Time Cells in Hippocampal Area CA3

Abstract

Studies on time cells in the hippocampus have so far focused on area CA1 in animals performing memory tasks. Some studies have suggested that temporal processing within the hippocampus may be exclusive to CA1 and CA2, but not CA3, and may occur only under strong demands for memory. Here we examined the temporal and spatial coding properties of CA3 and CA1 neurons in rats performing a maze task that demanded working memory and a control task with no explicit working memory demand. In the memory demanding task, CA3 cells exhibited robust temporal modulation similar to the pattern of time cell activity in CA1, and the same populations of cells also exhibited typical place coding patterns in the same task. Furthermore, the temporal and spatial coding patterns of CA1 and CA3 were equivalently robust when animals performed a simplified version of the task that made no demands on working memory. However, time and place coding did differ in that the resolution of temporal coding decreased over time within the delay interval, whereas the resolution of place coding was not systematically affected by distance along the track. These findings support the view that CA1 and CA3 both participate in encoding the temporal and spatial organization of ongoing experience.

Viewpoints: how the hippocampus contributes to memory, navigation and cognition

“…Importantly, the division of time by time cells in hippocampus depends on having a goal: when rats simply run on a running wheel in a place field, cells fire at their place fields forever at a specific phase, but when rats have a goal of running in the wheel for a set time, the ensemble divides up the time with time cells 21,89 . Division of time by time cells seems to depend on having a target time but does not depend on maintaining working memory across that time 90 , consistent with place cells that divide up space, whether that space is necessary for navigation or not (in contrast, for example, to striatal cells that only represent space, time, or other information when it provides useful signals for getting reward).…”

Temporal and spatial context in the mind and brain

“…These predictions resemble the properties of hippocampal “time cells” that fire sequentially during a circumscribed period within a delay period [60, 49]. Consistent with the hypothesis that the compressed representation of the past is accessed in many different forms of memory, time cells are not only observed in the hippocampus [51], but also the entorhinal cortex [52], striatum [54, 61], and medial PFC [53, 62]. Notably, in all of these studies, time cells show a characteristic compression as qualitatively predicted by theory (Fig.…”

“…The theoretical framework in [50] predicts a linear increase. Clockwise from top left, rodent hippocampus (different colors for CA1 vs CA3) [51], rodent medial entorhinal cortex (different colors show grid cells vs non-grid cells [52], medial prefrontal cortex [53], and striatum (different colors are different delay durations) [54]. …”

Nonspatial sequence coding varies along the CA1 transverse axis

“…Several prominent computational models have suggested that the unique neural architecture of CA3 (high density of recurrent collaterals) is well suited for sequence coding (e.g., McNaughton and Morris, 1987;Levy, 1996;Lisman, 1999), which is consistent with our preliminary findings that CA3 inactivations during task performance impair learning of a novel sequence (Asem et al, 2016). Notably, a different form of nonspatial temporal coding was recently reported in CA3 as well as in CA1 ("time cells"; Salz et al, 2016). Recent studies also suggest a potential role for CA2 in temporal coding (Mankin et al, 2015).…”