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Local circuit amplification of spatial selectivity in the hippocampus

Tristan Geiller (), Sadra Sadeh, Sebastian V. Rolotti, Heike Blockus, Bert Vancura, Adrian Negrean, Andrew J. Murray, Balázs Rózsa, Franck Polleux, Claudia Clopath and Attila Losonczy ()
Additional contact information
Tristan Geiller: Columbia University
Sadra Sadeh: Imperial College London
Sebastian V. Rolotti: Columbia University
Heike Blockus: Columbia University
Bert Vancura: Columbia University
Adrian Negrean: Columbia University
Andrew J. Murray: University College London
Balázs Rózsa: Institute of Experimental Medicine
Franck Polleux: Columbia University
Claudia Clopath: Imperial College London
Attila Losonczy: Columbia University

Nature, 2022, vol. 601, issue 7891, 105-109

Abstract: 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.

Date: 2022
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DOI: 10.1038/s41586-021-04169-9

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