Post-learning hippocampal dynamics promote preferential retention of rewarding events

Gruber, Matthias J.; Ritchey, Maureen; Wang, Shao-Fang; Doss, Manoj K.; Ranganath, Charan

doi:10.1016/j.neuron.2016.01.017

Cited by 213Memory and Neural MechanismsMemory Processes and InfluencesSleep and Wakefulness Research

Post-learning hippocampal dynamics promote preferential retention of rewarding events

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Gruber, Matthias J., Ritchey, Maureen, Wang, Shao-Fang, Doss, Manoj K., Ranganath, Charan·2016·Neuron

DOI 10.1016/j.neuron.2016.01.017PMC PMC4777629

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Abstract

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 fMRI to test the effect of reward motivation on post-learning neural dynamics and subsequent memory for objects that were learned in high- and 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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Signs of reward-related biasing of reactivations during sleep and wake have been observed in humans using fMRI.
“Signs of reward-related biasing of reactivations during sleep and wake have been likewise observed in humans using fMRI.”
From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [147]
The Results report preferential reactivation of high-reward contexts in human hippocampal fMRI data during post-learning rest, supporting the wakeful-rest portion of the claim. The Discussion’s references to sleep concern rodent replay and human intracranial recordings, not reward-biased reactivation during sleep measured with human fMRI. Page numbers are unavailable in our copy. (LLM, conf=0.90)
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Authors: Gruber, M. J., Ritchey, M., Wang, S.-F., Doss, M. K., & Ranganath, C.
Affiliations: University of California, Davis (US)
Corresponding author: Gruber, Matthias J.
ORCID: Gruber, Matthias J.
Ritchey, Maureen
Wang, Shao-Fang
Doss, Manoj K.
Venue: Neuron
Publisher: Elsevier BV
Published: 2016-03
Volume: 89
Issue: 5
Pages: 1110-1120
ISSN: 0896-6273 (ISSN-L)
DOI: 10.1016/j.neuron.2016.01.017
PMC: PMC4777629
OpenAlex: W2257753958
Cited by: 212
References: 67
Citations by year: 2026: 10 · 2025: 19 · 2024: 27 · 2023: 18 · 2022: 25 · 2021: 28 · 2020: 17 · 2019: 21 · 2018: 24 · 2017: 16 · 2016: 7
FWCI: 14.41
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 366 d)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: Neuron (publishedVersion)
PubMed (publishedVersion)
ORCA Online Research @Cardiff (Cardiff University) (acceptedVersion)
PubMed Central (acceptedVersion)
eScholarship (California Digital Library) (submittedVersion)
Funders: Office of Naval Research (N00014-15-1-0033)
Guggenheim Fellowship
Parke-Davis Exchange Fellowship from the University of Cambridge
Visiting Professorship from the Leverhulme Trust
K99 NIH Pathway to Independence Award (K99MH103401)
German Academic Exchange Service
German Research Foundation
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
Keywords: reward motivation, memory consolidation, hippocampus, substantia nigra/ventral tegmental area, resting-state functional connectivity, hippocampal reactivation, object memory, reward context
MeSH terms: Adult, Brain Mapping, Female, Hippocampus, Humans, Image Processing, Computer-Assisted, Learning, Magnetic Resonance Imaging, Male, Oxygen, Reaction Time, Retention, Psychology, Reward, Young Adult

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Post-learning hippocampal dynamics promote preferential retention of rewarding events

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