VTA neurons coordinate with the hippocampal reactivation of spatial experience

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Abstract

Spatial learning requires the hippocampus, and the replay of spatial sequences during hippocampal sharp wave-ripple (SPW-R) events of quiet wakefulness and sleep is believed to play a crucial role. To test whether the coordination of VTA reward prediction error signals with these replayed spatial sequences could contribute to this process, we recorded from neuronal ensembles of the hippocampus and VTA as rats performed appetitive spatial tasks and subsequently slept. We found that many reward responsive (RR) VTA neurons coordinated with quiet wakefulness-associated hippocampal SPW-R events that replayed recent experience. In contrast, coordination between RR neurons and SPW-R events in subsequent slow wave sleep was diminished. Together, these results indicate distinct contributions of VTA reinforcement activity associated with hippocampal spatial replay to the processing of wake and SWS-associated spatial memory.

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Stephen N Gomperts

MassGeneral Institute for Neurodegenerative Disease, Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, United States

For correspondence
sgomperts@partners.org

Competing interests
The authors declare that no competing interests exist.
Fabian Kloosterman

NERF, Leuven, Belgium

Competing interests
The authors declare that no competing interests exist.
Matthew A Wilson

Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, United States

Competing interests
The authors declare that no competing interests exist.

Ethics

Animal experimentation: All procedures were approved by the Committee on Animal Care of Massachusetts Institute of Technology (Protocol Number 0505-032-08) and followed the ethical guidelines of the US National Institutes of Health.

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This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.