Time cells lead neural reinstatement of episodic memory

Abstract

The episodic memory system provides humans with a unique ability to form and retrieve rich and detailed memories. This capacity requires representing temporal context at encoding and recovering it at retrieval to drive successful recall. Time cells and ramping cells in human medial temporal cortex have been proposed as substrates of temporal context, but whether they participate in context recovery during retrieval remains unknown. Using microelectrode recordings from neurosurgical patients across two classical episodic paradigms, free recall and serial reconstruction, we identify time sensitive neurons and demonstrate that these neuron populations participate in neuronal assemblies and organized sequences on gamma and theta time scales respectively. Consistent with recovery of temporal context predicted by behavioral models of episodic processing, time cell firing precedes the broader assembly population and initiates sequential activation retrieval. These properties predict contextually-mediated recall behavior. We also identify phase coding by complementary populations as convergent mechanisms whose recruitment depends on task demands. Finally, we demonstrate the emergence of context-sensitive neurons in a naturalistic viewing dataset lacking the predictable temporal scaffold of canonical assays. These findings identify cellular mechanisms by which the human medial temporal cortex represents temporal context during episodic encoding and recovers it during retrieval.