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

Department of Neurology, Ludwig-Maximilians University, Munich, Germany.
Brain (Impact Factor: 10.23). 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, Aug 17, 2015
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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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    • "Presumably, the intrinsic stimulus during physical activity essentially consists of proprioception and vision. Likewise, there are numerous reports on links between the vestibular system and hippocampal function [(Brandt et al. 2005); see Ref. Smith et al. (2010) for review] even though effects on adult neurogenesis have not yet been specifically addressed. In order to identify relevant sensory stimuli independent of locomotion , we here focused on auditory input as a potential signal to affect adult hippocampal neurogenesis. "
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    ABSTRACT: We have previously hypothesized that the reason why physical activity increases precursor cell proliferation in adult neurogenesis is that movement serves as non-specific signal to evoke the alertness required to meet cognitive demands. Thereby a pool of immature neurons is generated that are potentially recruitable by subsequent cognitive stimuli. Along these lines, we here tested whether auditory stimuli might exert a similar non-specific effect on adult neurogenesis in mice. We used the standard noise level in the animal facility as baseline and compared this condition to white noise, pup calls, and silence. In addition, as patterned auditory stimulus without ethological relevance to mice we used piano music by Mozart (KV 448). All stimuli were transposed to the frequency range of C57BL/6 and hearing was objectified with acoustic evoked potentials. We found that except for white noise all stimuli, including silence, increased precursor cell proliferation (assessed 24 h after labeling with bromodeoxyuridine, BrdU). This could be explained by significant increases in BrdU-labeled Sox2-positive cells (type-1/2a). But after 7 days, only silence remained associated with increased numbers of BrdU-labeled cells. Compared to controls at this stage, exposure to silence had generated significantly increased numbers of BrdU/NeuN-labeled neurons. Our results indicate that the unnatural absence of auditory input as well as spectrotemporally rich albeit ethological irrelevant stimuli activate precursor cells-in the case of silence also leading to greater numbers of newborn immature neurons-whereas ambient and unstructured background auditory stimuli do not.
    Brain Structure and Function 12/2013; DOI:10.1007/s00429-013-0679-3 · 4.57 Impact Factor
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    • "Indeed, although incorporating only a small sample, Soza Ried and Aviles (2007) found that the vestibular system of people suffering from depression is functionally affected in the sense that they have a hypoactive right vestibular nucleus. Interestingly, not only depressed subjects display reduced hippocampus volume size (McKinnon et al., 2009), patients with vestibular dysfunction also do so (Brandt et al., 2005; Smith et al., 2005) and this leads to disturbed cognitive function in both groups. Physiotherapeutic vestibular rehabilitation has been reported to alleviate symptoms of anxiety and depression (Whitney et al., 2005; Meli et al., 2007). "
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    ABSTRACT: We are familiar with both pleasant and unpleasant psychotropic effects of movements associated with vestibular stimulation. However, there has been no attempt to scientifically explore the impact of different kinds of vestibular stimulation on mood states and biomarkers. A sample of 23 healthy volunteers were subjected to a random sequence of three different passive rotational (yaw, pitch, roll) and translational (heave, sway, surge) vestibular stimulation paradigms using a motion-simulator (hexapod). Mood states were measured by means of questionnaires and visual analog scales. In addition, saliva cortisol and α-amylase samples were taken. Compared to a subliminal control paradigm all rotational and two translational stimulations produced significant changes in mood states: Yaw rotation was associated with feeling more comfortable, pitch rotation with feeling more alert and energetic, and roll rotation with feeling less comfortable. Heave translation was associated with feeling more alert, less relaxed, and less comfortable and surge translation with feeling more alert. Biomarkers were not affected. In conclusion, we provide first experimental evidence that passive rotational and translational movements may influence mood states on a short-term basis and that the quality of these psychotropic effects may depend on the plane and axis of the respective movements.
    Frontiers in Psychology 11/2012; 3:499. DOI:10.3389/fpsyg.2012.00499 · 2.80 Impact Factor
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