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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    • "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.
    Neuroscience 08/2015; 305. DOI:10.1016/j.neuroscience.2015.07.089 · 3.36 Impact Factor
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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.
    Multisensory research 07/2015; 28(5-6):461-485. DOI:10.1163/22134808-00002469 · 0.78 Impact Factor
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    • "Patients with bilateral vestibulopathy have significant deficits of spatial memory and navigation (tested with a virtual variant of the Morris water task) as well as atrophy of the hippocampus (Brandt et al., 2005), but the rest of their memory functions are not affected. The latter was tested by the Wechsler Memory Scale-Revised in full which constitutes the most universally employed memory test battery (Brandt et al., 2005). Patients with unilateral labyrinthine failure, however, do not have significant disorders of spatial memory or atrophy of the hippocampus (Hüfner et al., 2007). "
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    ABSTRACT: Background: Vestibular disorders are commonly characterized by a combination of perceptual, ocular motor, postural, and vegetative manifestations, which cause the symptoms of vertigo, nystagmus, ataxia, and nausea. Multisensory convergence and numerous polysynaptic pathways link the bilaterally organized central vestibular network with limbic, hippocampal, cerebellar, and non-vestibular cortex structures to mediate "higher" cognitive functions. Anatomical classification of vestibular disorders: The traditional classification of vestibular disorders is based on the anatomical site of the lesion. While it distinguishes between the peripheral and the central vestibular systems, certain weaknesses become apparent when applied clinically. There are two reasons for this: first, peripheral and central vestibular disorders cannot always be separated by the clinical syndrome; second, a third category, namely disorders of "higher vestibular function", is missing. These disorders may be caused by peripheral as well as central vestibular lesions. Functional classification: Here we discuss a new concept of disorders of higher vestibular function which involve cognition and more than one sensory modality. Three conditions are described that exemplify such higher disorders: room tilt illusion, spatial hemineglect, and bilateral vestibulopathy all of which present with deficits of orientation and spatial memory. Conclusions: Further elaboration of such disorders of higher multisensory functions with respect to lesion site and symptomatology is desirable. The room tilt illusion and spatial hemineglect involve vestibular and visual function to the extent that both conditions can be classified as either disorders of higher vestibular or of higher visual functions. A possible way of separating these disorders in a first step is to determine whether the causative lesion site affects the vestibular or the visual system. For the vestibular system this lesion site may be peripheral or central. The criterion of "higher function" is fulfilled if cognition or senses other than the primarily affected one come into play.
    Frontiers in Integrative Neuroscience 06/2014; 8:47. DOI:10.3389/fnint.2014.00047
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