Neuron
Volume 110, Issue 5, 2 March 2022, Pages 783-794.e6
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Local feedback inhibition tightly controls rapid formation of hippocampal place fields

https://doi.org/10.1016/j.neuron.2021.12.003Get rights and content
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Highlights

  • Rapidly forming place fields can be optogenetically induced in mouse CA1 neurons

  • Feedback inhibition limits rapid place field induction to fewer principal neurons

  • Suppressing local inhibition allows induction of place fields in larger ensembles

  • Ensemble place field induction can enhance subsequent spatial association learning

Summary

Hippocampal place cells underlie spatial navigation and memory. Remarkably, CA1 pyramidal neurons can form new place fields within a single trial by undergoing rapid plasticity. However, local feedback circuits likely restrict the rapid recruitment of individual neurons into ensemble representations. This interaction between circuit dynamics and rapid feature coding remains unexplored. Here, we developed “all-optical” approaches combining novel optogenetic induction of rapidly forming place fields with 2-photon activity imaging during spatial navigation in mice. 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 subpopulations due to local circuit constraints imposed by recurrent inhibition. Temporary relief of local inhibition permits the simultaneous induction of place fields in larger ensembles. We demonstrate the behavioral implications of these dynamics, showing that our ensemble place field induction protocol can enhance subsequent spatial association learning.

Keywords

hippocampus
place cell
inhibition
disinhibition
engram
ensembles
plasticity
photostimulation
all-optical
BTSP

Data and code availability

  • All data reported in this paper will be shared upon reasonable request to the lead contact.

  • All original code has been deposited at Zenodo and is publicly available on GitHub as of the date of publication. DOIs are listed in the key resources table.

  • Any additional information required to reanalyze the data reported in this paper is available upon reasonable request to the lead contact.

Cited by (0)

8

These authors contributed equally

9

Lead contact