The Ventral Striatum in Off-Line Processing: Ensemble Reactivation during Sleep and Modulation by Hippocampal Ripples

By Cyriel M. A. Pennartz, Eunjeong Lee, J. Verheul, Peter Lipa, C. A. Barnes, Bruce L. McNaughton. 2004

297 citations recorded by the source corpus.

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.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience

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Citations in the corpus

Cellular and neurochemical basis of sleep stages in the thalamocortical network (2016, background): “Precise coordination of different EEG rhythms during sleep is believed to be critical for memory consolidation which manifests in reactivation of specific neural activity patterns – sleep replay – that have been observed in different brain areas including the hippocampus, amygdala, neocortex and str”
Sequence Learning and the Role of the Hippocampus in Rodent Navigation (2012, unknown): “Moreover, ventral striatum neurons exhibit a close connection to fine-timescale dynamics in the hippocampal representation of state, specifically theta phase precession [25 ], forward sweeps [23 ], and replay [22,27,28], which are discussed in the following sections.”
Reward-motivated learning: mesolimbic activation precedes memory formation. (2006, background): “…MTL neural activity (Weiss et al., 2003), and conversely, that neural activity in the MTL influences activity in the NAcc (Pennartz and Kitai, 1991; Pennartz et al., 2004; Tabuchi et al., 2000) and the VTA (Floresco et al., 2001; Lodge and Grace, 2005), but previous research has not demonstrated…”
High-density, long-lasting, and multi-region electrophysiological recordings using polymer electrode arrays (2018, unknown): “, 2003) and subcortical regions (Dragoi et al., 1999; Lansink et al., 2009; Pennartz et al., 2004) show changes in firing rates around the time of SWRs.”
Sleep spindles predict neural and behavioral changes in motor sequence consolidation (2013, result): “The latter hypothesis is supported by several studies in rodents [Pennartz et al., 2004] and humans [Maquet et al.”
Current issues related to motor sequence learning in humans (2018, result): “Although still conjectural, however, animal [62] and human [21,22] work also suggest that a similar neurophysiological mechanism involving the interplay between the hippocampus and striatum might take place during the post-learning sleep episodes, hence possibly mediating the off-line memory enhance”
Neural Ensembles in CA3 Transiently Encode Paths Forward of the Animal at a Decision Point (2007, background): “The hippocampus projects to ventral striatum (McGeorge and Faull, 1989; Finch, 1996; Swanson, 2000) and ventral striatal firing patterns reflect hippocampal neural activity (Martin, 2001; Pennartz et al., 2004).”
Replay Comes of Age. (2017, background): “Indeed, both nucleus accumbens (Lansink et al. 2009, Pennartz et al. 2004) and prefrontal cortex ( Jadhav et al. 2016) exhibit activity that is temporally coordinated with hippocampal replay, as is the activity of dopamine neurons in the ventral tegmental area (Gomperts et al. 2015), in line with…”
Sleep and the Price of Plasticity: From Synaptic and Cellular Homeostasis to Memory Consolidation and Integration (2014, background): “…and Wilson, 1998; Sirota et al., 2003) may provide conditions conducive to long-term potentiation (e.g., Buzsáki, 1989; Louie and Wilson, 2001; Pennartz et al., 2004), because they may result in a large influx of calcium inside dendrites (Sejnowski and Destexhe, 2000; Steriade and Timofeev,…”
A unified framework for addiction: Vulnerabilities in the decision process (2008, background): “& Eastwood, B. (2005) Experimental manipulation of attentional bias increases the motivation to drink alcohol.”
Brain plasticity related to the consolidation of motor sequence learning and motor adaptation (2010, result): “Such interpretation is consistent with rodents’ work, which showed that reactivation during posttraining sleep can be observed in the ventral striatum after animals are trained on a reward-searching procedural task (28), as well as with previous positron emission tomography studies in humans, which ”