Coupling of prefrontal gamma amplitude and theta phase is strengthened in trace eyeblink conditioning

Trace eyeblink conditioning requires animals to associate a neutral stimulus (CS) and an aversive periorbital shock (US) that occurred moment later. Acquisition in this conditioning depends on several forebrain regions including the hippocampus, medial prefrontal, and entorhinal cortices in addition to the cerebellum. Activities of single and population neurons in these regions show several patterns of change with the conditioning. For example, the power and synchronization of theta oscillations are correlated with the rate of acquisition. Yet, little is known about how neuronal oscillations at other frequency bands change with the conditioning. The present study examined changes in gamma oscillations, which are typically associated with spiking activity of individual cells. We found that after CS offset the power of gamma oscillations at 35-45 Hz fluctuated at about 7 Hz. This rhythmic fluctuation of gamma power was observed in all three regions and locked to local theta oscillations at 4-8 Hz. Furthermore, over the course of 10 days of acquisition sessions, the coupling of gamma power and theta phase became stronger in the medial prefrontal cortex while it did not change in the hippocampus or lateral entorhinal cortex. Neither theta nor gamma power in any of the regions significantly changed across sessions, rejecting a possibility that the observed increase in prefrontal theta-gamma coupling was secondary to an increase in theta or gamma power. The theta-gamma coupling between different regions did not significantly change across sessions. These results suggest that prefrontal gamma oscillations become more effectively coordinated with concurrent theta oscillations in trace eyeblink conditioning. This may result in a stronger impact of prefrontal neuronal firing responses to the CS on the processing in down-stream regions, such as the lateral entorhinal cortex and/or pontine nuclei.