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The Journal of Neuroscience, July 23, 2003, 23(16):6490-6498

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Long-Term Effects of Permanent Vestibular Lesions on Hippocampal Spatial Firing

Noah A. Russell,¹ Arata Horii,^2,3 Paul F. Smith,² Cynthia L. Darlington,^1,2 and David K. Bilkey¹

¹Department of Psychology and Neuroscience Research Centre and ²Department of Pharmacology and Toxicology, School of Medical Sciences, University of Otago, Dunedin, 9001 New Zealand, and ³Department of Otolaryngology, Osaka University Medical School, Osaka, 565-0871 Japan

The hippocampus is thought to be important for spatial representation processes that depend on the integration of both self-movement and allocentric cues. The vestibular system is a particularly important source of self-movement information that may contribute to this spatial representation. To test the hypothesis that the vestibular system provides self-movement information to the hippocampus, rats were given either a bilateral labyrinthectomy (n = 6) or a sham surgery (n = 6), and at least 60 d after surgery hippocampal CA1 neurons were recorded extracellularly while the animals foraged freely in an open arena. Recorded cells were classified as complex spiking (n = 80) or noncomplex spiking (n = 33) neurons, and their spatial firing fields (place fields) were examined. The most striking effect of the lesion was that it appeared to completely abolish location-related firing. The results of this and previous studies provide converging evidence demonstrating that vestibular information is processed by the hippocampus. The disruption of the vestibular input to the hippocampus may interfere with the reconciliation of internal self-movement signals with the changes to the external sensory inputs that occur as a result of that movement. This would disrupt the ability of the animal to integrate allocentric and egocentric information into a coherent representation of space.

Key words: hippocampus; vestibular; labyrinthectomy; place cell; place field; self-motion; compensation; navigation

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Received Jan. 8, 2003; revised May. 5, 2003; accepted May. 7, 2003.

This article has been cited by other articles:

				K Jauregui-Renaud, F Y P Sang, M A Gresty, D A Green, and A M Bronstein Depersonalisation/derealisation symptoms and updating orientation in patients with vestibular disease J. Neurol. Neurosurg. Psychiatry, March 1, 2008; 79(3): 276 - 283. [Abstract] [Full Text] [PDF]

				N. A. Russell, A. Horii, P. F. Smith, C. L. Darlington, and D. K. Bilkey Lesions of the vestibular system disrupt hippocampal theta rhythm in the rat. J Neurophysiol, July 1, 2006; 96(1): 4 - 14. [Abstract] [Full Text] [PDF]

				T. Brandt, F. Schautzer, D. A. Hamilton, R. Bruning, H. J. Markowitsch, R. Kalla, C. Darlington, P. Smith, and M. Strupp Vestibular loss causes hippocampal atrophy and impaired spatial memory in humans Brain, November 1, 2005; 128(11): 2732 - 2741. [Abstract] [Full Text] [PDF]

				B. L. Day and R. C. Fitzpatrick Virtual head rotation reveals a process of route reconstruction from human vestibular signals J. Physiol., September 1, 2005; 567(2): 591 - 597. [Abstract] [Full Text] [PDF]

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