Abstract
Disambiguation of overlapping events is thought to be the hallmark of episodic memory. Recent rodent studies have reported that when navigating overlapping path segments in the different routes place cell activity in the same overlapping path segments were remapped according to different goal locations in different routes. However, it is unknown how hippocampal neurons disambiguate reward delivery in overlapping path segments in different routes. In the present study, we recorded monkey hippocampal neurons during performance of three virtual navigation (VN) tasks in which a monkey alternately navigated two different routes that included overlapping path segments (common central hallway) and acquired rewards in the same locations in overlapping path segments by manipulating a joystick. The results indicated that out of 106 hippocampal neurons, 57 displayed place-related activity (place-related neurons), and 18 neurons showed route-dependent activity in the overlapping path segments, consistent with a hippocampal role in the disambiguation of overlapping path segments. Moreover, 75 neurons showed neural correlates to reward delivery (reward-related neurons), whereas 56 of these 75 reward-related neurons showed route-dependent reward-related activity in the overlapping path segments. The ensemble activity of reward-related neurons represented reward delivery, locations, and routes in the overlapping path segments. In addition, ensemble activity patterns of hippocampal neurons more distinctly represented overlapping path segments than non-overlapping path segments. The present results provide neurophysiological evidence of disambiguation in the monkey hippocampus, consistent with a hippocampal role in episodic memory, and support a recent computational model of “neural differentiation,” in which overlapping items are better represented by repeated retrieval with competitive learning.
Highlights
The hippocampal formation (HF) has been implicated in human episodic memory and spatial navigation (Scoville and Milner, 1957; O’Keefe and Nadel, 1978; Squire and Zola-Morgan, 1991; Tulving and Markowitsch, 1998; Burgess et al, 2002)
We examined whether population activity of place-related and reward-related HF neurons in the overlapping path segments disambiguates overlapping items, and as well as whether reward-related activity across different environmental settings could differentiate multiple environments
Consistent with the results of the present study and previous rodent studies, a computational study suggested that episodic memory regarding routes is used to navigate by cueing retrieval at the choice point (Zilli and Hasselmo, 2008). These findings suggest that route-dependent activity in zone 3 might be involved in future behavioral decision, and that disambiguation of the same path segment in the same environment is a hallmark of the HF in episodic memory (Griffin and Hallock, 2013; Eichenbaum, 2017)
Summary
The hippocampal formation (HF) has been implicated in human episodic memory and spatial navigation (Scoville and Milner, 1957; O’Keefe and Nadel, 1978; Squire and Zola-Morgan, 1991; Tulving and Markowitsch, 1998; Burgess et al, 2002) Consistent with these roles of the HF, neurophysiological studies have reported that HF place cells code subject’s own position in Hippocampal Responses to Overlapping Events a specific place of the environment that the rodents navigate (O’Keefe and Dostrovsky, 1971; McNaughton et al, 1983; Muller and Kubie, 1987; Eichenbaum et al, 1990). Route-dependent neuronal activity in nonhuman primates remains unknown
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