Dentate spikes and external control of hippocampal function

Abstract

Mouse hippocampus CA1 place-cell discharge typically encodes current location but during slow gamma dominance (SGdom), when slow gamma oscillations (30-60 Hz) dominate mid-frequency gamma oscillations (60-90 Hz) in CA1 local field potentials, CA1 discharge switches to represent distant recollected locations. We now report that dentate spike type 2 (DSM) events initiated by MECII→DG inputs promote SGdom and change CA1 discharge, whereas type 1 (DSL) events initiated by LECII→DG inputs do not. Just before SGdom, LECII-originating slow gamma oscillations in dentate gyrus and CA3-originating slow gamma oscillations in CA1 become optimally phase and frequency synchronized at the DSM peak when the firing rates of DG, CA3, and CA1 principal cells increase to promote DG→CA3→CA1 cofiring optimized for the 5-10 ms DG-to-CA1 neuro-transmission that coincides with SGdom. Several properties and consequences of DSM demonstrate extrahippocampal control of SGdom, identifying a cortico-hippocampal mechanism that switches between memory-related hippocampal information processing modes.

A manifold neural population code for space in hippocampal coactivity dynamics independent of place fields

“…We find that the strongly coactive and anti-coactive cell pairs are particularly discriminative at the 1-s timescale and, remarkably, anti-coactive cells are both more discriminative and more important for organizing the activity on a manifold (Okun et al, 2015). This is consistent with the increase of interneuron-principal cell cofiring that has been observed at moments of memory discrimination and recollection (Dvorak et al, 2021;van Dijk and Fenton, 2018). We analyzed activity fluctuations around place tuning (Agarwal et al, 2014), in effect removing the place signal from the time series, to compute cell-pair coactivity and found that it improved the ability to discriminate environments (Fig.…”

“…Remarkably, E®I and I®E plasticity are necessary for developing the place tuning, but E®E plasticity is not (Fig. 1C), illustrating that tunable excitation-inhibition coordination can be important for network and memory function (Caroni, 2015;Dvorak et al, 2021;Fenton, 2015b;Mongillo et al, 2018;van Dijk and Fenton, 2018). To simulate learning a second environment, we remapped the positionto-input relationships and allowed the recurrent weights to change according to the same STDP rules during another 30 laps.…”

Dentate gyrus and CA3 GABAergic interneurons bidirectionally modulate signatures of internal and external drive to CA1

“…Dentate spikes were detected as previously described (Dvorak et al, 2021) at the site with the highest MUA and visually confirmed dentate spikes. Raw LFP during rest sessions were band-pass equiripple filtered at 5-100 Hz and Z score normalized, then peaks were detected.…”

“…Analysis was restricted to periods of extended immobility, after the mouse Gaussian smoothed velocity had been <1 cm/s for 30 s or more. Site spacing was too large for CSD analysis, thus dentate spikes were not classified by type (Dvorak et al, 2021).…”

Do place cells dream of deceptive moves in a signaling game?

“…It is not obvious what sensory cues would switch firing from representing local position to non-local position, but SGdom transiently switching CA1 network function from processing local place information based on sensory cues to processing non-local information based on memory predicts these observations. SGdom is triggered by a medial entorhinal cortex-originating dentate spike event that switches hippocampal information processing from sensation-based encoding to memory based recollection (Dvorak et al, 2021). Figure based on (Dvorak et al, 2018).…”