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

• Published in: Nature communications Vol. 11; no. 1; pp. 1947 - 17
• Main Authors: Nitzan, Noam, McKenzie, Sam, Beed, Prateep, English, Daniel Fine, Oldani, Silvia, Tukker, John J., Buzsáki, György, Schmitz, Dietmar
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 23-04-2020; Nature Publishing Group; Nature Portfolio
• Subjects: 13/1; 14/19; 14/34; 14/63; 631/378/1595/1554; 631/378/3920; 64/60; 9/30; 9/74; Activity patterns; Animal memory; Animals; Brain Waves - physiology; CA1 Region, Hippocampal - physiology; Cerebral cortex; Communication; Coupling; High frequencies; Hippocampus; Hippocampus - physiology; Humanities and Social Sciences; Mice; Mice, Transgenic; multidisciplinary; Neocortex - physiology; Neural Pathways - physiology; Neurons; Neurons - metabolism; Neurons - physiology; Ripples; Science; Science (multidisciplinary); Subiculum; Synaptic Transmission; Vesicular Glutamate Transport Protein 2 - genetics; Vesicular Glutamate Transport Protein 2 - metabolism; Wakefulness - physiology
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-020-15787-8

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.
Communication between the hippocampus and neocortex is organized through high frequency sharp wave ripple activity. Here, the authors report ripple activity coupling between the hippocampus and granular retrosplenial cortex suggesting an involvement in communicating with the neocortex.