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Synaptic basis of feature selectivity in hippocampal neurons

Gonzalez, Kevin1; Negrean, Adrian1; Liao, Zhenrui1; Terada, Satoshi1; Zhang, Guofeng2; Lee, Sungmoo2; Ócsai, Katalin3; Rózsa, Balázs3; Lin, Michael2; Polleux, Franck1; Losonczy, Attila1

Published Nov 11, 2024 on Dryad. https://doi.org/10.5061/dryad.66t1g1k9r

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Nov 11, 2024 version files 669.04 KB

Abstract

A central question in neuroscience is how synaptic plasticity shapes the feature selectivity of neurons in behaving animals. Hippocampal CA1 pyramidal neurons display one of the most striking forms of feature selectivity by forming spatially and contextually selective receptive fields called place fields, which serve as a model for studying the synaptic basis of learning and memory. Various forms of synaptic plasticity have been proposed as cellular substrates for the emergence of place fields. However, despite decades of work, our understanding of how synaptic plasticity underlies place field formation and memory encoding remains limited, largely due to a shortage of tools and technical challenges associated with the visualization of synaptic plasticity at single-neuron resolution in awake-behaving animals. To address this, we developed an all-optical approach to monitor the spatiotemporal tuning and synaptic weight changes of dendritic spines, before and after the induction of a place field in single CA1 pyramidal neurons during spatial navigation. We identified a temporally asymmetric synaptic plasticity kernel resulting from bidirectional modifications of synaptic weights around the induction of a place field. Surprisingly, our work uncovered compartment-specific differences in the magnitude and temporal expression of synaptic plasticity between basal and oblique dendrites. Our results provide the first experimental evidence linking synaptic plasticity to the rapid emergence of spatial selectivity in hippocampal neurons, a critical prerequisite for episodic memory.