Synaptic basis of feature selectivity in hippocampal neurons

Kevin C. Gonzalez, Adrian Negrean, Zhenrui Liao, Satoshi Terada, Guofeng Zhang, Sungmoo Lee, Katalin Ócsai, Balázs J. Rózsa, Michael Z. Lin, Franck Polleux () and Attila Losonczy ()
Additional contact information
Kevin C. Gonzalez: Columbia University
Adrian Negrean: Columbia University
Zhenrui Liao: Columbia University
Satoshi Terada: Columbia University
Guofeng Zhang: Stanford University
Sungmoo Lee: Stanford University
Katalin Ócsai: BrainVisionCenter
Balázs J. Rózsa: BrainVisionCenter
Michael Z. Lin: Stanford University
Franck Polleux: Columbia University
Attila Losonczy: Columbia University

Nature, 2025, vol. 637, issue 8048, 1152-1160

Abstract: Abstract A central question in neuroscience is how synaptic plasticity shapes the feature selectivity of neurons in behaving animals1. 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 the 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. Our work identified compartment-specific differences in the magnitude and temporal expression of synaptic plasticity between basal dendrites and oblique dendrites. Our results provide experimental evidence linking synaptic plasticity to the rapid emergence of spatial selectivity in hippocampal neurons, a critical prerequisite for episodic memory.

Date: 2025
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DOI: 10.1038/s41586-024-08325-9

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