A nap to recap or how reward regulates hippocampal-prefrontal memory networks during daytime sleep in humans

Igloi, Kinga; Gaggioni, Giulia; Sterpenich, Virginie; Schwartz, Sophie

doi:10.7554/elife.07903

Cited by 56 publications

(61 citation statements)

References 51 publications

(63 reference statements)

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“…To this end, we blocked dopamine d2-like-receptors -using the selective antagonist Sulpiride -during sleep after participants learned a set of highly or lowly rewarded pictures. We found that, generally, highly rewarded pictures were retained better than lowly rewarded pictures across sleep, which concurs with earlier reports [3,13] and is also in line with reports of sleep preferentially enhancing the retention of highly over lowly rewarded information (e.g., [7]).…”

Section: Discussionsupporting

confidence: 92%

Consolidation of reward memory during sleep does not require dopaminergic activation

Asfestani

Brechtmann

Santiago

et al. 2019

Preprint

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Sleep enhances memories, especially, if they are related to future rewards. Although dopamine has been shown to be a key determinant during reward learning, the role of dopaminergic neurotransmission for amplifying reward-related memories during sleep remains unclear. In the present study, we scrutinize the idea that dopamine is needed for the preferential consolidation of rewarded information. We blocked dopaminergic neurotransmission, thereby aiming to wipe out preferential sleep-dependent consolidation of high over low rewarded memories during sleep. Following a double-blind, balanced, crossover design 20 young healthy men received the dopamine d2-like receptor blocker Sulpiride (800 mg) or placebo, after learning a Motivated Learning Task. The task required participants to memorize 80 highly and 80 lowly rewarded pictures. Half of them were presented for a short (750 ms) and a long duration (1500 ms), respectively, which enabled to dissociate effects of reward on sleep-associated consolidation from those of mere encoding depth. Retrieval was tested after a retention interval of 20 h that included 8 h of nocturnal sleep. As expected, at retrieval, highly rewarded memories were remembered better than lowly rewarded memories, under placebo. However, there was no evidence for an effect of blocking dopaminergic neurotransmission with Sulpiride during sleep on this differential retention of rewarded information. This result indicates that dopaminergic activation is not required for the preferential consolidation of reward-associated memory. Rather it appears that dopaminergic activation only tags such memories at encoding for intensified reprocessing during sleep.

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Section: Discussionsupporting

confidence: 92%

Consolidation of reward memory during sleep does not require dopaminergic activation

Asfestani

Brechtmann

Santiago

et al. 2019

Preprint

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“…Another fruitful approach for future studies might be to relate physiological markers of sleep or consolidation to post-learning RSFC and reactivations. Recently, Igloi et al (2015) showed that learning -related functional connectivity between the hippocampus and the caudate correlated with the number of cortical spindles (recorded via scalp EEG) during a post-learning nap.…”

Section: Discussionmentioning

confidence: 99%

Post-learning Hippocampal Dynamics Promote Preferential Retention of Rewarding Events

Gruber

Ritchey

Wang

et al. 2016

Neuron

188

214

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Reward motivation is known to modulate memory encoding, and this effect depends on interactions between the substantia nigra/ ventral tegmental area complex (SN/VTA) and the hippocampus. It is unknown, however, whether these interactions influence offline neural activity in the human brain that is thought to promote memory consolidation. Here, we used functional magnetic resonance imaging (fMRI) to test the effect of reward motivation on post-learning neural dynamics and subsequent memory for objects that were learned in high- or low-reward motivation contexts. We found that post-learning increases in resting-state functional connectivity between the SN/VTA and hippocampus predicted preferential retention of objects that were learned in high-reward contexts. In addition, multivariate pattern classification revealed that hippocampal representations of high-reward contexts were preferentially reactivated during post-learning rest, and the number of hippocampal reactivations was predictive of preferential retention of items learned in high-reward contexts. These findings indicate that reward motivation alters offline post-learning dynamics between the SN/VTA and hippocampus, providing novel evidence for a potential mechanism by which reward could influence memory consolidation.

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“…Thus, reward does not only support memory consolidation by increasing neuroplasticity in the hippocampus via dopamine release at encoding, but also by potentiating selective replay during sleep after encoding (Singer and Frank, 2009), recently confirmed also by optogenetic stimulation of mouse dopamine VTA-dorsal hippocampus pathway at encoding which enhanced spatial memory and increased reactivation of the stimulated neurons during sharp-wave ripples in post-encoding sleep (McNamara et al, 2014). In fact in humans, reward association or expectation has been shown to boost sleep-related gains in memory (Fischer and Born, 2009;Oudiette et al, 2013;Wilhelm et al, 2011;Igloi et al 2015). Reward circuits may play a role not only in selective memory consolidation during sleep, but also in the generation of dreams.…”

Section: Box 2: Role Of Sleep In the Consolidation And Generalizationmentioning

confidence: 99%

Influence of reward motivation on human declarative memory

Miendlarzewska

Bavelier

Schwartz

2016

Neuroscience & Biobehavioral Reviews

Self Cite

149

134

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a b s t r a c tMotivational relevance can prioritize information for memory encoding and consolidation based on reward value. In this review, we pinpoint the possible psychological and neural mechanisms by which reward promotes learning, from guiding attention to enhancing memory consolidation. We then discuss how reward value can spill-over from one conditioned stimulus to a non-conditioned stimulus. Such generalization can occur across perceptually similar items or through more complex relations, such as associative or logical inferences. Existing evidence suggests that the neurotransmitter dopamine boosts the formation of declarative memory for rewarded information and may also control the generalization of reward values. In particular, temporally-correlated activity in the hippocampus and in regions of the dopaminergic circuit may mediate value-based decisions and facilitate cross-item integration. Given the importance of generalization in learning, our review points to the need to study not only how reward affects later memory but how learned reward values may generalize to related representations and ultimately alter memory structure.

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A nap to recap or how reward regulates hippocampal-prefrontal memory networks during daytime sleep in humans

Cited by 56 publications

References 51 publications

Consolidation of reward memory during sleep does not require dopaminergic activation

Consolidation of reward memory during sleep does not require dopaminergic activation

Post-learning Hippocampal Dynamics Promote Preferential Retention of Rewarding Events

Influence of reward motivation on human declarative memory

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