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

ABSTRACT 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, Sep 29, 2015
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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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    • "To test topographical memory, three tests were used: the Camden Topographical Recognition Memory Test (CTRMT), a computerized topographical mental rotation test (TMRT) similar to the “four mountains” test used by Bird et al. (2010) and Hartley and Harlow (2012), and a virtual version of the widely used Morris water maze used in animals (Sharma et al., 2010) and humans (e.g., Moffat and Resnick, 2002; Brandt et al., 2005). While the CTRMT has not been specifically linked to hippocampal function, scene memory in general has been linked to the hippocampus (Epstein and Kanwisher, 1998; Arcaro et al., 2009; Bonnici et al., 2012). "
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    ABSTRACT: Research during the past two decades has demonstrated an important role of the vestibular system in topographical orientation and memory and the network of neural structures associated with them. Almost all of the supporting data have come from animal or human clinical studies, however. The purpose of the present study was to investigate the link between vestibular function and topographical memory in normal elderly humans. Twenty-five participants aged 70 to 85 years who scored from mildly impaired to normal on the Montreal Cognitive Assessment (MoCA) received three topographical memory tests: the Camden Topographical Recognition Memory Test (CTMRT), a computerized topographical mental rotation test (TMRT), and a virtual pond maze (VPM). They also received six vestibular or oculomotor tests: optokinetic nystagmus (OKN), visual pursuit (VP), actively generated vestibulo-ocular reflex (VOR), the sensory orientation test (SOT) for posture, and two measures of rotational memory (error in degrees, or RM°, and correct directional recognition, or RM→). The only significant bivariate correlations were among the three vestibular measures primarily assessing horizontal canal function (VOR, RM°, and RM→). A multiple regression analysis showed significant relationships between vestibular and demographic predictors and both the TMRT (R = 0.78) and VPM (R = 0.66) measures. The significant relationship between the vestibular and topographical memory measures supports the theory that vestibular loss may contribute to topographical memory impairment in the elderly.
    Frontiers in Integrative Neuroscience 06/2014; 8:46. DOI:10.3389/fnint.2014.00046
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    • "It is likely that participants imagined self-motion by means of visual flow, and, indeed, there was a deactivation of vestibular areas such as the inferior parietal lobule during imagery. Vestibular deactivation has been reported repeatedly during visually induced self-motion (e.g., Brandt et al., 2002). This discrepancy illustrates that subtle changes in how people perform mental imagery tasks can substantially change brain activation, and it will be a challenge for future research to narrow down the cognitive processes. "
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    ABSTRACT: A growing number of studies in humans demonstrate the involvement of vestibular information in tasks that are seemingly remote from well-known functions such as space constancy or postural control. In this review article we point out three emerging streams of research highlighting the importance of vestibular input: (1) Spatial Cognition: Modulation of vestibular signals can induce specific changes in spatial cognitive tasks like mental imagery and the processing of numbers. This has been shown in studies manipulating body orientation (changing the input from the otoliths), body rotation (changing the input from the semicircular canals), in clinical findings with vestibular patients, and in studies carried out in microgravity. There is also an effect in the reverse direction; top-down processes can affect perception of vestibular stimuli. (2) Body Representation: Numerous studies demonstrate that vestibular stimulation changes the representation of body parts, and sensitivity to tactile input or pain. Thus, the vestibular system plays an integral role in multisensory coordination of body representation. (3) Affective Processes and Disorders: Studies in psychiatric patients and patients with a vestibular disorder report a high comorbidity of vestibular dysfunctions and psychiatric symptoms. Recent studies investigated the beneficial effect of vestibular stimulation on psychiatric disorders, and how vestibular input can change mood and affect. These three emerging streams of research in vestibular science are-at least in part-associated with different neuronal core mechanisms. Spatial transformations draw on parietal areas, body representation is associated with somatosensory areas, and affective processes involve insular and cingulate cortices, all of which receive vestibular input. Even though a wide range of different vestibular cortical projection areas has been ascertained, their functionality still is scarcely understood.
    Frontiers in Integrative Neuroscience 05/2014; 8:44. DOI:10.3389/fnint.2014.00044
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