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      Hippocampal Ripple Coordinates Retrosplenial Inhibitory Neurons during Slow-Wave Sleep

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          SUMMARY

          The hippocampus and retrosplenial cortex (RSC) play indispensable roles in memory formation, and importantly, a hippocampal oscillation known as ripple is key to consolidation of new memories. However, it remains unclear how the hippocampus and RSC communicate and the role of ripple oscillation in coordinating the activity between these two brain regions. Here, we record from the dorsal hippocampus and RSC simultaneously in freely behaving mice during sleep and reveal that the RSC displays a pre-ripple activation associated with slow and fast oscillations. Immediately after ripples, a subpopulation of RSC putative inhibitory neurons increases firing activity, while most RSC putative excitatory neurons decrease activity. Consistently, optogenetic stimulation of this hippocampus-RSC pathway activates and suppresses RSC putative inhibitory and excitatory neurons, respectively. These results suggest that the dorsal hippocampus mainly inhibits RSC activity via its direct innervation of RSC inhibitory neurons, which overshadows the RSC in supporting learning and memory functions.

          In Brief

          Converging evidence suggests that hippocampal ripple oscillations and their interaction with the neocortex are critical for memory consolidation. By combining electrophysiology and optogenetic techniques in freely behaving mice, Opalka et al. provide direct evidence that hippocampal ripples communicate with retrosplenial cortex (RSC) interneurons and inhibit RSC population activity during sleep-associated memory consolidation.

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          Most cited references49

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          Memory consolidation, retrograde amnesia and the hippocampal complex.

          Results from recent studies of retrograde amnesia following damage to the hippocampal complex of human and non-human subjects have shown that retrograde amnesia is extensive and can encompass much of a subject's lifetime; the degree of loss may depend upon the type of memory assessed. These and other findings suggest that the hippocampal formation and related structures are involved in certain forms of memory (e.g. autobiographical episodic and spatial memory) for as long as they exist and contribute to the transformation and stabilization of other forms of memory stored elsewhere in the brain.
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            Awake hippocampal sharp-wave ripples support spatial memory.

            The hippocampus is critical for spatial learning and memory. Hippocampal neurons in awake animals exhibit place field activity that encodes current location, as well as sharp-wave ripple (SWR) activity during which representations based on past experiences are often replayed. The relationship between these patterns of activity and the memory functions of the hippocampus is poorly understood. We interrupted awake SWRs in animals learning a spatial alternation task. We observed a specific learning and performance deficit that persisted throughout training. This deficit was associated with awake SWR activity, as SWR interruption left place field activity and post-experience SWR reactivation intact. These results provide a link between awake SWRs and hippocampal memory processes, which suggests that awake replay of memory-related information during SWRs supports learning and memory-guided decision-making.
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              Awake replay of remote experiences in the hippocampus

              Hippocampal replay is thought to be essential for the consolidation of event memories in hippocampal–neocortical networks. Replay is present during both sleep and waking behavior, but while sleep replay involves the reactivation of stored representations in the absence of specific sensory inputs, awake replay is thought to depend on sensory input from the current environment. Here we show that stored representations are reactivated during both waking and sleep replay. We found frequent awake replay of sequences of rat hippocampal place cells from a previous experience. This spatially remote replay was as common as local replay of the current environment and was most robust when the animal had recently been in motion as compared to during extended periods of quiescence. These results indicate that the hippocampus consistently replays past experiences during brief pauses in waking behavior, suggesting a role for waking replay in memory consolidation and retrieval.
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                Author and article information

                Journal
                101573691
                39703
                Cell Rep
                Cell Rep
                Cell reports
                2211-1247
                15 January 2020
                14 January 2020
                09 February 2020
                : 30
                : 2
                : 432-441.e3
                Affiliations
                [1 ]Department of Neurobiology and Anatomy, Drexel University College of Medicine, Philadelphia, PA 19129, USA
                [2 ]School of Biomedical Engineering, Drexel University, Philadelphia, PA 19104, USA
                [3 ]Lead Contact
                Author notes

                AUTHOR CONTRIBUTIONS

                Conceptualization, D.V.W.; Methodology, D.V.W. and H.L.; Investigation, A.N.O., W.-q.H., J.L., and D.V.W.; Writing - Original Draft, A.N.O. and D.V.W.; Writing - Review & Editing, A.N.O., W.-q.H., J.L., H.L., and D.V.W.; Funding Acquisition, D.V.W.; Resources, D.V.W.; Supervision, D.V.W.

                [* ]Correspondence: dw657@ 123456drexel.edu
                Article
                NIHMS1549889
                10.1016/j.celrep.2019.12.038
                7007963
                31940487
                b96e75ed-bc91-4c39-aed7-2eb3addb77b2

                This is an open access article under the CC BY license ( http://creativecommons.org/licenses/by/4.0/).

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                Cell biology
                Cell biology

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