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Local circuit amplification of spatial selectivity in the hippocampus

Geiller, Tristan and Sadeh, Sadra and Rolotti, Sebastian V. and Blockus, Heike and Vancura, Bert and Rózsa J., Balázs and Losonczy, Attila (2022) Local circuit amplification of spatial selectivity in the hippocampus. NATURE, 601. pp. 105-109. ISSN 0028-0836

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Abstract

Local circuit architecture facilitates the emergence of feature selectivity in the cerebral cortex1. In the hippocampus, it remains unknown whether local computations supported by specific connectivity motifs2 regulate the spatial receptive fields of pyramidal cells3. Here we developed an in vivo electroporation method for monosynaptic retrograde tracing4 and optogenetics manipulation at single-cell resolution to interrogate the dynamic interaction of place cells with their microcircuitry during navigation. We found a local circuit mechanism in CA1 whereby the spatial tuning of an individual place cell can propagate to a functionally recurrent subnetwork5 to which it belongs. The emergence of place fields in individual neurons led to the development of inverse selectivity in a subset of their presynaptic interneurons, and recruited functionally coupled place cells at that location. Thus, the spatial selectivity of single CA1 neurons is amplified through local circuit plasticity to enable effective multi-neuronal representations that can flexibly scale environmental features locally without degrading the feedforward input structure.

Item Type: Article
Additional Information: Department of Neuroscience, Columbia University, New York, NY, United States Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York, NY, United States Bioengineering Department, Imperial College London, London, United Kingdom Sainsbury Wellcome Centre, University College London, London, United Kingdom Institute of Experimental Medicine, Budapest, Hungary The Kavli Institute for Brain Science, Columbia University, New York, NY, United States Cited By :12 Export Date: 7 February 2023 CODEN: NATUA Correspondence Address: Geiller, T.; Department of Neuroscience, United States; email: tcg2117@columbia.edu Correspondence Address: Losonczy, A.; Department of Neuroscience, United States; email: al2856@columbia.edu Funding details: National Institutes of Health, NIH, F30MH125628, T32GN007367 Funding details: National Institute of Mental Health, NIMH, 1R01MH124047, 1R01MH124867 Funding details: National Institute of Neurological Disorders and Stroke, NINDS, 1U01NS115530, 1U19NS104590 Funding details: Simons Foundation, SF, 564408 Funding details: Kavli Foundation Funding details: Wellcome Trust, WT, 090843/F/09/Z, F31MH117892, K99NS115984-01, R01NS067557, R21NS109753-442 01A1 Funding details: Engineering and Physical Sciences Research Council, EPSRC, 1S10OD023587-01, EP/R035806/1 Funding details: Biotechnology and Biological Sciences Research Council, BBSRC, 200790/Z/16/Z, BB/N013956/1, BB/N019008/1 Funding details: Gatsby Charitable Foundation Funding text 1: Acknowledgements A.L. is supported by the National Institute of Mental Health (NIMH) 1R01MH124047 and 1R01MH124867; the National Institute of Neurological Disorders and Stroke (NINDS) 1U19NS104590 and 1U01NS115530; and the Kavli Foundation. B.V. is supported by (NIH) T32GN007367 and (NIMH) F30MH125628. A.J.M. is supported by the Gatsby Charitable Foundation (GAT3361) and the Wellcome Trust (090843/F/09/Z). S.V.R. is supported by (NIMH) F31MH117892. F.P. is supported by (NINDS) R01NS067557 and R21NS109753-442 01A1. H.B. is supported by (NINDS) K99NS115984-01. C.C. is supported by the Biotechnology and Biological Sciences Research Council (BB/N013956/1 and BB/N019008/1), the Wellcome Trust (200790/Z/16/Z), the Simons Foundation (564408) and the EPSRC (EP/R035806/1). We thank the Zuckerman Institute’s Cellular Imaging platform for instrument use and technical advice. Imaging was performed with support from the Zuckerman Institute’s Cellular Imaging platform and the NIH (1S10OD023587-01). We thank S. Siegelbaum and members of the Losonczy laboratory for comments on the manuscript.
Subjects: R Medicine / orvostudomány > R1 Medicine (General) / orvostudomány általában
SWORD Depositor: MTMT SWORD
Depositing User: MTMT SWORD
Date Deposited: 26 Feb 2023 12:03
Last Modified: 26 Feb 2023 12:03
URI: http://real.mtak.hu/id/eprint/160663

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