The DOI matches its Crossref record; 67 of the 67 references it cites were found in a registry or an index.
Post-learning Hippocampal Dynamics Promote Preferential Retention of Rewarding Events
Open accessAbstract
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.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“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]
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages
Cox, R. W. (1996) · Computers and Biomedical Research · doi:10.1006/cbmr.1996.0014 · Cited by 10,913
The Nature of Recollection and Familiarity: A Review of 30 Years of Research
Yonelinas, A. P. (2002) · Journal of Memory and Language · doi:10.1006/jmla.2002.2864 · Cited by 3,840
The reward circuit: linking primate anatomy and human imaging
Haber, S. N., & Knutson, B. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.129 · Cited by 3,718
Large-scale automated synthesis of human functional neuroimaging data.
Yarkoni, T., Poldrack, R. A., Nichols, T. E., Van Essen, D. C., & Wager, T. D. (2011) · Nature Methods · doi:10.1038/nmeth.1635 · Cited by 3,686
The Medial Temporal Lobe and Recognition Memory
Eichenbaum, H., Yonelinas, A. P., & Ranganath, C. (2007) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.30.051606.094328 · Cited by 2,580
Self-citationAnticipation of Increasing Monetary Reward Selectively Recruits Nucleus Accumbens
Knutson, B., Adams, C. M., Fong, G. W., & Hommer, D. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-16-j0002.2001 · Cited by 2,244
The organization of recent and remote memories
Frankland, P. W., & Bontempi, B. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1607 · Cited by 2,138
The hippocampal-VTA loop: controlling the entry of information into long-term memory
Lisman, J. E., & Grace, A. A. (2005) · Neuron · doi:10.1016/j.neuron.2005.05.002 · Cited by 1,983
Hippocampal sharp wave-ripple: A cognitive biomarker for episodic memory and planning
Buzsáki, G. (2015) · Hippocampus · doi:10.1002/hipo.22488 · Cited by 1,759
Reverse replay of behavioural sequences in hippocampal place cells during the awake state
Foster, D. J., & Wilson, M. A. (2006) · Nature · doi:10.1038/nature04587 · Cited by 1,727
Coordinated memory replay in the visual cortex and hippocampus during sleep
Ji, D., & Wilson, M. A. (2007) · Nature Neuroscience · doi:10.1038/nn1825 · Cited by 1,669
Interplay of Hippocampus and Prefrontal Cortex in Memory
Preston, A. R., & Eichenbaum, H. (2013) · Current Biology · doi:10.1016/j.cub.2013.05.041 · Cited by 1,389
Amunts, K., Kedo, O., Kindler, M., Pieperhoff, P., Mohlberg, H., Shah, N. J., Habel, U., Schneider, F., & Zilles, K. (2005) · Anatomy and Embryology · doi:10.1007/s00429-005-0025-5 · Cited by 1,264
Imaging recollection and familiarity in the medial temporal lobe: a three-component model
Diana, R. A., Yonelinas, A. P., & Ranganath, C. (2007) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2007.08.001 · Cited by 1,231
Visual long-term memory has a massive storage capacity for object details
Brady, T. F., Konkle, T., Alvarez, G. A., & Oliva, A. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0803390105 · Cited by 1,106
Reward-motivated learning: mesolimbic activation precedes memory formation
Adcock, R. A., Thangavel, A., Whitfield-Gabrieli, S., Knutson, B., & Gabrieli, J. D. E. (2006) · Neuron · doi:10.1016/j.neuron.2006.03.036 · Cited by 977
Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval
Carr, M. F., Jadhav, S. P., & Frank, L. M. (2011) · Nature Neuroscience · doi:10.1038/nn.2732 · Cited by 958
Staresina, B. P., Bergmann, T. O., Bonnefond, M., van der Meij, R., Jensen, O., Deuker, L., Elger, C. E., Axmacher, N., & Fell, J. (2015) · Nature Neuroscience · doi:10.1038/nn.4119 · Cited by 831
States of Curiosity Modulate Hippocampus-Dependent Learning via the Dopaminergic Circuit
Gruber, M. J., Gelman, B. D., & Ranganath, C. (2014) · Neuron · doi:10.1016/j.neuron.2014.08.060 · Cited by 812
Self-citationShohamy, D., & Adcock, R. A. (2010) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2010.08.002 · Cited by 736
Wittmann, B. C., Schott, B. H., Guderian, S., Frey, J. U., Heinze, H.-J., & Düzel, E. (2005) · Neuron · doi:10.1016/j.neuron.2005.01.010 · Cited by 698
Mather, M., Clewett, D., Sakaki, M., & Harley, C. W. (2016) · Behavioral and Brain Sciences · doi:10.1017/s0140525x15000667 · Cited by 695
Category-Specific Cortical Activity Precedes Retrieval During Memory Search
Polyn, S. M., Natu, V. S., Cohen, J. D., & Norman, K. A. (2005) · Science · doi:10.1126/science.1117645 · Cited by 690
Enhanced Brain Correlations during Rest Are Related to Memory for Recent Experiences
Tambini, A., Ketz, N., & Davachi, L. (2010) · Neuron · doi:10.1016/j.neuron.2010.01.001 · Cited by 596
Absolute Coding of Stimulus Novelty in the Human Substantia Nigra/VTA
Bunzeck, N., & Düzel, E. (2006) · Neuron · doi:10.1016/j.neuron.2006.06.021 · Cited by 503
Dopaminergic neurons promote hippocampal reactivation and spatial memory persistence
McNamara, C. G., Tejero-Cantero, Á., Trouche, S., Campo-Urriza, N., & Dupret, D. (2014) · Nature Neuroscience · doi:10.1038/nn.3843 · Cited by 486
A neoHebbian framework for episodic memory; role of dopamine-dependent late LTP
Lisman, J., Grace, A. A., & Duzel, E. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.07.006 · Cited by 465 · cited 3×
“In line with the idea that dopamine affects late LTP (Lisman et al., 2011), McNamara et al. (2014) demonstrated that dopaminergic stimulation via optogenetics during hippocampus-dependent learning led specifically to increased reactivation of hippocampal firing patterns during a post-learning period, but dopaminergic…”
BackgroundHippocampal-cortical interaction during periods of subcortical silence
Logothetis, N. K., Eschenko, O., Murayama, Y., Augath, M., Steudel, T., Evrard, H. C., Besserve, M., & Oeltermann, A. (2012) · Nature · doi:10.1038/nature11618 · Cited by 420
Hippocampus leads ventral striatum in replay of place-reward information
Lansink, C. S., Goltstein, P. M., Lankelma, J. V., McNaughton, B. L., & Pennartz, C. M. A. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000173 · Cited by 400
Rewarded Outcomes Enhance Reactivation of Experience in the Hippocampus
Singer, A. C., & Frank, L. M. (2009) · Neuron · doi:10.1016/j.neuron.2009.11.016 · Cited by 385
Memory trace reactivation in hippocampal and neocortical neuronal ensembles
Sutherland, G. (2000) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00079-9 · Cited by 384
McKenzie, S., Frank, A. J., Kinsky, N. R., Porter, B., Rivière, P. D., & Eichenbaum, H. (2014) · Neuron · doi:10.1016/j.neuron.2014.05.019 · Cited by 373
Ripples in the medial temporal lobe are relevant for human memory consolidation
Axmacher, N., Elger, C. E., & Fell, J. (2008) · Brain · doi:10.1093/brain/awn103 · Cited by 372
Hippocampal ripples and memory consolidation
Girardeau, G., & Zugaro, M. (2011) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.02.005 · Cited by 330
Pennartz, C. M. A., Lee, E., Verheul, J., Lipa, P., Barnes, C. A., & McNaughton, B. L. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.0575-04.2004 · Cited by 282
Memory Consolidation by Replay of Stimulus-Specific Neural Activity
Deuker, L., Olligs, J., Fell, J., Kranz, T. A., Mormann, F., Montag, C., Reuter, M., Elger, C. E., & Axmacher, N. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0414-13.2013 · Cited by 273
Offline Persistence of Memory-Related Cerebral Activity during Active Wakefulness
Peigneux, P., Orban, P., Balteau, E., Degueldre, C., Luxen, A., Laureys, S., & Maquet, P. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040100 · Cited by 263
Persistence of hippocampal multivoxel patterns into postencoding rest is related to memory
Tambini, A., & Davachi, L. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1308499110 · Cited by 230
The Role of Memory Reactivation during Wakefulness and Sleep in Determining Which Memories Endure
Oudiette, D., Antony, J. W., Creery, J. D., & Paller, K. A. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.5497-12.2013 · Cited by 220
Awake reactivation predicts memory in humans
Staresina, B. P., Alink, A., Kriegeskorte, N., & Henson, R. N. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1311989110 · Cited by 219
Internally generated sequences in learning and executing goal-directed behavior
Pezzulo, G., van der Meer, M. A. A., Lansink, C. S., & Pennartz, C. M. A. (2014) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2014.06.011 · Cited by 217
Functional imaging of the human dopaminergic midbrain
Düzel, E., Bunzeck, N., Guitart-Masip, M., Wittmann, B., Schott, B. H., & Tobler, P. N. (2009) · Trends in Neurosciences · doi:10.1016/j.tins.2009.02.005 · Cited by 216
Guitart-Masip, M., Fuentemilla, L., Bach, D. R., Huys, Q. J. M., Dayan, P., Dolan, R. J., & Duzel, E. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.6376-10.2011 · Cited by 216
VTA neurons coordinate with the hippocampal reactivation of spatial experience
Gomperts, S. N., Kloosterman, F., & Wilson, M. A. (2015) · eLife · doi:10.7554/elife.05360 · Cited by 191
Memory trace replay: The shaping of memory consolidation by neuromodulation
Atherton, L. A., Dupret, D., & Mellor, J. R. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2015.07.004 · Cited by 180
Off-line replay maintains declarative memories in a model of hippocampal-neocortical interactions
Káli, S., & Dayan, P. (2004) · Nature Neuroscience · doi:10.1038/nn1202 · Cited by 175
Preferential Reactivation of Motivationally Relevant Information in the Ventral Striatum
Lansink, C. S., Goltstein, P. M., Lankelma, J. V., Joosten, R. N. J. M. A., McNaughton, B. L., & Pennartz, C. M. A. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1054-08.2008 · Cited by 168
Murty, V. P., & Adcock, R. A. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht063 · Cited by 167
Murayama, K., & Kitagami, S. (2013) · Journal of Experimental Psychology General · doi:10.1037/a0031992 · Cited by 163
Wolosin, S. M., Zeithamová, D., & Preston, A. R. (2012) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00237 · Cited by 162
Delay-dependent contributions of medial temporal lobe regions to episodic memory retrieval
Ritchey, M., Montchal, M. E., Yonelinas, A. P., & Ranganath, C. (2015) · eLife · doi:10.7554/elife.05025 · Cited by 148
Self-citationKahn, I., & Shohamy, D. (2012) · Hippocampus · doi:10.1002/hipo.22077 · Cited by 139
Libby, L. A., Hannula, D. E., & Ranganath, C. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0655-14.2014 · Cited by 137
Money enhances memory consolidation – But only for boring material
Murayama, K., & Kuhbandner, C. (2011) · Cognition · doi:10.1016/j.cognition.2011.01.001 · Cited by 130
Memory reactivation during rest supports upcoming learning of related content
Schlichting, M. L., & Preston, A. R. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1404396111 · Cited by 126
Moderate levels of activation lead to forgetting in the think/no-think paradigm
Detre, G. J., Natarajan, A., Gershman, S. J., & Norman, K. A. (2013) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2013.02.017 · Cited by 120
Farovik, A., Place, R., McKenzie, S., Porter, B. S., Munro, C. E., & Eichenbaum, H. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0134-15.2015 · Cited by 105
Diversity of sharp-wave–ripple LFP signatures reveals differentiated brain-wide dynamical events
Ramírez-Villegas, J. F., Logothetis, N. K., & Besserve, M. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1518257112 · Cited by 105
Moderate Excitation Leads to Weakening of Perceptual Representations
Newman, E. L., & Norman, K. A. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhq021 · Cited by 104
Tompary, A., Duncan, K. D., & Davachi, L. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.4816-14.2015 · Cited by 98
Valdés, J. L., McNaughton, B. L., & Fellous, J. (2015) · Journal of Neurophysiology · doi:10.1152/jn.00758.2014 · Cited by 61
Iglói, K., Gaggioni, G., Virginie Sterpenich, A., & Schwartz, S. (2015) · eLife · doi:10.7554/elife.07903 · Cited by 59
Decoding overlapping memories in the medial temporal lobes using high-resolution fMRIPreprint
Chadwick, M. J., Hassabis, D., & Maguire, E. A. (2011) · Learning & Memory · doi:10.1101/lm.023671.111 · Cited by 58
Feld, G. B., Besedovsky, L., Kaida, K., Münte, T. F., & Jan Born, A. (2014) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00629 · Cited by 51
Wolosin, S. M., Zeithamová, D., & Preston, A. R. (2013) · Journal of Experimental Psychology General · doi:10.1037/a0033609 · Cited by 45
Poppenk, J., & Norman, K. A. (2012) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2012.07.010 · Cited by 31
Patterned activation of hippocampal network (∼10 Hz) during in vitro sharp wave-ripples
Papatheodoropoulos, C. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.03.058 · Cited by 22
Flagged first, then by citations
Cited by
Sorted by citations
Locus coeruleus and dopaminergic consolidation of everyday memory
Takeuchi, T., Duszkiewicz, A. J., Sonneborn, A., Spooner, P. A., Yamasaki, M., Watanabe, M., Smith, C. C., Fernández, G., Deisseroth, K., Greene, R. W., et al. (2016) · Nature · doi:10.1038/nature19325 · Cited by 827
A contextual binding theory of episodic memory: systems consolidation reconsidered
Yonelinas, A. P., Ranganath, C., Ekstrom, A. D., & Wiltgen, B. J. (2019) · Nature reviews. Neuroscience · doi:10.1038/s41583-019-0150-4 · Cited by 492
Sleep—A brain-state serving systems memory consolidation
Brodt, S., Inostroza, M., Niethard, N., & Born, J. (2023) · Neuron · doi:10.1016/j.neuron.2023.03.005 · Cited by 343
Schapiro, A. C., McDevitt, E. A., Rogers, T. T., Mednick, S. C., & Norman, K. A. (2018) · Nature Communications · doi:10.1038/s41467-018-06213-1 · Cited by 282
Mechanisms of Memory Disruption in Depression
Dillon, D. G., & Pizzagalli, D. A. (2018) · Trends in Neurosciences · doi:10.1016/j.tins.2017.12.006 · Cited by 292
Metadata
- 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.
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2016-03
- Volume
- 89
- Issue
- 5
- Pages
- 1110-1120
- ISSN
- 0896-6273 (ISSN-L)
- 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
- 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
