A Hippocampus-Accumbens Tripartite Neuronal Motif Guides Appetitive Memory in Space

Stéphanie Trouche, Vadim Koren, Natalie M Doig, Tommas J Ellender, Mohamady El-Gaby, Vítor Lopes-Dos-Santos, Hayley M Reeve, Pavel V Perestenko, Farid N Garas, Peter J Magill, Andrew Sharott, David Dupret

Research output: Contribution to journalArticle (Academic Journal)

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Abstract

Retrieving and acting on memories of food-predicting environments are fundamental processes for animal survival. Hippocampal pyramidal cells (PYRs) of the mammalian brain provide mnemonic representations of space. Yet the substrates by which these hippocampal representations support memory-guided behavior remain unknown. Here, we uncover a direct connection from dorsal CA1 (dCA1) hippocampus to nucleus accumbens (NAc) that enables the behavioral manifestation of place-reward memories. By monitoring neuronal ensembles in mouse dCA1→NAc pathway, combined with cell-type selective optogenetic manipulations of input-defined postsynaptic neurons, we show that dCA1 PYRs drive NAc medium spiny neurons and orchestrate their spiking activity using feedforward inhibition mediated by dCA1-connected parvalbumin-expressing fast-spiking interneurons. This tripartite cross-circuit motif supports spatial appetitive memory and associated NAc assemblies, being independent of dorsal subiculum and dispensable for both spatial novelty detection and reward seeking. Our findings demonstrate that the dCA1→NAc pathway instantiates a limbic-motor interface for neuronal representations of space to promote effective appetitive behavior.

Original languageEnglish
Pages (from-to)1393-1406.e16
Number of pages31
JournalCell
Volume176
Issue number6
Early online date14 Feb 2019
DOIs
Publication statusPublished - 7 Mar 2019

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