Fast gamma rhythms in the hippocampus promote encoding of novel object-place pairings

Abstract

Hippocampal gamma rhythms increase during mnemonic operations (Johnson and Redish, 2007; Montgomery and Buzsaki, 2007; Sederberg et al., 2007; Jutras et al., 2009; Trimper et al., 2014) and may affect memory encoding by coordinating activity of neurons that code related information (Jensen and Lisman, 2005). Here, a hippocampal-dependent, object-place association task (Clark et al., 2000; Broadbent et al., 2004; Eacott and Norman, 2004; Lee et al., 2005; Winters et al., 2008; Barker and Warburton, 2011) was used in rats to investigate how slow and fast gamma rhythms in the hippocampus relate to encoding of memories for novel object-place associations. In novel object tasks, the degree of hippocampal dependence has been reported to vary depending on the type of novelty (Eichenbaum et al., 2007; Winters et al., 2008). Therefore, gamma activity was examined during three novelty conditions: a novel object presented in a location where a familiar object had been (NO), a familiar object presented in a location where no object had been (NL), and a novel object presented in a location where no object had been (NO+NL). The strongest and most consistent effects were observed for fast gamma rhythms during the NO+NL condition. Fast gamma power, CA3-CA1 phase synchrony, and phase-locking of place cell spikes increased during exploration of novel, compared to familiar, object-place associations. Additionally, place cell spiking during exploration of novel object-place pairings was increased when fast gamma rhythms were present. These results suggest that fast gamma rhythms promote encoding of memories for novel object-place associations.

Significance Statement: This study provides the first evidence that links fast gamma rhythms in the hippocampus to encoding of novel object-place associations in a behavioral task. The results also relate these effects to firing patterns in place cells that resemble stimulation patterns that are routinely used to induce long-term potentiation, the presumed synaptic substrate of memory formation.