Slow gamma rhythms in CA3 are entrained by slow gamma activity in the dentate gyrus

Abstract

In hippocampal area CA1, slow (∼25-55 Hz) and fast (∼60-100 Hz) gamma rhythms are coupled with different CA1 afferents. CA1 slow gamma is coupled to inputs from CA3, and CA1 fast gamma is coupled to inputs from the medial entorhinal cortex (Colgin LL, Denninger T, Fyhn M, Hafting T, Bonnevie T, Jensen O, Moser MB, Moser EI. Nature 462: 353-357, 2009). CA3 gives rise to highly divergent associational projections, and it is possible that reverberating activity in these connections generates slow gamma rhythms in the hippocampus. However, hippocampal gamma is maximal upstream of CA3, in the dentate gyrus (DG) region (Bragin A, Jando G, Nadasdy Z, Hetke J, Wise K, Buzsaki G. J Neurosci 15: 47-60, 1995). Thus it is possible that slow gamma in CA3 is driven by inputs from DG, yet few studies have examined slow and fast gamma rhythms in DG recordings. Here we investigated slow and fast gamma rhythms in paired recordings from DG and CA3 in freely moving rats to determine whether slow and fast gamma rhythms in CA3 are entrained by DG. We found that slow gamma rhythms, as opposed to fast gamma rhythms, were particularly prominent in DG. We investigated directional causal influences between DG and CA3 by Granger causality analysis and found that DG slow gamma influences CA3 slow gamma. Moreover, DG place cell spikes were strongly phase-locked to CA3 slow gamma rhythms, suggesting that DG excitatory projections to CA3 may underlie this directional influence. These results indicate that slow gamma rhythms do not originate in CA3 but rather slow gamma activity upstream in DG entrains slow gamma rhythms in CA3.

Comparison of three gamma oscillations in the mouse entorhinal–hippocampal system

“…For CA3, gamma oscillations increased from 23 ± 0 Hz at 22 °C to 41 ± 2 Hz at 30 °C ( n = 14; Fig. H), getting closer to the in vivo slow gamma frequency (Schomburg et al ., ; Hsiao et al ., ; Lasztóczi & Klausberger, ). The frequency of gamma oscillations in the mEC at 30 °C was also in agreement with medium gamma frequency described in vivo (Colgin et al ., ; Belluscio et al ., ; Schomburg et al ., ), reaching a frequency of 68 ± 3 Hz at 30 °C ( n = 12).…”

“…A and B). Furthermore, the CA1 and mEC waveforms appeared to have more of a sawtooth shape than that of CA3 gamma waveforms, which is consistent with reports of CA1 and CA3 gamma oscillation waveforms in vivo (Colgin et al ., ; Hsiao et al ., ). Gamma oscillations in the entorhinal–hippocampal system therefore have a consistent asymmetric waveform reflecting the origin of the signal in the perisomatic or dendritic layer of the region.…”

Quantitative properties of a feedback circuit predict frequency-dependent pattern separation

“…Perhaps most interestingly, the occurrence of oscillations in the slow-gamma range has recently been reported to be causally related to associative memory formation 41,44 , a process thought to require pattern separation. Consistent with this finding, Hsiao et al 43 report DG driven gamma entrainment of CA3, the presumed primary storage location of associative memories. Together, this suggests that the dentate pattern separator may be optimized to rapidly detect subtle degrees of difference within the environment in gamma-dominated exploratory brain states, a capability likely to support successful memory encoding of novel environmental features, and potentially aiding in rapid discrimination during recall.…”

“…It is furthermore necessary to quantify the spatial and temporal properties of the elicited inhibition, in order to investigate its impact on biologically plausible, temporally structured input. For instance, the DG shows prominent theta oscillations during exploration and distinctive slow-gamma activity during associative memory encoding [41][42][43][44] .…”

CA3 place cells that represent a novel waking experience are preferentially reactivated during sharp wave-ripples in subsequent sleep

“…Data were acquired using a Digital Lynx system and Cheetah recording software (Neuralynx, Bozeman, Montana). The recording setup has been described in detail previously (Hsiao et al, 2016; Zheng et al, 2016). Briefly, LFPs from one randomly chosen channel within each tetrode were continuously recorded in the 0.1-500 Hz band at a 2000 Hz sampling rate.…”