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      From ear to uncertainty: vestibular contributions to cognitive function

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          Abstract

          In addition to the deficits in the vestibulo-ocular and vestibulo-spinal reflexes that occur following vestibular dysfunction, there is substantial evidence that vestibular loss also causes cognitive disorders, some of which may be due to the reflexive deficits and some of which are related to the role that ascending vestibular pathways to the limbic system and neocortex play in spatial orientation. In this review we summarize the evidence that vestibular loss causes cognitive disorders, especially spatial memory deficits, in animals and humans and critically evaluate the evidence that these deficits are not due to hearing loss, problems with motor control, oscillopsia or anxiety and depression. We review the evidence that vestibular lesions affect head direction and place cells as well as the emerging evidence that artificial activation of the vestibular system, using galvanic vestibular stimulation (GVS), can modulate cognitive function.

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          Most cited references141

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          Path integration and the neural basis of the 'cognitive map'.

          The hippocampal formation can encode relative spatial location, without reference to external cues, by the integration of linear and angular self-motion (path integration). Theoretical studies, in conjunction with recent empirical discoveries, suggest that the medial entorhinal cortex (MEC) might perform some of the essential underlying computations by means of a unique, periodic synaptic matrix that could be self-organized in early development through a simple, symmetry-breaking operation. The scale at which space is represented increases systematically along the dorsoventral axis in both the hippocampus and the MEC, apparently because of systematic variation in the gain of a movement-speed signal. Convergence of spatially periodic input at multiple scales, from so-called grid cells in the entorhinal cortex, might result in non-periodic spatial firing patterns (place fields) in the hippocampus.
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            Regional dissociations within the hippocampus--memory and anxiety.

            The amnestic effects of hippocampal lesions are well documented, leading to numerous memory-based theories of hippocampal function. It is debatable, however, whether any one of these theories can satisfactorily account for all the consequences of hippocampal damage: Hippocampal lesions also result in behavioural disinhibition and reduced anxiety. A growing number of studies now suggest that these diverse behavioural effects may be associated with different hippocampal subregions. There is evidence for at least two distinct functional domains, although recent neuroanatomical studies suggest this may be an underestimate. Selective lesion studies show that the hippocampus is functionally subdivided along the septotemporal axis into dorsal and ventral regions, each associated with a distinct set of behaviours. Dorsal hippocampus has a preferential role in certain forms of learning and memory, notably spatial learning, but ventral hippocampus may have a preferential role in brain processes associated with anxiety-related behaviours. The latter's role in emotional processing is also distinct from that of the amygdala, which is associated specifically with fear. Gray and McNaughton's theory can in principle incorporate these apparently distinct hippocampal functions, and provides a plausible unitary account for the multiple facets of hippocampal function.
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              Stochastic resonance and sensory information processing: a tutorial and review of application.

              To review the stochastic resonance phenomena observed in sensory systems and to describe how a random process ('noise') added to a subthreshold stimulus can enhance sensory information processing and perception. Nonlinear systems need a threshold, subthreshold information bearing stimulus and 'noise' for stochastic resonance phenomena to occur. These three ingredients are ubiquitous in nature and man-made systems, which accounts for the observation of stochastic resonance in fields and conditions ranging from physics and engineering to biology and medicine. The stochastic resonance paradigm is compatible with single-neuron models or synaptic and channels properties and applies to neuronal assemblies activated by sensory inputs and perceptual processes as well. Here we review a few of the landmark experiments (including psychophysics, electrophysiology, fMRI, human vision, hearing and tactile functions, animal behavior, single/multiunit activity recordings). Models and experiments show a peculiar consistency with known neuronal and brain physiology. A number of naturally occurring 'noise' sources in the brain (e.g. synaptic transmission, channel gating, ion concentrations, membrane conductance) possibly accounting for stochastic resonance phenomena are also reviewed. Evidence is given suggesting a possible role of stochastic resonance in brain function, including detection of weak signals, synchronization and coherence among neuronal assemblies, phase resetting, 'carrier' signals, animal avoidance and feeding behaviors. Stochastic resonance is a ubiquitous and conspicuous phenomenon compatible with neural models and theories of brain function. The available evidence suggests cautious interpretation, but justifies research and should encourage neuroscientists and clinical neurophysiologists to explore stochastic resonance in biology and medical science.
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                Author and article information

                Journal
                Front Integr Neurosci
                Front Integr Neurosci
                Front. Integr. Neurosci.
                Frontiers in Integrative Neuroscience
                Frontiers Media S.A.
                1662-5145
                13 September 2013
                26 November 2013
                2013
                : 7
                : 84
                Affiliations
                Department Pharmacology and Toxicology, School of Medical Sciences, and the Brain Health Research Centre, University of Otago Dunedin, New Zealand
                Author notes

                Edited by: Stephane Besnard, INSERM U1075, France

                Reviewed by: Alberto E. Pereda, Albert Einstein College of Medicine of Yeshiva University, USA; Stephane Besnard, INSERM U1075, France

                *Correspondence: Paul F. Smith, Department Pharmacology and Toxicology, School of Medical Sciences, and the Brain Health Research Centre, University of Otago, Frederick St., 9045, Dunedin, New Zealand e-mail: paul.smith@ 123456stonebow.otago.ac.nz

                This article was submitted to the journal Frontiers in Integrative Neuroscience.

                Article
                10.3389/fnint.2013.00084
                3840327
                23355815
                f824b610-af04-4123-95b4-90e7a5a77663
                Copyright © 2013 Smith and Zheng.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 01 August 2013
                : 07 November 2013
                Page count
                Figures: 10, Tables: 0, Equations: 0, References: 153, Pages: 13, Words: 11268
                Categories
                Neuroscience
                Review Article

                Neurosciences
                spatial memory,vestibular lesions,vestibular,cognition,hippocampus
                Neurosciences
                spatial memory, vestibular lesions, vestibular, cognition, hippocampus

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