Hippocampal neuronal synchronization in the rat - Dissociation of perception and associative learning.

Learning requires flexible switching between perceiving and encoding external sensory stimuli, making associations with representations already stored in memory (retrieval) and acting accordingly to adapt to the environment. Hippocampus is known to be central in creating mnemonic representations, but how it could support the integration of these processes of memory encoding and retrieval during repetitive learning experiences has remained unknown. In this study, we recorded local-field potentials (LFPs) from the dorsal hippocampus during classical trace eyeblink conditioning in rats. An auditory conditioned stimulus (CS) was followed by a periorbital shock-unconditioned stimulus (US). From the LFPs, we separated hippocampal oscillations that were linked with the variation in the trial-by-trial processing of the CS from those linked with the gradual learning of the CS-US association over daily sessions of training. Short latency transient theta and gamma band oscillations were associated with learning so that both the oscillation amplitudes (strength) and phase locking increased as a function of training. In contrast, long-latency sustained alpha and beta oscillations were associated with perception of CS. These data show divergent oscillatory neural signatures for perception and learning in hippocampal subfields.