Local Feedback Inhibition Tightly Controls Rapid Formation of Hippocampal Place Fields

Abstract

Hippocampal place cells form a physiological substrate for spatial navigation and memory in the brain. Remarkably, CA1 pyramidal neurons can acquire stable place fields in a few trials through a novel behavioral timescale synaptic plasticity rule (BTSP). While this process can enable rapid learning, local feedback circuits likely tightly restrict the recruitment of individual cells into ensemble representations; this interaction between local circuit dynamics and BTSP remains unexplored. Here we developed \all-optical approaches that combine novel optogenetic induction of place fields via BTSP in CA1 pyramidal cells with 2-photon calcium activity imaging during spatial navigation. We find that induction efficacy depends strongly on the density of co-activated neurons. Place fields can be reliably induced in single cells, but induction fails during co-activation of larger CA1 populations. Our results implicate local circuit constraints on the induction of place fields, whereby recurrent inhibition regulates the prevalence of BTSP across the ensemble. Consistent with this interpretation, we found that temporary relief of local inhibition permitted the simultaneous induction of place fields in larger CA1 ensembles. We demonstrate the behavioral consequences of these dynamics, as applying our ensemble optogenetic induction protocol at an arbitrary location enhanced animals' subsequent performance in a spatial reward learning task involving that location.