Phase-locked hippocampal theta-band responses are related to discriminative eyeblink conditioned responding

Hippocampal electrophysiological oscillatory activity is undoubtedly related to learning and memory. The relative power of spontaneously occurring hippocampal theta (∼4-8 Hz) oscillations predicts how fast and how well an animal will learn: more theta predicts faster acquisition of the conditioned response in eyeblink conditioning in both rats and rabbits. Here, our aim was to study how hippocampal theta-band responses to conditioned stimuli elicited during very-long delay discrimination eyeblink conditioning relate to the accompanying conditioned behavior. We trained adult male New Zealand White rabbits using 1500-ms auditory stimuli as conditioned stimuli and a 100-ms airpuff as an unconditioned stimulus. The reinforced conditioned stimulus overlapped and co-terminated with the unconditioned stimulus whereas the non-reinforced conditioned stimulus was always presented alone. Consistent with previous results, hippocampal theta-band responses to the conditioned stimuli diminished in amplitude across training. Interestingly, hippocampal theta-band responses were most consistently time-locked when a well-trained animal failed to suppress behavioral learned responses to the non-reinforced conditioned stimulus. We suggest that phase-locking of hippocampal theta-band oscillations in response to external stimuli reflects retrieval of the dominant memory trace (adaptive or not) along with initiating the most prominent action scheme related to that memory trace.