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Brain Advance Access originally published online on September 1, 2005
Brain 2005 128(11):2732-2741; doi:10.1093/brain/awh617
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© The Author (2005). Published by Oxford University Press on behalf of the Guarantors of Brain. All rights reserved. For Permissions, please e-mail: journals.permissions@oxfordjournals.org

Vestibular loss causes hippocampal atrophy and impaired spatial memory in humans

Thomas Brandt1, Franz Schautzer2, Derek A. Hamilton3, Roland Brüning4, Hans J. Markowitsch5, Roger Kalla1, Cynthia Darlington6, Paul Smith6 and Michael Strupp1

1 Department of Neurology, Ludwig-Maximilians University, Munich, Germany, 2 Department of Neurology and Psychosomatics, LKH Villach, Austria, 3 Department of Psychology, University of New Mexico, Albuquerque, USA, 4 Department of Neuroradiology, Ludwig-Maximilians University, Munich, Germany, 5 Physiological Psychology, University of Bielefeld, Bielefeld, Germany and 6 Department of Pharmacology and Toxicology, School of Medical Sciences, University of Otago Medical School, Dunedin, New Zealand

Correspondence to: Thomas Brandt, MD, FRCP, Department of Neurology, Ludwig-Maximilians University, D-81377 Munich, Germany E-mail: Thomas.Brandt{at}med.uni-muenchen.de

The human hippocampal formation plays a crucial role in various aspects of memory processing. Most literature on the human hippocampus stresses its non-spatial memory functions, but older work in rodents and some other species emphasized the role of the hippocampus in spatial learning and memory as well. A few human studies also point to a direct relation between hippocampal size, navigation and spatial memory. Conversely, the importance of the vestibular system for navigation and spatial memory was until now convincingly demonstrated only in animals. Using magnetic resonance imaging volumetry, we found that patients (n = 10) with acquired chronic bilateral vestibular loss (BVL) develop a significant selective atrophy of the hippocampus (16.9% decrease relative to controls). When tested with a virtual variant (on a PC) of the Morris water task these patients exhibited significant spatial memory and navigation deficits that closely matched the pattern of hippocampal atrophy. These spatial memory deficits were not associated with general memory deficits. The current data on BVL patients and bilateral hippocampal atrophy revive the idea that a major—and probably phylogenetically ancient—function of the archicortical hippocampal tissue is still evident in spatial aspects of memory processing for navigation. Furthermore, these data demonstrate for the first time in humans that spatial navigation critically depends on preserved vestibular function, even when the subjects are stationary, e.g. without any actual vestibular or somatosensory stimulation.

Key Words: hippocampus; bilateral vestibular failure; spatial memory; navigation

Abbreviations: BVL = bilateral vestibular loss; VMWT = virtual Morris water task; GM = grey matter; WM = white matter

Received December 17, 2004. Revised July 18, 2005. Accepted July 26, 2005.


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