Granular retrosplenial cortex high frequency oscillation dynamics in hippocampo-cortical dialogue

We used dense (20 m site spacing) local field potential (LFP) and single unit recordings across all layers of the gRSC concurrent with CA1 LFP recordings in behaving mice to investigate circuit activity of high-frequency oscillations (HFOs) in theta and sharp wave-ripples (SWRs). By comparing HFOs occurring at times of SWRs (+/-50 ms) or during theta, we found using current-source density analysis that HFOs in different states are uniformly localized to layer 2/3 (L2/3) with current sources and sinks bridging the L1-L2/3 border. HFOs that occurred outside of SWR times where rhythmically locked to the descending phase of theta and co-occurred with HPC theta locked gamma oscillations. In ensemble recordings of gRSC neurons, subsets of both excitatory and inhibitory neurons had different activity during each type of HFO and findings were consistent with previously reported event triggered neural activity (Nitzan et al., 2020). Additionally, using mice chronically expressing the excitatory rhodopsin Channelrhodopsin in pyramidal cells, we show that a broad light stimulus delivered to specific layers with a LED probe is sufficient to induce HFOs in L2/3 and L5 (Wu, F. et al., 2015). Interestingly, while we don’t see HFOs naturally occurring in L5 the local synaptic network is structured to support HFOs. These findings suggest that gRSC networks support HFOs in the same location at different states, though the natural drivers of these HFO events are different between states. That being the SWR via excitatory subiculum connections, and the highly synchronous HPC-gRSC theta oscillation. HFO events in different states play key roles in hippocampo-cortical dialogue and may allow for information transfer using theta locked gamma-HFO synchrony during locomotion and SWR-HFO synchrony during quiet wakefulness.