Context-dependent incremental timing cells in the primate hippocampus

Significance Episodic memory refers to the ability to recall specifics of past events in our lives. An essential aspect of events is timing when things occur during an episode. A number of recent studies have shown that the hippocampus, a structure known to be essential to form episodic memories, possesses neurons that explicitly mark moments in time. We add a previously unidentified finding to this work by showing that individual primate hippocampal neurons not only track time, but do so only when specific contextual information (e.g., object identity/location) is cued. These time context-sensitive neurons represent a novel way in which the brain unites disparate streams that comprise an episode and will aid in our understanding of how we store and retrieve episodic memories. We examined timing-related signals in primate hippocampal cells as animals performed an object-place (OP) associative learning task. We found hippocampal cells with firing rates that incrementally increased or decreased across the memory delay interval of the task, which we refer to as incremental timing cells (ITCs). Three distinct categories of ITCs were identified. Agnostic ITCs did not distinguish between different trial types. The remaining two categories of cells signaled time and trial context together: One category of cells tracked time depending on the behavioral action required for a correct response (i.e., early vs. late release), whereas the other category of cells tracked time only for those trials cued with a specific OP combination. The context-sensitive ITCs were observed more often during sessions where behavioral learning was observed and exhibited reduced incremental firing on incorrect trials. Thus, single primate hippocampal cells signal information about trial timing, which can be linked with trial type/context in a learning-dependent manner.