Most hippocampal CA1 pyramidal cells in rabbits increase firing during awake sharpwave ripples and some do so in response to external stimulation and theta

Abstract

Hippocampus forms neural representations of real-life events including multimodal information of spatial and temporal context. These representations, i.e. organized sequences of neuronal firing are repeated during following rest and sleep, especially when so-called sharp-wave ripples (SPW-Rs) characterize hippocampal local-field potentials. This SPW-R –related replay is thought to underlie memory consolidation. Here, we set out to explore how hippocampal CA1 pyramidal cells respond to the conditioned stimulus during trace eyeblink conditioning and how these responses manifest during SPW-Rs in awake adult female New Zealand White rabbits. Based on reports in rodents, we expected SPW-Rs to take place in bursts, possibly according to a slow endogenous rhythm. In awake rabbits, half of all SPWRs took place in bursts, but no endogenous slow rhythm appeared. Conditioning trials suppressed SPW-Rs while increasing theta for a period of several seconds. As expected based on previous findings, only a quarter of the putative CA1 pyramidal cells increased firing in response to the conditioned stimulus. Compared to other cells, rate increasing cells were more active during spontaneous epochs of hippocampal theta while response profile during conditioning did not affect firing during SPW-Rs. Taken together, CA1 pyramidal cell firing during SPW-Rs is not limited to cells that fired during the preceding experience. Further, the importance of possible reactivations taking place during theta epochs on memory consolidation warrants further investigation.