Theta and gamma oscillations in the rat hippocampus during attentive lever pressing

Abstract

The hippocampus is known to be pivotal for spatial memory but emerging evidence suggests its contribution to temporal memories as well. However, it is not clear how the hippocampus represents time and how it synchronizes spatial and temporal presentations into a coherent memory. We assessed the specific role of hippocampal theta and gamma oscillations and their interaction in short-term timing of motor reactions. Rats were trained to maintain lever pressing for 2.5 s and then to quickly release the lever and retrieve water reward from a nearby water port guided by a cue light. In essence, this task allows observation of hippocampal rhythms during timed anticipation when no overt movements take place. Then we implanted wire electrodes to five hippocampal layers for recording local field potentials during the task. Consistent with earlier reports, theta showed a declining trend during the lever press. We also found that fast-gamma declined in tandem with theta while slow-gamma showed an opposite trend. Theta-phase to gamma-amplitude cross-frequency coupling measured with modulation index (MI) varied significantly between the three task phases. Interestingly, also changes in MI were opposite for fast- and slow-gamma. The MI was also related to the task performance, so that during omission trials the MI for fast-gamma in CA1 was smaller than during trials with premature lever release. In addition, the MI in dentate hilus was higher during all error trials than during correctly performed trials. Collectively, these data suggest an important role of synchronization of hippocampal theta and gamma rhythms to timing of cued motor reactions.