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      Decoding Neuronal Ensembles in the Human Hippocampus

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          Summary

          Background

          The hippocampus underpins our ability to navigate, to form and recollect memories, and to imagine future experiences. How activity across millions of hippocampal neurons supports these functions is a fundamental question in neuroscience, wherein the size, sparseness, and organization of the hippocampal neural code are debated.

          Results

          Here, by using multivariate pattern classification and high spatial resolution functional MRI, we decoded activity across the population of neurons in the human medial temporal lobe while participants navigated in a virtual reality environment. Remarkably, we could accurately predict the position of an individual within this environment solely from the pattern of activity in his hippocampus even when visual input and task were held constant. Moreover, we observed a dissociation between responses in the hippocampus and parahippocampal gyrus, suggesting that they play differing roles in navigation.

          Conclusions

          These results show that highly abstracted representations of space are expressed in the human hippocampus. Furthermore, our findings have implications for understanding the hippocampal population code and suggest that, contrary to current consensus, neuronal ensembles representing place memories must be large and have an anisotropic structure.

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          Most cited references30

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          Episodic memory: from mind to brain.

          Episodic memory is a neurocognitive (brain/mind) system, uniquely different from other memory systems, that enables human beings to remember past experiences. The notion of episodic memory was first proposed some 30 years ago. At that time it was defined in terms of materials and tasks. It was subsequently refined and elaborated in terms of ideas such as self, subjective time, and autonoetic consciousness. This chapter provides a brief history of the concept of episodic memory, describes how it has changed (indeed greatly changed) since its inception, considers criticisms of it, and then discusses supporting evidence provided by (a) neuropsychological studies of patterns of memory impairment caused by brain damage, and (b) functional neuroimaging studies of patterns of brain activity of normal subjects engaged in various memory tasks. I also suggest that episodic memory is a true, even if as yet generally unappreciated, marvel of nature.
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            Information-based functional brain mapping.

            The development of high-resolution neuroimaging and multielectrode electrophysiological recording provides neuroscientists with huge amounts of multivariate data. The complexity of the data creates a need for statistical summary, but the local averaging standardly applied to this end may obscure the effects of greatest neuroscientific interest. In neuroimaging, for example, brain mapping analysis has focused on the discovery of activation, i.e., of extended brain regions whose average activity changes across experimental conditions. Here we propose to ask a more general question of the data: Where in the brain does the activity pattern contain information about the experimental condition? To address this question, we propose scanning the imaged volume with a "searchlight," whose contents are analyzed multivariately at each location in the brain.
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              A cortical representation of the local visual environment.

              Medial temporal brain regions such as the hippocampal formation and parahippocampal cortex have been generally implicated in navigation and visual memory. However, the specific function of each of these regions is not yet clear. Here we present evidence that a particular area within human parahippocampal cortex is involved in a critical component of navigation: perceiving the local visual environment. This region, which we name the 'parahippocampal place area' (PPA), responds selectively and automatically in functional magnetic resonance imaging (fMRI) to passively viewed scenes, but only weakly to single objects and not at all to faces. The critical factor for this activation appears to be the presence in the stimulus of information about the layout of local space. The response in the PPA to scenes with spatial layout but no discrete objects (empty rooms) is as strong as the response to complex meaningful scenes containing multiple objects (the same rooms furnished) and over twice as strong as the response to arrays of multiple objects without three-dimensional spatial context (the furniture from these rooms on a blank background). This response is reduced if the surfaces in the scene are rearranged so that they no longer define a coherent space. We propose that the PPA represents places by encoding the geometry of the local environment.
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                Author and article information

                Contributors
                Journal
                Curr Biol
                Current Biology
                Cell Press
                0960-9822
                1879-0445
                14 April 2009
                14 April 2009
                : 19
                : 7-3
                : 546-554
                Affiliations
                [1 ]Wellcome Trust Centre for Neuroimaging, Institute of Neurology, University College London, 12 Queen Square, London WC1N 3BG, UK
                [2 ]Institute of Cognitive Neuroscience, University College London, 17 Queen Square, London WC1N 3AR, UK
                [3 ]Lionhead Studios, 1 Occam Court, Surrey Research Park, Guildford, Surrey GU2 7YQ, UK
                Author notes
                []Corresponding author d.hassabis@ 123456fil.ion.ucl.ac.uk
                [∗∗ ]Corresponding author e.maguire@ 123456fil.ion.ucl.ac.uk
                Article
                CURBIO7109
                10.1016/j.cub.2009.02.033
                2670980
                19285400
                1654522b-8434-47d7-bc1d-a78c199fe0e0
                © 2009 ELL & Excerpta Medica.

                This document may be redistributed and reused, subject to certain conditions.

                History
                : 22 October 2008
                : 27 January 2009
                : 10 February 2009
                Categories
                Article

                Life sciences
                sysneuro
                Life sciences
                sysneuro

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