The ventral striatum in off-line processing: ensemble reactivation during sleep and modulation by hippocampal ripples.
Previously it has been shown that the hippocampus and neocortex can spontaneously reactivate ensemble activity patterns during post-behavioral sleep and rest periods. Here we examined whether such reactivation also occurs in a subcortical structure, the ventral striatum, which receives a direct input from the hippocampal formation and has been implicated in guidance of consummatory and conditioned behaviors. During a reward-searching task on a T-maze, flanked by sleep and rest periods, parallel recordings were made from ventral striatal ensembles while EEG signals were derived from the hippocampus. Statistical measures indicated a significant amount of reactivation in the ventral striatum. In line with hippocampal data, reactivation was especially prominent during post-behavioral slow-wave sleep, but unlike the hippocampus, no decay in pattern recurrence was visible in the ventral striatum across the first 40 min of post-behavioral rest. We next studied the relationship between ensemble firing patterns in ventral striatum and hippocampal ripples-sharp waves, which have been implicated in pattern replay. Firing rates were significantly modulated in close temporal association with hippocampal ripples in 25% of the units, showing a marked transient enhancement in the average response profile. Strikingly, ripple-modulated neurons in ventral striatum showed a clear reactivation, whereas nonmodulated cells did not. These data suggest, first, the occurrence of pattern replay in a subcortical structure implied in the processing and prediction of reward and, second, a functional linkage between ventral striatal reactivation and a specific type of high-frequency population activity associated with hippocampal replay.
Graduate School of Neurosciences Amsterdam, University of Amsterdam, Faculty of Science, Swammerdam Institute for Life Sciences, 1090 GB, Amsterdam, The Netherlands. pennartz@science.uva.nl
C M A
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Pennartz
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Lee
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Verheul
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Lipa
C A
CA
Barnes
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McNaughton
D000200:Action Potentials; D000818:Animals; D001479:Basal Ganglia / Q000502:physiology*; D001522:Behavior, Animal; D003213:Conditioning, Psychological; D004569:Electroencephalography; D006624:Hippocampus / Q000502:physiology*; D008297:Male; D009474:Neurons / Q000502:physiology; D051381:Rats; D011916:Rats, Inbred F344; D012201:Reward; D012890:Sleep / Q000502:physiology*