Theta and beta oscillatory dynamics in the dentate gyrus reveal a shift in network processing state during cue encounters

Abstract

The hippocampus is an important structure for learning and memory processes, and has strong rhythmic activity. Although a large amount of research has been dedicated toward understanding the rhythmic activity in the hippocampus during exploratory behaviors, specifically in the theta (5–10 Hz) frequency range, few studies have examined the temporal interplay of theta and other frequencies during the presentation of meaningful cues. We obtained in vivo electrophysiological recordings of local field potentials (LFP) in the dentate gyrus (DG) of the hippocampus as rats performed three different associative learning tasks. In each task, cue presentations elicited pronounced decrements in theta amplitude in conjunction with increases in beta (15–30 Hz) amplitude. These changes were often transient but were sustained from the onset of cue encounters until the occurrence of a reward outcome. This oscillatory profile shifted in time to precede cue encounters over the course of the session, and was not present during similar behaviors in the absence of task relevant stimuli. The observed decreases in theta amplitude and increases in beta amplitude in the DG may thus reflect a shift in processing state that occurs when encountering meaningful cues.

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

“…Stationary moments were distinguished by relatively high beta (13–25 Hz) power in DG and CA3, as well as relative decreases in fast gamma power in CA1 and subiculum and in theta power in all four subregions. The oscillatory patterns associated with stationary moments are consistent with previous studies that reported changes associated with cessation of locomotion (Ahmed & Mehta, 2012; Kemere et al, 2013; Zheng et al, 2015; though Rangel et al, 2015 observed increases in DG beta only when cessation of locomotion occurred at behaviorally relevant locations). The two conditions involving locomotion (i.e., approaching an object or running on a track with no object present) were similar to one another and were distinguished from the other conditions by lower levels of (and perhaps somewhat lower frequency) slow gamma power (relative to object exploration), particularly in DG and CA3, and by high levels of theta power, particularly in CA1 and subiculum.…”

Differential responsivity of neurons in perirhinal cortex, lateral entorhinal cortex, and dentate gyrus during time‐bridging learning

“…Theta‐frequency stimulation of EC stellate inputs to DG induce LTP in CA1 (Stepan et al, ). Theta‐gamma coupling in DG plays a role in spatial learning (Bott et al, ) and in an associative task, cue presentation results in a decrease in theta amplitude (Rangel, Chiba, & Quinn, ). However, whether hippocampal subregions express similar theta modulation during trace eyeblink conditioning remains unclear.…”

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.…”