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      Noisy galvanic vestibular stimulation modulates spatial memory in young healthy adults

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          Abstract

          Hippocampal and striatal circuits play important roles in spatial navigation. These regions integrate environmental information and receive intrinsic afferent inputs from the vestibular system. Past research indicates that galvanic vestibular stimulation (GVS) is a non-invasive technique that modulates hippocampal and striatal activities. There are also evidences for enhanced motor and cognitive functions through GVS. This study extends previous research to investigate whether noisy GVS may improve hippocampal- and striatal-associated aspects of spatial navigation performance. Using a virtual navigation task, we examined effects of noisy GVS on spatial learning and memory. To probe the participants’ sensitivity to hippocampal- or striatal-associated spatial information, we either enlarged the virtual environment’s boundary or replaced an intra-environmental location cue, respectively. Noisy GVS or sham stimulation was applied online during the learning phase in a within-subject crossover design. The results showed that noisy GVS enhanced spatial learning and the sensitivity foremost to hippocampal-dependent spatial information both in males and females. Individual differences in spatial working memory capacity moderated the effects of GVS, with individuals with lower capacity benefitting more from the stimulation. Furthermore, sex-related differences in GVS effects on the two forms of spatial representations may reflect differences between males and females in preferred spatial strategies.

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          Most cited references43

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

            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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              Parallel striatal and hippocampal systems for landmarks and boundaries in spatial memory.

              How the memory systems centered on the hippocampus and dorsal striatum interact to support behavior remains controversial. We used functional MRI while people learned the locations of objects by collecting and replacing them over multiple trials within a virtual environment comprising a landmark, a circular boundary, and distant cues for orientation. The relative location of landmark and boundary was occasionally changed, with specific objects paired with one or other cue, allowing dissociation of learning and performance relative to either cue. Right posterior hippocampal activation reflected learning and remembering of boundary-related locations, whereas right dorsal striatal activation reflected learning and remembering of landmark-related locations. Within the right hippocampus, anterior processing of environmental change (spatial novelty) was dissociated from posterior processing of location. Behavioral studies show that landmark-related learning obeys associative reinforcement, whereas boundary-related learning is incidental [Doeller CF, Burgess N (2008) Proc Natl Acad Sci USA 105:5909-5914]. The distinct incidental hippocampal processing of boundaries is suggestive of a "geometric module" or "cognitive map" and may explain the hippocampal support of incidental/observational learning in "declarative" or "episodic" memory versus the striatal support of trial-and-error learning in "procedural" memory. Finally, the hippocampal and striatal systems appear to combine "bottom-up," simply influencing behavior proportional to their activations, without direct interaction, with "top-down" ventromedial prefrontal involvement when both are similarly active.
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                Author and article information

                Contributors
                danica.hilliard@dzne.de
                shu-chen.li@tu-dresden.de
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                27 June 2019
                27 June 2019
                2019
                : 9
                : 9310
                Affiliations
                [1 ]ISNI 0000 0004 0438 0426, GRID grid.424247.3, German Center for Neurodegenerative Diseases (DZNE), ; D-01307 Dresden, Germany
                [2 ]ISNI 0000 0001 2111 7257, GRID grid.4488.0, CRTD – Center for Regenerative Therapies Dresden, , Technische Universität Dresden, ; D-01307 Dresden, Germany
                [3 ]ISNI 0000 0001 2111 7257, GRID grid.4488.0, Faculty of Psychology, Chair of Lifespan Developmental Neuroscience, , Technische Universität Dresden, ; D-01069 Dresden, Germany
                [4 ]ISNI 0000 0000 9859 7917, GRID grid.419526.d, Max Planck Research Group NeuroCode, , Max Planck Institute for Human Development, ; D-14195 Berlin, Germany
                [5 ]ISNI 0000 0001 2111 7257, GRID grid.4488.0, CeTI – Centre for Tactile Internet with Human-in-the-Loop, , Technische Universität Dresden, ; D-01069 Dresden, Germany
                Author information
                http://orcid.org/0000-0003-3315-0550
                http://orcid.org/0000-0001-8409-5390
                Article
                45757
                10.1038/s41598-019-45757-0
                6597709
                31249334
                cd65e2d2-5b37-43fc-ac53-d50b1363823c
                © The Author(s) 2019

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 16 May 2018
                : 14 June 2019
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                © The Author(s) 2019

                Uncategorized
                cognitive neuroscience,human behaviour
                Uncategorized
                cognitive neuroscience, human behaviour

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