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J Neurosci. 2019 Aug 28;39(35):6978-6991. doi: 10.1523/JNEUROSCI.2158-18.2019. Epub 2019 Jul 8.

Monosynaptic Hippocampal-Prefrontal Projections Contribute to Spatial Memory Consolidation in Mice.

Author information

1
Institute of Experimental and Clinical Pharmacology and Toxicology, lisa.marshall@pharma.uni-luebeck.de sonja.binder@pharma.uni-luebeck.de.
2
Center for Brain, Behavior and Metabolism.
3
Leibniz Institute for Neurobiology, Systems Physiology of Learning, Center for Behavioral Brain Sciences, 39118 Magdeburg, Germany.
4
Institute for Robotics and Cognitive Systems, University of Luebeck, 23562 Lübeck, Germany.
5
Institute of Experimental and Clinical Pharmacology and Toxicology.
6
Otto-von-Guericke University Magdeburg, Faculty for Natural Sciences, 39106 Magdeburg, Germany, and.
7
University Medical Center Hamburg-Eppendorf, Center for Molecular Neurobiology Hamburg (ZMNH), 20251 Hamburg, Germany.

Abstract

Time locking between neocortical sleep slow oscillations, thalamo-cortical spindles, and hippocampal sharp-wave ripples has convincingly been shown to be a key element of systems consolidation. Here we investigate the role of monosynaptic projections from ventral/intermediate hippocampus to medial prefrontal cortex (mPFC) in sleep-dependent memory consolidation in male mice. Following acquisition learning in the Barnes maze, we optogenetically silenced the axonal terminals of hippocampal projections within mPFC during slow-wave sleep. This silencing during SWS selectively impaired recent but not remote memory in the absence of effects on error rate and escape latencies. Furthermore, it prevented the development of the most efficient search strategy and sleep spindle time-locking to slow oscillation. An increase in post-learning sleep sharp-wave ripple (SPWR) density and reduced time locking of learning-associated SPWR activity to sleep spindles may be a less specific response. Our results demonstrate that monosynaptic projections from hippocampus to mPFC contribute to sleep-dependent memory consolidation, potentially by affecting the temporal coupling of sleep-associated electrophysiological events.SIGNIFICANCE STATEMENT Convincing evidence supports the role of slow-wave sleep (SWS), and the relevance of close temporal coupling of neuronal activity between brain regions for systems consolidation. Less attention has been paid so far to the specific neuronal pathways underlying these processes. Here, we optogenetically silenced the direct monosynaptic projection from ventral/intermediate hippocampus (HC) to medial prefrontal cortex (mPFC) during SWS in male mice following repeated learning trials in a weakly aversive spatial task. Our results confirm the concept that the monosynaptic projection between HC and mPFC contributes to memory consolidation and support an important functional role of this pathway in shaping the temporal precision among sleep-associated electrophysiological events.

KEYWORDS:

Barnes maze; hippocampus; optogenetics; prefrontal cortex; sleep; spatial memory

PMID:
31285301
PMCID:
PMC6733568
[Available on 2020-02-28]
DOI:
10.1523/JNEUROSCI.2158-18.2019
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