Vestibular loss causes hippocampal atrophy and impaired spatial memory in humans. Brain

Department of Neurology, Ludwig-Maximilians University, Munich, Germany.
Brain (Impact Factor: 9.2). 12/2005; 128(Pt 11):2732-41. DOI: 10.1093/brain/awh617
Source: PubMed


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.

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Available from: Derek A Hamilton
    • "On the other hand, we cannot rule out that a decreased visual recognition memory deficit accounts for the significant interaction. However, in contrast to spatial memory deficits (Brandt et al., 2005), visual memory deficits have not yet been described in BVF patients and BVF patients in our study showed no visual memory impairment compared to controls. BVF patients rather show increased visual dependence during spatial orientation and navigation as they stronger rely on proprioceptive and visual cues and their interaction (Cutfield et al., 2014). "
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    ABSTRACT: Spatial orientation and navigation depends on information from the vestibular system. Previous work suggested impaired spatial navigation in patients with bilateral vestibular failure (BVF). The aim of this study was to investigate event-related brain activity (fMRI) during spatial navigation and visual memory tasks in BVF patients. Twenty-three BVF patients and healthy age-and gender matched control subjects performed learning sessions of spatial navigation by watching short films taking them through various streets from a driver's perspective along a route to the Cathedral of Cologne using virtual reality videos (adopted and modified from Google Earth(®)). In the MRI scanner, participants were asked to respond to questions testing for visual memory or spatial navigation while they viewed short video clips. From a similar but not identical perspective depicted video frames of routes were displayed which they had previously seen or which were completely novel to them. Compared with controls, posterior cerebellar activity in BVF patients was higher during spatial navigation than during visual memory tasks, in the absence of performance differences. This cerebellar activity correlated with disease duration. Cerebellar activity during spatial navigation in BVF patients may reflect increased non-vestibular efforts to counteract the development of spatial navigation deficits in BVF. Conceivably, cerebellar activity indicates a change in navigational strategy of BVF patients, i.e. from a more allocentric, landmark or place -based strategy (hippocampus) to a more sequence-based strategy. This interpretation would be in accord with recent evidence for a cerebellar role in sequence-based navigation. Copyright © 2015. Published by Elsevier Ltd.
    No preview · Article · Aug 2015 · Neuroscience
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    • "Despite this, LTP appears to be normal. It appears to date as if the hippocampal atrophy that has been documented in humans with bilateral vestibular loss by Brandt et al. (2005) does not occur in rats; whether this is due to the hyperactivity that occurs in BVD rats is unknown, but more subtle changes in dendritic length appear to occur. At present, there are too few studies of neurochemical changes in the hippocampus following BVD to be certain of how glutamate receptors and other receptors are affected. "
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    ABSTRACT: Our studies conducted over the last 14 years have demonstrated that a complete bilateral vestibular deafferentation (BVD) in rats results in spatial memory deficits in a variety of behavioural tasks, such as the radial arm maze, the foraging task and the spatial T maze, as well as deficits in other tasks such as the five-choice serial reaction time task (5-CSRT task) and object recognition memory task. These deficits persist long after the BVD, and are not simply attributable to ataxia, anxiety, hearing loss or hyperactivity. In tasks such as the foraging task, the spatial memory deficits are evident in darkness when vision is not required to perform the task. The deficits in the radial arm maze, the foraging task and the spatial T maze, in particular, suggest hippocampal dysfunction following BVD, and this is supported by the finding that both hippocampal place cells and theta rhythm are dysfunctional in BVD rats. Now that it is clear that the hippocampus is adversely affected by BVD, the next challenge is to determine what vestibular information is transmitted to it and how that information is used by the hippocampus and the other brain structures with which it interacts.
    Full-text · Article · Jul 2015 · Multisensory research
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    • "The virtual Morris maze is also commonly used in humans to investigate changes due to diseases of the central nervous system involving mostly the hippocampal formation. Spatial navigation in this task is impaired in patients after the first episode of schizophrenia[15]and in patients affected by major depression[12]and by vestibular disorders[8], with hippocampal damage[3,20]or following traumatic brain injury[46]. As for ethanol related diseases children with Fetal Alcohol Syndrome are impaired at place learning but not in cued- navigation[23]. "
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    ABSTRACT: Alcohol dependence is a major public health problem worldwide. Brain and behavioral disruptions including changes in cognitive abilities are common features of alcohol addiction. Thus, the present study was aimed to investigate spatial learning and memory in 29 alcoholic men undergoing alcohol detoxification by using a virtual Morris maze task. As age-matched controls we recruited 29 men among occasional drinkers without history of alcohol dependence and/or alcohol related diseases and with a negative blood alcohol level at the time of testing. We found that the responses to the virtual Morris maze are impaired in men undergoing alcohol detoxification. Notably they showed increased latencies in the first movement during the trials, increased latencies in retrieving the hidden platform and increased latencies in reaching the visible platform. These findings were associated with reduced swimming time in the target quadrant of the pool where the platform had been during the 4 hidden platform trials of the learning phase compared to controls. Such increasing latency responses may suggest motor control, attentional and motivational deficits due to alcohol detoxification.
    Full-text · Article · Jul 2015 · Physiology & Behavior
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