Fast Gamma Rhythms in the Hippocampus Promote Encoding of Novel Object–Place Pairings

Changes in slow and fast gamma power in CA1 in response to exploration of novel object–place pairings. A–C, Color-coded power across gamma frequencies in CA1 as a function of running speed, plotted during time periods of familiarity exploration versus novelty exploration, averaged across all CA1 tetrodes and rats. The time periods of exploration of familiar object–place pairing A in F conditions were time-matched with those during exploration of familiar object–place pairing A (top row) and novel object–place pairings C, A′, and B (bottom row) in NO+NL (A), NL (B), and NO (C) conditions, respectively. Note that x- and y-axes are shown in log scale. D, Changes in fast and slow gamma power between time-matched periods in the F condition and the three novelty conditions (NO+NL, NL, and NO), during exploration of familiar (A) and novel (ie, C, A′, and B) object–place pairings. Data from individual rats are shown in gray. *Indicates significantly (p < 0.05) different changes in gamma power from familiarization session to novelty session for exploration of novel object–place pairings compared to exploration of familiar object–place pairings; # and ## indicate that the change in gamma power between N and F sessions was significantly (#p < 0.05, ## p < 0.01) greater than zero.

No significant changes in slow and fast gamma power in CA3 during exploration of novel object–place pairings. A–C, Same as in Figure 2A-C , except for CA3 recordings instead of CA1. D, Changes in fast and slow gamma power in CA3 between time-matched periods in the F condition and the three novelty conditions (NO+NL, NL, and NO) during exploration of familiar (A) and novel (ie, C, A′, and B) object–place pairings. Data from individual rats are shown in gray.

Changes in slow and fast gamma phase synchrony between CA3 and CA1 during exploration of novel object–place pairings. The difference in CA3–CA1 slow and fast gamma phase synchrony between exploration periods for novel and familiar object–place pairings in NO+NL (A), NL (B), and NO (C) conditions. The differences in slow and fast gamma interregional phase synchrony between the explorations periods for the two familiar object–place pairings in the F condition are also shown (D). Data from individual rats are shown in gray. **p < 0.01.

Phase-locking of CA3 and CA1 place cell spikes to CA1 slow and fast gamma during exploration of novel object–place pairings. A–C, Mean vector lengths of CA1 slow and fast gamma phase distributions were estimated for spike times of CA3 and CA1 place cells with place fields close to either familiar or novel object–place pairings in the novelty conditions. For the NO+NL condition, place cell spikes were significantly more phase-locked to fast gamma during exploration of the novel object–place pairing than during exploration of the familiar object–place pairing. D, Mean vector lengths of CA1 slow and fast gamma phase distributions were estimated for spike times of CA3 and CA1 place cells with fields near either of the familiar object–place pairings in the familiar condition. E, Example spike time-gamma phase distributions from individual place cells. Spike counts were normalized (ie, number of spikes in each bin/total spike count). A representative place cell from each cell category is shown for fast gamma (top row, red) and slow gamma (bottom row, blue). Grey lines indicate moving average (moving size = 2 bins). **p < 0.01.

CA1 place cell spiking increased selectively in fast gamma periods during exploration of novel object–place pairings. A–C, Examples of color-coded rate maps of CA1 place cells that exhibited place fields close to the novel object–place pairs in the NO+NL (A), NL (B), and NO (C) conditions. Red indicates peak firing rate, dark blue represents no firing, and white pixels indicate unvisited areas. Rate maps constructed from spikes across the entire exploration session are shown in the left columns. Rate maps constructed from spike times during slow and fast gamma episodes are shown in the middle and right columns, respectively. Black dots indicate the defined place fields. Each map is shown scaled to the peak firing rate of the cell across the entire session, which is shown to the left. D, Mean in-field firing rates of CA1 place cells during slow and fast gamma episodes that occurred during exploration of novel or familiar object–place pairings. In these plots, slow and fast gamma episodes were detected from the same tetrodes on which the cells were recorded. E, The same as D, except that slow and fast gamma were detected using different tetrodes than the ones on which cells were recorded. *p < 0.05, **p < 0.01.