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      Connecting multiple spatial scales to decode the population activity of grid cells

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          Abstract

          Reading the neural code for space: discrete scales of grid-cell activity enable goal-directed navigation and localization.

          Abstract

          Mammalian grid cells fire when an animal crosses the points of an imaginary hexagonal grid tessellating the environment. We show how animals can navigate by reading out a simple population vector of grid cell activity across multiple spatial scales, even though neural activity is intrinsically stochastic. This theory of dead reckoning explains why grid cells are organized into discrete modules within which all cells have the same lattice scale and orientation. The lattice scale changes from module to module and should form a geometric progression with a scale ratio of around 3/2 to minimize the risk of making large-scale errors in spatial localization. Such errors should also occur if intermediate-scale modules are silenced, whereas knocking out the module at the smallest scale will only affect spatial precision. For goal-directed navigation, the allocentric grid cell representation can be readily transformed into the egocentric goal coordinates needed for planning movements. The goal location is set by nonlinear gain fields that act on goal vector cells. This theory predicts neural and behavioral correlates of grid cell readout that transcend the known link between grid cells of the medial entorhinal cortex and place cells of the hippocampus.

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          Microstructure of a spatial map in the entorhinal cortex.

          The ability to find one's way depends on neural algorithms that integrate information about place, distance and direction, but the implementation of these operations in cortical microcircuits is poorly understood. Here we show that the dorsocaudal medial entorhinal cortex (dMEC) contains a directionally oriented, topographically organized neural map of the spatial environment. Its key unit is the 'grid cell', which is activated whenever the animal's position coincides with any vertex of a regular grid of equilateral triangles spanning the surface of the environment. Grids of neighbouring cells share a common orientation and spacing, but their vertex locations (their phases) differ. The spacing and size of individual fields increase from dorsal to ventral dMEC. The map is anchored to external landmarks, but persists in their absence, suggesting that grid cells may be part of a generalized, path-integration-based map of the spatial environment.
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            Representation of geometric borders in the entorhinal cortex.

            We report the existence of an entorhinal cell type that fires when an animal is close to the borders of the proximal environment. The orientation-specific edge-apposing activity of these "border cells" is maintained when the environment is stretched and during testing in enclosures of different size and shape in different rooms. Border cells are relatively sparse, making up less than 10% of the local cell population, but can be found in all layers of the medial entorhinal cortex as well as the adjacent parasubiculum, often intermingled with head-direction cells and grid cells. Border cells may be instrumental in planning trajectories and anchoring grid fields and place fields to a geometric reference frame.
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              Choice-specific sequences in parietal cortex during a virtual-navigation decision task

              The posterior parietal cortex (PPC) plays an important role in many cognitive behaviors; however, the neural circuit dynamics underlying PPC function are not well understood. Here we optically imaged the spatial and temporal activity patterns of neuronal populations in mice performing a PPC-dependent task that combined a perceptual decision and memory-guided navigation in a virtual environment. Individual neurons had transient activation staggered relative to one another in time, forming a sequence of neuronal activation spanning the entire length of a task trial. Distinct sequences of neurons were triggered on trials with opposite behavioral choices and defined divergent, choice-specific trajectories through a state space of neuronal population activity. Cells participating in the different sequences and at distinct time points in the task were anatomically intermixed over microcircuit length scales (< 100 micrometers). During working memory decision tasks the PPC may therefore perform computations through sequence-based circuit dynamics, rather than long-lived stable states, implemented using anatomically intermingled microcircuits.
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                Author and article information

                Journal
                Sci Adv
                Sci Adv
                SciAdv
                advances
                Science Advances
                American Association for the Advancement of Science
                2375-2548
                December 2015
                18 December 2015
                : 1
                : 11
                : e1500816
                Affiliations
                [1 ]Bernstein Center for Computational Neuroscience Munich and Department of Biology II, Ludwig-Maximilians-Universität München, Grosshadernerstrasse 2, 82152 Planegg-Martinsried, Germany.
                [2 ]Department of Molecular and Cellular Biology and Center for Brain Science, Harvard University, 16 Divinity Avenue, Cambridge, MA 02138, USA.
                Author notes
                [*]

                These authors contributed equally to this work.

                []Corresponding author. E-mail: herz@ 123456bio.lmu.de
                Author information
                http://orcid.org/0000-0002-3777-2202
                http://orcid.org/0000-0002-3836-565X
                Article
                1500816
                10.1126/science.1500816
                4730856
                26824061
                529a00c8-28d5-4ac4-985f-069fe4a00a09
                Copyright © 2015, The Authors

                This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license, which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.

                History
                : 22 June 2015
                : 24 November 2015
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100002347, Bundesministerium für Bildung und Forschung (DE);
                Award ID: ID0E42AG4272
                Award ID: 01GQ1004A
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft (DE);
                Award ID: ID0EOEBG4273
                Award ID: MA 6176/1-1
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100004963, Seventh Framework Programme (BE);
                Award ID: ID0ETJBG4274
                Award ID: PIOF-GA-2013-622943
                Award Recipient :
                Categories
                Research Article
                Research Articles
                SciAdv r-articles
                Neuroscience
                Custom metadata
                Abel Bellen

                grid cell,entorhinal cortex,spatial cognition,goal-directed navigation,self localization,maximum likelihood decoding,population vector,nonlinear gain fields,goal-vector cells

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