Integration of rate and temporal codes by hippocampal cell-assemblies supports theta phase coding of episodic information

Abstract

AbstractSpatial information is encoded by location-dependent hippocampal place cell firing rates and sub-second, rhythmic modulation of spike times. These ‘rate’ and ‘temporal’ codes have primarily been characterized in low-dimensional environments under limited cognitive demands; but how is coding configured in complex environments when individual place cells signal several locations, individual locations contribute to multiple routes and functional demands vary? Quantifying rat CA1 population dynamics during a decision-making task, we show that the phase of individual place cells’ spikes relative to the local theta rhythm shifts to differentiate activity in different place fields. Theta phase coding also disambiguates repeated visits to the same location during different routes, particularly preceding spatial decisions. Using unsupervised detection of cell assemblies alongside theoretical simulation, we show that integrating rate and phase coding mechanisms dynamically recruits units to different assemblies, generating spiking sequences that disambiguate episodes of experience and multiplexing spatial information with cognitive context.