National Institute of Mental Health, NIMH(1R01MH124047)
National Institute of Mental Health, NIMH(1R01MH124867)
National Institute of Neurological Disorders and Stroke(NINDS 1U01NS115530)
National Institute of Neurological Disorders and Stroke NINDS(NINDS 1U19NS104590)
Simons Foundation(564408)
Wellcome Trust, WT(090843/F/09/Z)
Wellcome Trust, WT(F31MH117892)
Wellcome Trust, WT(K99NS115984-01)
Wellcome Trust, WT(R01NS067557)
Wellcome Trust, WT(R21NS109753-442 01A1)
Engineering and Physical Sciences Research Council, EPSRC(1S10OD023587-01)
Engineering and Physical Sciences Research Council, EPSRC(EP/R035806/1)
Biotechnology and Biological Sciences Research Council(BBSRC 200790/Z/16/Z)
Biotechnology and Biological Sciences Research Council(BBSRC BB/N019008/1)
Biotechnology and Biological Sciences Research Council(BBSRC BB/N013956/1)
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.