Boundary cells in the representation of episodes in the human hippocampus

Abstract

The representation of episodes is a fundamental requirement for forming episodic memories, but the specific electrophysiological mechanisms supporting episode construction in the human hippocampus remain unknown. Experiments in rodent models indicate that a population of neurons sensitive to edges of an environment, termed border or boundary neurons in spatial navigation, fulfills a role analogous to episode demarcation. We hypothesized that such boundary neurons could be identified in the human mesial temporal lobe, with firing rates sensitive specifically to the beginning and end of mnemonically-relevant episodes in the free recall task. Using a generalized linear model to control for factors such as encoding success and item onset times along with other variables, we found 44 Boundary neurons out of a total 736 single neurons recorded across 27 subjects. We distinguish boundary neurons from a separate population of ramping neurons, which are time-sensitive neurons whose activity provides complementary but distinct information during episodic representation. We also describe evidence that the firing of boundary neurons within the preferred windows (at the beginning and end of episodes) is organized by hippocampal theta oscillations, using spike-field coherence metrics.