Sharp Wave Ripple Replay of Hippocampal Cells that Represent a Non-spatial Dimension

Abstract

The role of the hippocampus in spatial navigation tasks has been well characterized, especially by studies of place cells, which fire preferentially in specific parts of the physical environment and can form sequences corresponding to stereotyped trajectories. Additionally, long-term consolidation of memories is known to depend on sharp wave ripples (SWRs), hippocampus-wide synchronous bursts of activity often accompanied by replay of previously generated place cell sequences. During these replay events, cortical regions become active, suggesting that hippocampal-cortical interactions during SWRs serve as a conduit for memory consolidation. The exact nature of these interactions and the extent of cortical activation is not well understood. The current understanding of the hippocampus assumes spatial position is the default contextual variable for which hippocampal representations are formed. In a sound manipulation experiment, we showed that place cells can form discrete firing fields correlated to sound frequency and also combinations of contextual variables. Furthermore, we found evidence of SWR replay during these tasks, suggesting that the same circuit responsible for representation of spatial positions and long-term consolidation of learned trajectories performs both functions for nonspatial parameters.