Reverse replay of behavioural sequences in hippocampal place cells during the awake state

• Published in: Nature 2006-03, Vol.440 (7084), p.680-683
• Main Authors: Foster, David J., Wilson, Matthew A.
• Format: Article
• Language: English
• Subjects: Action Potentials - physiology; Animals; Behavior - physiology; Biological and medical sciences; Brain; Electrophysiology; Fundamental and applied biological sciences. Psychology; Hippocampus - cytology; Hippocampus - physiology; Humanities and Social Sciences; Learning; Learning - physiology; letter; Memory; Memory - physiology; Models, Neurological; multidisciplinary; Neurology; Primates; Rats; Rest - physiology; Rodents; Running - physiology; Science; Science (multidisciplinary); Sleep; Sleep. Vigilance; Space Perception - physiology; Vertebrates: nervous system and sense organs; Wakefulness - physiology
• ISSN: 0028-0836; 1476-4687; 1476-4679
• DOI: 10.1038/nature04587

Run that by me again... During sleep, neurons in the rat hippocampus are known to replay sequences of activity that took place when the rat was awake. A new study, in rats running around a track, eating and grooming, shows that replay also occurs repeatedly during the awake state, and that behavioural sequences are replayed in reverse order . Theories of spatial learning have previously suggested that reverse replay might be useful. Replay during the awake state might also explain in part why learning can be more effective if learning sessions are spaced out in time rather than clustered together, why hyperactivity causes learning problems, and why simply being awake and resting can help learning. The hippocampus has long been known to be involved in spatial navigational learning in rodents 1 , 2 , and in memory for events in rodents 3 , 4 , primates 5 and humans 6 . A unifying property of both navigation and event memory is a requirement for dealing with temporally sequenced information. Reactivation of temporally sequenced memories for previous behavioural experiences has been reported in sleep in rats 7 , 8 . Here we report that sequential replay occurs in the rat hippocampus during awake periods immediately after spatial experience. This replay has a unique form, in which recent episodes of spatial experience are replayed in a temporally reversed order. This replay is suggestive of a role in the evaluation of event sequences in the manner of reinforcement learning models. We propose that such replay might constitute a general mechanism of learning and memory.