Human Hippocampal Neurons Track Moments in a Sequence of Events

• DOI: 10.1523/jneurosci.3157-20.2021
• Publication Date: 2021-06-28T17:50:15Z
• Authors: Leila Reddy; Benedikt Zoefel; Jessy K. Possel; Judith Peters; Doris E. Dijkster...; Marlene Poncet; Elisabeth C. W. v...; Johannes C. Baayen; Sander Idema; Matthew W. Self
• Keywords: time cells; Adult; Male; 0301 basic medicine; CORTEX; human electrophysiology; BF Psychology; [SDV]Life Sciences [q-bio]; Memory, Episodic; EPISODIC MEMORY RETRIEVAL; 150; NDAS; PLACE; BF; FACES; Sequence learning; human hippocampus; Hippocampus; Human hippocampus; 03 medical and health sciences; temporal coding; Human electrophysiology; 616; SPACE; Humans; [SDV.NEU] Life Sciences [q-bio]/Neurons and Cognition [q-bio.NC]; Temporal coding; Neurons; sequence learning; 0303 health sciences; TIME CELLS; Middle Aged; AC; Time Perception; [SDV.NEU]Life Sciences [q-bio]/Neurons and Cognition [q-bio.NC]; Female; Electrocorticography; Time cells

AbstractAn indispensable feature of episodic memory is our ability to temporally piece together different elements of an experience into a coherent memory. Hippocampal “time cells” – neurons that represent temporal information – may play a critical role in this process. While these cells have been repeatedly found in rodents, it is still unclear to what extent similar temporal selectivity exists in the human hippocampus. Here we show that temporal context modulates the firing activity of human hippocampal neurons during structured temporal experiences. We recorded neuronal activity in the human brain while patients learned predictable sequences of pictures. We report that human time cells fire at successive moments in this task. Furthermore, time cells also signaled inherently changing temporal contexts during empty 10-second gap periods between trials, while participants waited for the task to resume. Finally, population activity allowed for decoding temporal epoch identity, both during sequence learning and during the gap periods. These findings suggest that human hippocampal neurons could play an essential role in temporally organizing distinct moments of an experience in episodic memory.Significance StatementEpisodic memory refers to our ability to remember the “what, where, and when” of a past experience. Representing time is an important component of this form of memory. Here, we show that neurons in the human hippocampus represent temporal information. This temporal signature was observed both when participants were actively engaged in a memory task, as well as during 10s-long gaps when they were asked to wait before performing the task. Furthermore, the activity of the population of hippocampal cells allowed for decoding one temporal epoch from another. These results suggest a robust representation of time in the human hippocampus.