The ventral striatum in off-line processing: Ensemble reactivation during sleep and modulation by hippocampal ripples

C. M A Pennartz, E. Lee, J. Verheul, P. Lipa, Carol A Barnes, B. L. McNaughton

Research output: Contribution to journalArticle

178 Citations (Scopus)

Abstract

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 striaturn 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.

Original languageEnglish (US)
Pages (from-to)6446-6456
Number of pages11
JournalJournal of Neuroscience
Volume24
Issue number29
DOIs
StatePublished - Jul 21 2004

Fingerprint

Sleep
Hippocampus
Corpus Striatum
Reward
Consummatory Behavior
Neocortex
Electroencephalography
Ventral Striatum
Neurons
Recurrence
Population

Keywords

  • Consolidation
  • Memory
  • Nucleus accumbens
  • Reward
  • Sharp waves
  • Tetrodes

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

The ventral striatum in off-line processing : Ensemble reactivation during sleep and modulation by hippocampal ripples. / Pennartz, C. M A; Lee, E.; Verheul, J.; Lipa, P.; Barnes, Carol A; McNaughton, B. L.

In: Journal of Neuroscience, Vol. 24, No. 29, 21.07.2004, p. 6446-6456.

Research output: Contribution to journalArticle

Pennartz, C. M A ; Lee, E. ; Verheul, J. ; Lipa, P. ; Barnes, Carol A ; McNaughton, B. L. / The ventral striatum in off-line processing : Ensemble reactivation during sleep and modulation by hippocampal ripples. In: Journal of Neuroscience. 2004 ; Vol. 24, No. 29. pp. 6446-6456.
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