Gamma oscillations coordinate amygdalo-rhinal interactions during learning.

The rhinal cortices contribute to memory formation by integrating and transferring neocortical information to the hippocampus. Rhinal contributions to memory are likely influenced by the amygdala because strong reciprocal connections exist between these structures. In light of previous data showing that oscillations regulate neuronal activity during memory formation and recall, we tested the possibility that coherent oscillations serve to coordinate amygdalo-rhinal activity during learning. To this end, we performed simultaneous extracellular recordings of basolateral amygdala (BLA), perirhinal, and entorhinal activity. We first tested whether there are correlated fluctuations in the power of BLA and rhinal field activity during the waking state. Correlated power fluctuations were most pronounced in the 35-45 Hz band. Within each structure, firing probability fluctuated rhythmically with the fast oscillations, indicating that they were not volume conducted. To test whether fast oscillations coordinate BLA and rhinal activity during learning, animals were trained on a trace-conditioning task in which a visual conditioned stimulus (CS) predicted a food reward after a delay. The predictive value of the CS was learned gradually over 9 d. As learning progressed, the 35-45 Hz power increased in the BLA and rhinal cortices, particularly during the late part of the CS and delay. Moreover, the firing of BLA and rhinal neurons became rhythmically entrained by BLA oscillations at that time. Thus, our data suggest that neuronal interactions are coordinated by fast oscillations in the BLA-rhinal network. By telescoping the periods of effective neuronal interactions in short recurring time windows, these fast oscillations may facilitate rhinal interactions and synaptic plasticity.