Cell Reports (Mar 2024)

Spine plasticity of dentate gyrus parvalbumin-positive interneurons is regulated by experience

  • Dorthe Kaufhold,
  • Eduardo Maristany de las Casas,
  • María Del Ángel Ocaña-Fernández,
  • Aurore Cazala,
  • Mei Yuan,
  • Akos Kulik,
  • Thibault Cholvin,
  • Stefanie Steup,
  • Jonas-Frederic Sauer,
  • Mark D. Eyre,
  • Claudio Elgueta,
  • Michael Strüber,
  • Marlene Bartos

Journal volume & issue
Vol. 43, no. 3
p. 113806

Abstract

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Summary: Experience-driven alterations in neuronal activity are followed by structural-functional modifications allowing cells to adapt to these activity changes. Structural plasticity has been observed for cortical principal cells. However, how GABAergic interneurons respond to experience-dependent network activity changes is not well understood. We show that parvalbumin-expressing interneurons (PVIs) of the dentate gyrus (DG) possess dendritic spines, which undergo behaviorally induced structural dynamics. Glutamatergic inputs at PVI spines evoke signals with high spatial compartmentalization defined by neck length. Mice experiencing novel contexts form more PVI spines with elongated necks and exhibit enhanced network and PVI activity and cFOS expression. Enhanced green fluorescent protein reconstitution across synaptic partner-mediated synapse labeling shows that experience-driven PVI spine growth boosts targeting of PVI spines over shafts by glutamatergic synapses. Our findings propose a role for PVI spine dynamics in regulating PVI excitation by their inputs, which may allow PVIs to dynamically adjust their functional integration in the DG microcircuitry in relation to network computational demands.

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