Gamma Oscillations in Rat Hippocampal Subregions Dentate Gyrus, CA3, CA1, and Subiculum Underlie Associative Memory Encoding

Abstract

SUMMARY Neuronal oscillations in the rat hippocampus relate to both memory and locomotion, raising the question of how these cognitive and behavioral correlates interact to determine the oscillatory network state of this region. Here, rats freely locomoted while performing an object-location task designed to test hippocampus-dependent spatial associative memory. Rhythmic activity in theta, beta, slow gamma, and fast gamma frequency ranges were observed in both action potentials and local field potentials (LFPs) across four main hippocampal subregions. Several patterns of LFP oscillations corresponded to overt behavior (e.g., increased dentate gyrus-CA3 beta coherence during stationary moments and CA1-subiculum theta coherence during locomotion). In comparison, slow gamma (~40 Hz) oscillations throughout the hippocampus related most specifically to object-location associative memory encoding rather than overt behavior. The results help to untangle how hippocampal oscillations relate to both memory and motion, and single out slow gamma oscillations as a distinguishing correlate of spatial associative memory.

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

“…Indeed, the DG and its inputs have a strong, behaviorally relevant, temporal structure 42,69,70 . Novelty experience can induce increased gamma and beta range activity 41,71,72 , and explorative activity with rearing is also associated with increased gamma oscillations 73 . A recent model has addressed how fast, rhythmic gamma-frequency feedback inhibition may implement a type of 'k-winners-take-all' operation, a basic computational component of pattern separation models 60 , though this model relies on faster synaptic timescales than we observed in our compound IPSCs.…”

“…A recent model has addressed how fast, rhythmic gamma-frequency feedback inhibition may implement a type of 'k-winners-take-all' operation, a basic computational component of pattern separation models 60 , though this model relies on faster synaptic timescales than we observed in our compound IPSCs. 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.…”

“…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] .…”

“…Specifically, we created input trains with constant mean rate, but with either theta (10 Hz) or slow-gamma (30 Hz) modulation ( Supplementary Figs. 6C, 7A), which are prominent during exploration and novelty exposure respectively 41,44 . To model rapid pattern separation in behaviorally relevant timescale we chose an input duration of approximately five theta cycles (600ms, corresponding to the approximate duration of place cell spiking during traversal of its place field).…”

Impairments in Hippocampal Place Cell Sequences during Errors in Spatial Memory

“…A number of rodent studies have also related gamma rhythms to performance on mnemonic tasks [22][23][24][25][26][27][28][29][30] . In addition, recent studies have shown that low (~25-55 Hz) and high (~60-100 Hz) frequencies of hippocampal gamma activity are associated with CA3 and entorhinal cortex inputs to subfield CA1 [31][32][33][34] , respectively, raising the possibility that "slow" and "fast" gamma subtypes facilitate transmission of different inputs to CA1 place cells.…”