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

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...

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Published in:	Cell reports (Cambridge) Vol. 43; no. 3; p. 113806
Main Authors:	Kaufhold, Dorthe, Maristany de las Casas, Eduardo, Ocaña-Fernández, María Del Ángel, Cazala, Aurore, Yuan, Mei, Kulik, Akos, Cholvin, Thibault, Steup, Stefanie, Sauer, Jonas-Frederic, Eyre, Mark D., Elgueta, Claudio, Strüber, Michael, Bartos, Marlene
Format:	Journal Article
Language:	English
Published:	United States Elsevier Inc 26-03-2024 Elsevier
Subjects:	Animals behavior CP: Neuroscience dentate gyrus Dentate Gyrus - metabolism eGRASP experience- and context-dependent spine dynamics fast-spiking parvalbumin-positive interneurons hippocampus Interneurons - metabolism in vitro electrophysiology Mice Neuronal Plasticity Neurons - metabolism Parvalbumins - metabolism spines Synapses - metabolism dentate gyrus in vitro electrophysiology fast-spiking parvalbumin-positive interneurons hippocampus CP: Neuroscience eGRASP spines behavior experience- and context-dependent spine dynamics
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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. [Display omitted] •A substantial proportion of PVIs in the DG, but not hippocampal CA1-3, are spiny•PVI spine length regulates chemical and functional input isolation•Experience-driven DG network activity controls PVI spine density and shape•Experience increases the preference of glutamatergic inputs for PVI spines over shafts Kaufhold et al. investigate the conditions leading to spine dynamics in dentate gyrus PVIs. Experience-driven elevated neuronal network activity increases the number and length of spines at PVI dendrites, a regulatory mechanism supporting the preference of synaptic inputs to spines over dendritic shafts for their functional isolation.
Bibliography:	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23
ISSN:	2211-1247 2211-1247
DOI:	10.1016/j.celrep.2024.113806