn 28, Issue 5-6, 2015, Pages 461-485

  Smith, Paul F ^a   Darlington, Cynthia L ^a   Zheng, Yiwen ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

hippocampus; place cells; rat; spatial memory; theta rhythm; Vestibular

Indexed keywords

AUDITION; OBJECT RECOGNITION; RATING; RATS;

HIPPOCAMPUS; PLACE CELL; SPATIAL MEMORY; THETA RHYTHMS; VESTIBULAR;

BRAIN;

RATTUS;

ANIMAL; DEPTH PERCEPTION; DISEASE MODEL; EXPLORATORY BEHAVIOR; HIPPOCAMPUS; MEMORY DISORDER; PATHOPHYSIOLOGY; PHYSIOLOGY; RAT; SPATIAL MEMORY; VESTIBULAR DISORDER; VESTIBULAR LABYRINTH;

ANIMALS; DISEASE MODELS, ANIMAL; EXPLORATORY BEHAVIOR; HIPPOCAMPUS; MEMORY DISORDERS; RATS; SPACE PERCEPTION; SPATIAL MEMORY; VESTIBULAR DISEASES; VESTIBULE, LABYRINTH;

EID: 84938596638     PISSN: 22134794     EISSN: 22134808     Source Type: Journal    
DOI: 10.1163/22134808-00002469     Document Type: Article

References (47)

1. Baek, J.-H., Zheng, Y., Darlington, C. L. and Smith, P. F. (2010). Evidence that spatial memory deficits in rats following bilateral vestibular loss is probably permanent, Neurobiol. Learn. Mem. 94, 402-413.
2. Besnard, S., Machado, M. L., Vignaux, G., Boulouard, M., Coquerel, A., Bouet, V., Freret, T., Denise, P. and Lelong-Boulouard, V. (2012). Influence of vestibular input on spatial and nonspatial memory and on hippocampal NMDA receptors, Hippocampus 22, 814-826.
3. Brandt, T., Schautzer, F., Hamilton, D. A., Bruning, R., Markowitsch, H., Kalla, R., Darlington, C. L., Smith, P. F. and Strupp, M. (2005). Vestibular loss causes hippocampal atrophy and impaired spatial memory in humans, Brain 128, 2732-2741.
4. Chapuis, N., Krimm, M., deWaele, C., Vibert, N. and Berthoz, A. (1992). Effect of post-training unilateral labyrinthectomy in a spatial orientation task by Guinea pigs, Behav. Brain Res. 51, 115-126.
5. Curthoys, I. S. and Halmagyi, G. M. (1995). Vestibular compensation: a review of the ocular motor, neural and clinical consequences of unilateral vestibular loss, J. Vest. Res. 5, 67-107.
6. Cutfield, N. J., Scott, G., Waldman, A. D., Sharp, D. J. and Bronstein, A. M. (2014). Visual and proprioceptive interaction in patients with bilateral vestibular loss, Neuroimage Clin. 4, 274-282.
7. Cuthbert, P. C., Gilchrist, D. P., Hicks, S. L., MacDougall, H. G. and Curthoys, I. S. (2000). Electrophysiological evidence for vestibular activation of the Guinea pig hippocampus, NeuroReport 11, 1443-1447.
8. Goble, T. J., Mller, A. R. and Thompson, L. T. (2009). Acute high-intensity sound exposure alters responses of place cells in hippocampus, Hear. Res. 253, 52-59.
9. Goddard, M., Zheng, Y., Darlington, C. L. and Smith, P. F. (2008a). Locomotor and exploratory behaviour in the rat following bilateral vestibular deafferentation, Behav. Neurosci. 122, 448-459.
10. Goddard, M., Zheng, Y., Darlington, C. L. and Smith, P. F. (2008b). Synaptic protein expression in the medial temporal lobe and frontal cortex following chronic bilateral vestibular loss, Hippocampus 18, 440-444.
11. Goddard, M., Zheng, Y., Darlington, C. L. and Smith, P. F. (2008c). Monoamine transporter and enzyme expression in the medial temporal lobe and frontal lobes following chronic bilateral vestibular loss, Neurosci. Lett. 437, 107-110.
12. Hitier, M., Besnard, S. and Smith, P. F. (2014). Vestibular pathways involved in cognition, Front. Integr. Neurosci. 8, 59, 1-16.
13. Horii, A., Takeda, N., Mochizuki, T., Okakura-Mochizuki, K., Yamamoto, Y. and Yamatodani, A. (1994). Effects of vestibular stimulation on acetylcholine release from rat hippocampus: an in vivo microdialysis study, J. Neurophysiol. 72, 605-611.
14. Horii, A., Russell, N., Smith, P. F., Darlington, C. L. and Bilkey, D. K. (2004). Vestibular influences on CA1 neurons in the rat hippocampus: an electrophysiological study in vivo, Exp. Brain Res. 155, 245-250.
15. Horn, K. M., DeWitt, J. R. and Nielson, H. C. (1981). Behavioral assessment of sodium arsanilate induced vestibular dysfunction in rats, Physiol. Psychol. 9, 371-378.
16. Jacob, P. Y., Poucet, B., Liberge, M., Save, E. and Sargolini, F. (2014). Vestibular control of entorhinal cortex activity in spatial navigation, Front Integr. Neurosci. 8, 38.
17. Jeewajee, A., Barry, C., OKeefe, J. and Burgess, N. (2008). Grid cells and theta as oscillatory interference: electrophysiological data from freely moving rats, Hippocampus 18, 1175-1185.
18. Lever, C., Jeewajee, A., Burton, S., OKeefe, J. and Burgess, N. (2009). Hippocampal theta frequency, novelty and behavior, Hippocampus 19, 409-410.
19. Lopez, C. and Blanke, O. (2011). The thalamocortical vestibular system in animals and humans, Brain Res. Rev. 67, 119-146.
20. Machado, M. L., Lelong-Boulouard, V., Smith, P. F., Freret, T., Philoxene, B., Denise, P. and Besnard, S. (2012). Influence of anxiety in spatial memory impairments related to the loss of vestibular function in rat, Neuroscience 218, 161-169.
21. Neo, P., Carter, D., Zheng, Y., Smith, P. F., Darlington, C. L. and McNaughton, N. (2012). Septal elicitation of hippocampal theta rhythm did not repair the cognitive and emotional deficits resulting from vestibular lesions, Hippocampus 22, 1176-1187.
22. Ossenkopp, K. P. and Hargreaves, E. L. (1993). Spatial learning in an enclosed eight-arm maze in rats with sodium arsinilate-induced labyrinthectomies, Behav. Neur. Biol. 59, 253-257.
23. Russell, N., Horii, A., Smith, P. F., Darlington, C. L. and Bilkey, D. (2003a). Effects of bilateral vestibular deafferentation on radial arm maze performance, J. Vestib. Res. 13, 9-16.
24. Russell, N., Horii, A., Smith, P. F., Darlington, C. L. and Bilkey, D. (2003b). The long-term effects of permanent vestibular lesions on hippocampal spatial firing, J. Neurosci. 23, 6490-6498.
25. Russell, N., Horii, A., Smith, P. F., Darlington, C. L. and Bilkey, D. (2006). Lesions of the vestibular system disrupt hippocampal theta rhythm in the rat, J. Neurophysiol. 96, 4-14.
26. Schaeppi, U., Krinke, G., FitzGerald, R. E. and Classen, W. (1991). Impaired tunnel-maze behavior in rats with sensory lesions: vestibular and auditory systems, Neurotoxicology 12, 445-454.
27. Shinder, M. E. and Taube, J. S. (2010). Differentiating ascending vestibular pathways to the cortex involved in spatial cognition, J. Vestib. Res. 20, 3-23.
28. Smith, P. F. and Zheng, Y. (2013a). From ear to uncertainty: vestibular contributions to cognitive function, Front. Integr. Neurosci. 7, 84.
29. Smith, P. F. and Zheng, Y. (2013b). Principal component analysis suggests subtle changes in glutamate receptor subunit expression in the rat hippocampus following bilateral vestibular deafferentation in the rat, Neurosci. Lett. 548, 265-268.
30. Smith, P. F., Haslett, S. J. and Zheng, Y. (2013). A multivariate statistical and data mining analysis of spatial memory-related behavior following bilateral vestibular deafferentation in the rat, Behav. Brain Res. 246, 15-23.
31. Stackman, R. W., Clark, A. S. and Taube, J. S. (2002). Hippocampal spatial representations require vestibular input, Hippocampus 12, 291-303.
32. Stackman, R. W. and Herbert, A. M. (2002). Rats with lesions of the vestibular system require a visual landmark for spatial navigation, Behav. Brain Res. 128, 27-40.
33. Stiles, L., Zheng, Y., Darlington, C. L. and Smith, P. F. (2012). The D2 dopamine receptor and locomotor hyperactivity following bilateral vestibular deafferentation in the rat, Behav. Brain Res. 227, 150-158.
34. Tai, S. K., Ma, J., Ossenkopp, K. P. and Leung, L. S. (2012). Activation of immobility-related hippocampal theta by cholinergic septohippocampal neurons during vestibular stimulation, Hippocampus 22, 914-925.
35. Wallace, D. G., Hines, D. J., Pellis, S. M. and Whishaw, I. Q. (2002). Vestibular information is required for dead reckoning in the rat, J. Neurosci. 15, 10009-10017.
36. Zheng, Y., Kerr, D. S., Darlington, C. L. and Smith, P. F. (2003). Peripheral vestibular damage causes a lasting decrease in the electrical excitability of CA1 in hippocampal slices in vitro, Hippocampus 13, 873-878.
37. Zheng, Y., Darlington, C. L. and Smith, P. F. (2004). Bilateral vestibular deafferentation impairs object recognition in rat, NeuroReport 15, 1913-1916.
38. Zheng, Y., Goddard, M., Darlington, C. L. and Smith, P. F. (2007). Bilateral vestibular deafferentation impairs performance in a spatial forced alternation task in rats, Hippocampus 17, 253-256.
39. Zheng, Y., Goddard, M., Darlington, C. L. and Smith, P. F. (2009a). Long-term deficits on a foraging task after bilateral vestibular deafferentation in rats, Hippocampus 19, 480-486.
40. Zheng, Y., Balabhadrapatruni, S., Munn, O., Masumura, C., Darlington, C. L. and Smith, P. F. (2009b). Evidence for deficits in a 5 choice serial reaction time task in rats with bilateral vestibular deafferentation, Behav. Brain Res. 203, 113-117.
41. Zheng, Y., Mason-Parker, S. E., Logan, B., Darlington, C. L., Smith, P. F. and Abraham, W. C. (2010). Hippocampal synaptic transmission and LTP in vivo are intact following bilateral vestibular deafferentation in the rat, Hippocampus 20, 461-468.
42. Zheng, Y., Hamilton, E., Begum, S., Smith, P. F. and Darlington, C. L. (2011). The effects of acoustic trauma that can cause tinnitus on spatial performance in rats, Neuroscience 186, 48-56.
43. Zheng, Y., Cheung, I. and Smith, P. F. (2012a). Performance in anxiety and spatial memory tests following bilateral vestibular loss in the rat and effects of anxiolytic and anxiogenic drugs, Behav. Brain Res. 235, 21-29.
44. Zheng, Y., Balabhadrapatruni, S., Chung, P., Gliddon, C. M., Zhang, M., Napper, R., Baek, J.-H., Brandt, T., Strupp, M., Darlington, C. L. and Smith, P. F. (2012b). The effects of bilateral vestibular loss on hippocampal volume, neuronal number and cell proliferation in rats, Front. Neuro-Otol. 3, 20.
45. Zheng, Y., Wilson, G., Stiles, L. and Smith, P. F. (2013). Glutamate receptor subunit and calmodulin kinase II expression in the rat hippocampus, with and without T maze experience, following bilateral vestibular deafferentation, PLoS One 8(2), e54527. DOI:10.1371/journal. pone.0054527.
46. Zheng, Y., Geddes, L., Sato, G., Stiles, L., Darlington, C. L. and Smith, P. F. (2014). Galvanic vestibular stimulation impairs cell proliferation and neurogenesis in the rat hippocampus but not spatial memory, Hippocampus 24, 541-552.
47. zu Eulenburg, P., Stoeter, P. and Dieterich, M. (2010). Voxel-based morphometry depicts central compensation after vestibular neuritis, Annal. Neurol. 68, 241-249.