Propagation of hippocampal ripples to the neocortex by way of a subiculum-retrosplenial pathway

Noam Nitzan, Sam McKenzie, Prateep Beed, Daniel Fine English, Silvia Oldani, John J. Tukker, György Buzsáki () and Dietmar Schmitz ()
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Noam Nitzan: Charité-Universitätsmedizin Berlin, Corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Neuroscience Research Center
Sam McKenzie: Neuroscience Institute and Department of Neurology New York University Langone Medical Center
Prateep Beed: Charité-Universitätsmedizin Berlin, Corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Neuroscience Research Center
Daniel Fine English: Neuroscience Institute and Department of Neurology New York University Langone Medical Center
Silvia Oldani: Charité-Universitätsmedizin Berlin, Corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Neuroscience Research Center
John J. Tukker: Charité-Universitätsmedizin Berlin, Corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Neuroscience Research Center
György Buzsáki: Neuroscience Institute and Department of Neurology New York University Langone Medical Center
Dietmar Schmitz: Charité-Universitätsmedizin Berlin, Corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Neuroscience Research Center

Nature Communications, 2020, vol. 11, issue 1, 1-17

Abstract: Abstract Bouts of high frequency activity known as sharp wave ripples (SPW-Rs) facilitate communication between the hippocampus and neocortex. However, the paths and mechanisms by which SPW-Rs broadcast their content are not well understood. Due to its anatomical positioning, the granular retrosplenial cortex (gRSC) may be a bridge for this hippocampo-cortical dialogue. Using silicon probe recordings in awake, head-fixed mice, we show the existence of SPW-R analogues in gRSC and demonstrate their coupling to hippocampal SPW-Rs. gRSC neurons reliably distinguished different subclasses of hippocampal SPW-Rs according to ensemble activity patterns in CA1. We demonstrate that this coupling is brain state-dependent, and delineate a topographically-organized anatomical pathway via VGlut2-expressing, bursty neurons in the subiculum. Optogenetic stimulation or inhibition of bursty subicular cells induced or reduced responses in superficial gRSC, respectively. These results identify a specific path and underlying mechanisms by which the hippocampus can convey neuronal content to the neocortex during SPW-Rs.

Date: 2020
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DOI: 10.1038/s41467-020-15787-8

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