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      Hippocampus-dependent emergence of spatial sequence coding in retrosplenial cortex

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          Significance

          Retrosplenial cortex (RSC) is a major relay of hippocampal formation output to other neocortical areas and is critical for spatial and some other forms of learning. We show here that the sparse, orthogonal, “place cell” sequence activity in RSC develops gradually over several days and is severely attenuated by hippocampal damage. These data support the theory that hippocampus endows RSC (and possibly other cortical areas) with an index-like, continuous representation of the context in which events occur, that could support coordinated retrieval of recent memory.

          Abstract

          Retrosplenial cortex (RSC) is involved in visuospatial integration and spatial learning, and RSC neurons exhibit discrete, place cell-like sequential activity that resembles the population code of space in hippocampus. To investigate the origins and population dynamics of this activity, we combined longitudinal cellular calcium imaging of dysgranular RSC neurons in mice with excitotoxic hippocampal lesions. We tracked the emergence and stability of RSC spatial activity over consecutive imaging sessions. Overall, spatial activity in RSC was experience-dependent, emerging gradually over time, but, as seen in the hippocampus, the spatial code changed dynamically across days. Bilateral but not unilateral hippocampal lesions impeded the development of spatial activity in RSC. Thus, the emergence of spatial activity in RSC, a major recipient of hippocampal information, depends critically on an intact hippocampus; the indirect connections between the dysgranular RSC and the hippocampus further indicate that hippocampus may exert such influences polysynaptically within neocortex.

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          Most cited references 34

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          Place navigation impaired in rats with hippocampal lesions

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            Place navigation impaired in rats with hippocampal lesions.

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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
                Proc Natl Acad Sci U S A
                Proc. Natl. Acad. Sci. U.S.A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                31 July 2018
                16 July 2018
                16 July 2018
                : 115
                : 31
                : 8015-8018
                Affiliations
                aCanadian Centre for Behavioural Neuroscience, Department of Neuroscience, University of Lethbridge , Lethbridge, AB T1K 3M4, Canada;
                bNeuro-Electronics Research Flanders , 3001 Leuven, Belgium;
                cVlaams Instituut voor Biotechnologie , 3000 Leuven, Belgium;
                dDepartment of Biology, KU Leuven , 3000 Leuven, Belgium;
                eDepartment of Neurobiology and Behavior, University of California, Irvine , CA 92697
                Author notes
                1To whom correspondence may be addressed. Email: zjumao@ 123456gmail.com or bruce.mcnaughton@ 123456uleth.ca .

                Edited by Gyorgy Buzsáki, New York University Neuroscience Institute, New York, NY, and approved June 20, 2018 (received for review February 21, 2018)

                Author contributions: D.M., V.B., M.H.M., and B.L.M. designed research; D.M., A.R.N., and J.S. performed research; D.M. analyzed data; and D.M., V.B., and B.L.M. wrote the paper.

                2Present address: Department of Neuroscience, Baylor College of Medicine, Houston, TX 77030.

                3V.B. and B.L.M. contributed equally to this work.

                Article
                201803224
                10.1073/pnas.1803224115
                6077725
                30012620
                Copyright © 2018 the Author(s). Published by PNAS.

                This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

                Page count
                Pages: 4
                Product
                Funding
                Funded by: Alberta Innovates - Health Solutions (AIHS) 501100000145
                Award ID: Polaris award
                Award Recipient : Dun Mao Award Recipient : Bruce L McNaughton
                Funded by: Alberta Innovates - Health Solutions (AIHS) 501100000145
                Award ID: Graduate studentship
                Award Recipient : Dun Mao Award Recipient : Bruce L McNaughton
                Funded by: Gouvernement du Canada | Natural Sciences and Engineering Research Council of Canada (NSERC) 501100000038
                Award ID: #40352
                Award Recipient : Majid Mohajerani Award Recipient : Bruce L McNaughton
                Funded by: Gouvernement du Canada | Natural Sciences and Engineering Research Council of Canada (NSERC) 501100000038
                Award ID: #RGPIN-2017-03857
                Award Recipient : Majid Mohajerani Award Recipient : Bruce L McNaughton
                Funded by: Fonds Wetenschappelijk Onderzoek (FWO) 501100003130
                Award ID: G0D0516N
                Award Recipient : Vincent Bonin
                Funded by: Onderzoeksraad, KU Leuven (Research Council, KU Leuven) 501100004497
                Award ID: C14/16/048
                Award Recipient : Vincent Bonin
                Funded by: National Science Foundation (NSF) 100000001
                Award ID: #1631465
                Award Recipient : Bruce L McNaughton
                Funded by: Canada Foundation for Innovation (CFI) 501100000196
                Award ID: #33598
                Award Recipient : Bruce L McNaughton
                Funded by: DOD | Defense Advanced Research Projects Agency (DARPA) 100000185
                Award ID: # HR0011-18-2-0021
                Award Recipient : Bruce L McNaughton
                Categories
                Biological Sciences
                Neuroscience

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