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The Journal of Neuroscience, July 21, 2004, 24(29):6446-6456; doi:10.1523/JNEUROSCI.0575-04.2004
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Behavioral/Systems/Cognitive
The Ventral Striatum in Off-Line Processing: Ensemble Reactivation during Sleep and Modulation by Hippocampal Ripples
C. M. A. Pennartz,1 E. Lee,1 J. Verheul,1 P. Lipa,2 C. A. Barnes,2 andB. L. McNaughton2 1Graduate School of Neurosciences Amsterdam, University of Amsterdam, Faculty of Science, Swammerdam Institute for Life Sciences, 1090 GB, Amsterdam, The Netherlands, and 2Arizona Research Laboratories Division of Neural Systems, Memory, and Aging, University of Arizona, Tucson, Arizona 85724
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.
Key words: consolidation; memory; nucleus accumbens; reward; sharp waves; tetrodes
Received Feb 18, 2004; revised June 1, 2004; accepted June 2, 2004.
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