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
Affiliations
Dorthe Kaufhold
Institute of Physiology I, Faculty of Medicine, Albert-Ludwigs-University Freiburg, 79104 Freiburg, Germany; Faculty of Biology, Albert-Ludwigs-University Freiburg, 79104 Freiburg, Germany
Eduardo Maristany de las Casas
Institute for Biology, Neuronal Plasticity, Humboldt University Berlin, 10117 Berlin, Germany
María Del Ángel Ocaña-Fernández
Institute of Physiology I, Faculty of Medicine, Albert-Ludwigs-University Freiburg, 79104 Freiburg, Germany
Aurore Cazala
Institute of Physiology I, Faculty of Medicine, Albert-Ludwigs-University Freiburg, 79104 Freiburg, Germany
Mei Yuan
Institute of Physiology I, Faculty of Medicine, Albert-Ludwigs-University Freiburg, 79104 Freiburg, Germany
Akos Kulik
Institute of Physiology II, Faculty of Medicine, Albert-Ludwigs-University Freiburg, 79104 Freiburg, Germany; BIOSS Centre for Biological Signaling Studies, Albert-Ludwigs-University Freiburg, 79104 Freiburg, Germany
Thibault Cholvin
Institute of Physiology I, Faculty of Medicine, Albert-Ludwigs-University Freiburg, 79104 Freiburg, Germany
Stefanie Steup
Institute of Physiology I, Faculty of Medicine, Albert-Ludwigs-University Freiburg, 79104 Freiburg, Germany
Jonas-Frederic Sauer
Institute of Physiology I, Faculty of Medicine, Albert-Ludwigs-University Freiburg, 79104 Freiburg, Germany
Mark D. Eyre
Institute of Physiology I, Faculty of Medicine, Albert-Ludwigs-University Freiburg, 79104 Freiburg, Germany
Claudio Elgueta
Institute of Physiology I, Faculty of Medicine, Albert-Ludwigs-University Freiburg, 79104 Freiburg, Germany
Michael Strüber
Epilepsy Center Frankfurt Rhine-Main, Center of Neurology and Neurosurgery, Goethe University, 60528 Frankfurt am Main, Germany
Marlene Bartos
Institute of Physiology I, Faculty of Medicine, Albert-Ludwigs-University Freiburg, 79104 Freiburg, Germany; Corresponding author
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.