Cited by 977Memory and Neural MechanismsMemory Processes and InfluencesNeurotransmitter Receptor Influence on Behavior

The DOI matches its Crossref record; 50 of the 50 references it cites were found in a registry or an index.

Reward-Motivated Learning: Mesolimbic Activation Precedes Memory Formation

Open access

Adcock, R. Alison, Thangavel, Arul, Whitfield-Gabrieli, Susan, Knutson, Brian, Gabrieli, John D.E.·2006·Neuron

DOI 10.1016/j.neuron.2006.03.036

Open this paper in CoChat — free account Open PDF

Abstract

We examined anticipatory mechanisms of reward-motivated memory formation using event-related FMRI. In a monetary incentive encoding task, cues signaled high- or low-value reward for memorizing an upcoming scene. When tested 24 hr postscan, subjects were significantly more likely to remember scenes that followed cues for high-value rather than low-value reward. A monetary incentive delay task independently localized regions responsive to reward anticipation. In the encoding task, high-reward cues preceding remembered but not forgotten scenes activated the ventral tegmental area, nucleus accumbens, and hippocampus. Across subjects, greater activation in these regions predicted superior memory performance. Within subject, increased correlation between the hippocampus and ventral tegmental area was associated with enhanced long-term memory for the subsequent scene. These findings demonstrate that brain activation preceding stimulus encoding can predict declarative memory formation. The findings are consistent with the hypothesis that reward motivation promotes memory formation via dopamine release in the hippocampus prior to learning.

Integrity signals

Registry

Crossref · 10.1016/j.neuron.2006.03.036

Cites

50 of 50 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

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
A neural substrate of prediction and reward
Schultz, W., Dayan, P., & Montague, P. R. (1997) · Science · doi:10.1126/science.275.5306.1593 · Cited by 9,388
LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS
Scoville, W. B., & Milner, B. (1957) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp.20.1.11 · Cited by 7,322
Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans.
Squire, L. R. (1992) · Psychological Review · doi:10.1037/0033-295x.99.2.195 · Cited by 5,376
Predictive reward signal of dopamine neurons
Schultz, W. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.80.1.1 · Cited by 4,564
Anticipation 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
Self-citation
Discrete coding of reward probability and uncertainty by dopamine neurons
Fiorillo, C. D., Tobler, P. N., & Schultz, W. (2003) · Science · doi:10.1126/science.1077349 · Cited by 2,085
Building Memories: Remembering and Forgetting of Verbal Experiences as Predicted by Brain Activity
Wagner, A. D., Schacter, D. L., Rotte, M., Koutstaal, W., Maril, A., Dale, A. M., Rosen, B. R., & Buckner, R. L. (1998) · Science · doi:10.1126/science.281.5380.1188 · Cited by 1,644
The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking
Ikemoto, S., & Panksepp, J. (1999) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00023-5 · Cited by 1,450
Dissociation of reward anticipation and outcome with event-related fMRI
Knutson, B., Fong, G. W., Adams, C. M., Varner, J. L., & Hommer, D. (2001) · Neuroreport · doi:10.1097/00001756-200112040-00016 · Cited by 1,300
Self-citation
Responses of monkey dopamine neurons to reward and conditioned stimuli during successive steps of learning a delayed response task
Schultz, W., Apicella, P., & Ljungberg, T. (1993) · The Journal of Neuroscience · doi:10.1523/jneurosci.13-03-00900.1993 · Cited by 1,291
Acute effects of cocaine on human brain activity and emotion
Breiter, H. C., Gollub, R. L., Weisskoff, R. M., Kennedy, D. N., Makris, N., Berke, J. D., Goodman, J. M., Kantor, H. L., Gastfriend, D. R., Riorden, J. P., et al. (1997) · Neuron · doi:10.1016/s0896-6273(00)80374-8 · Cited by 1,270
Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons
Frey, U., Huang, Y.-Y., & Kandel, E. R. (1993) · Science · doi:10.1126/science.8389057 · Cited by 1,218
Making Memories: Brain Activity that Predicts How Well Visual Experience Will Be Remembered
Brewer, J. B., Zhao, Z., Desmond, J. E., Glover, G. H., & Gabrieli, J. D. E. (1998) · Science · doi:10.1126/science.281.5380.1185 · Cited by 1,108
Self-citation
Coupling Between Neuronal Firing, Field Potentials, and fMRI in Human Auditory Cortex
Mukamel, R., Gelbard, H., Arieli, A., Hasson, U., Fried, I., & Malach, R. (2005) · Science · doi:10.1126/science.1110913 · Cited by 1,023
Distributed Neural Representation of Expected Value
Knutson, B., Taylor, J., Kaufman, M., Peterson, R., & Glover, G. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.0642-05.2005 · Cited by 955
Self-citation
A region of mesial prefrontal cortex tracks monetarily rewarding outcomes: characterization with rapid event-related fMRI
Knutson, B. D., Fong, G., Bennett, S. M., Adams, C. M., & Hommer, D. W. (2003) · NeuroImage · doi:10.1016/s1053-8119(02)00057-5 · Cited by 868
Self-citation
Parametric Analysis of fMRI Data Using Linear Systems Methods
Cohen, M. S. (1997) · NeuroImage · doi:10.1006/nimg.1997.0278 · Cited by 723
Interaction between the Amygdala and the Medial Temporal Lobe Memory System Predicts Better Memory for Emotional Events
Dolcos, F., LaBar, K. S., & Cabeza, R. (2004) · Neuron · doi:10.1016/s0896-6273(04)00289-2 · Cited by 714 · cited 1×
“We subtracted the intensity-normalized signal 1 s and 2 s prior to cue onset from the signal 5 s and 6 s after cue onset to estimate the percent signal change on each trial (for a similar approach, see Dolcos et al., 2004).”
Method
Reward-related FMRI activation of dopaminergic midbrain is associated with enhanced hippocampus-dependent long-term memory formation
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
Spiral‐in/out BOLD fMRI for increased SNR and reduced susceptibility artifacts
Glover, G. H., & Law, C. S. W. (2001) · Magnetic Resonance in Medicine · doi:10.1002/mrm.1222 · Cited by 600
Dopamine-dependent facilitation of LTP induction in hippocampal CA1 by exposure to spatial novelty
Li, S., Cullen, W. K., Anwyl, R., & Rowan, M. J. (2003) · Nature Neuroscience · doi:10.1038/nn1049 · Cited by 568
Glutamatergic Afferents from the Hippocampus to the Nucleus Accumbens Regulate Activity of Ventral Tegmental Area Dopamine Neurons
Floresco, S., Todd, C. L., & Grace, A. A. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-13-04915.2001 · Cited by 556
D1/D5 receptor agonists induce a protein synthesis-dependent late potentiation in the CA1 region of the hippocampus.
Huang, Y.-Y., & Kandel, E. R. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.7.2446 · Cited by 544
Prefrontal–Temporal Circuitry for Episodic Encoding and Subsequent Memory
Kirchhoff, B. A., Wagner, A. D., Maril, A., & Stern, C. E. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-16-06173.2000 · Cited by 536
Involvement of hippocampal cAMP/cAMP-dependent protein kinase signaling pathways in a late memory consolidation phase of aversively motivated learning in rats
Bernabeu, R., Bevilaqua, L. R., Ardenghi, P. G., Bromberg, E., Schmitz, P. K., Bianchin, M. M., Izquierdo, I., & Medina, J. H. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.13.7041 · Cited by 513
How emotion enhances the feeling of remembering
Sharot, T., Delgado, M., & Phelps, E. (2004) · Nature Neuroscience · doi:10.1038/nn1353 · Cited by 470
Different kinetics govern dopaminergic transmission in the amygdala, prefrontal cortex, and striatum: an in vivo voltammetric study
Garris, P. A., & Wightman, R. M. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-01-00442.1994 · Cited by 419
Subcortical afferents to the hippocampal formation in the monkey
Amaral, D. G., & Cowan, W. M. (1980) · Journal of Comparative Neurology · doi:10.1002/cne.901890402 · Cited by 390
D1/D5 dopamine receptor activation increases the magnitude of early long-term potentiation at CA1 hippocampal synapses
Otmakhova, N. A., & Lisman, J. E. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-23-07478.1996 · Cited by 377
Dopamine transporter immunoreactivity in monkey cerebral cortex: regional, laminar, and ultrastructural localization
Lewis, D. A., Melchitzky, D. S., Sesack, S. R., Whitehead, R. E., Auh, S., & Sampson, A. (2001) · Journal of Comparative Neurology · doi:10.1002/cne.1092 · Cited by 352
Volumetry of temporopolar, perirhinal, entorhinal and parahippocampal cortex from high-resolution MR images: considering the variability of the collateral sulcus
Pruessner, J. C. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.12.1342 · Cited by 297
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, C. A., & McNaughton, B. L. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.0575-04.2004 · Cited by 282
The Hippocampus Modulates Dopamine Neuron Responsivity by Regulating the Intensity of Phasic Neuron Activation
Lodge, D. J., & Grace, A. A. (2006) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300963 · Cited by 280
The Primate Substantia Nigra and VTA: Integrative Circuitry and Function
Haber, S. N., & Fudge, J. L. (1997) · Critical Reviews in Neurobiology · doi:10.1615/critrevneurobiol.v11.i4.40 · Cited by 228
State-related and item-related neural correlates of successful memory encoding
Otten, L. J., Henson, R. N., & Rugg, M. D. (2002) · Nature Neuroscience · doi:10.1038/nn967 · Cited by 196
Involvement of hippocampal D1/D5 receptor-cAMP signaling pathways in a late memory consolidation phase of an aversively-motivated task in rats
Bernabeu, R. (1997) · Medical Entomology and Zoology · Cited by 188
Spatial memory impairment induced by lesion of the mesohippocampal dopaminergic system in the rat
Gasbarri, A., Sulli, A., Innocenzi, R., Pacitti, C., & Brioni, J. D. (1996) · Neuroscience · doi:10.1016/0306-4522(96)00202-3 · Cited by 178
Hippocampal inputs to identified neurons in an in vitro slice preparation of the rat nucleus accumbens: evidence for feed-forward inhibition
Pennartz, C. M. A., & Kitai, S. (1991) · Journal of Neuroscience · doi:10.1523/jneurosci.11-09-02838.1991 · Cited by 137
Activation of Midbrain Structures by Associative Novelty and the Formation of Explicit Memory in HumansPreprint
Schott, B. H., Sellner, D., Lauer, C., Habib, R., Frey, J. U., Guderian, S., Heinze, H., & Düzel, E. (2004) · Learning & Memory · doi:10.1101/lm.75004 · Cited by 126
Dopamine D2 receptor expression in hippocampus and parahippocampal cortex of rat, cat, and human in relation to tyrosine hydroxylase‐immunoreactive fibers
Goldsmith, S. K., & Joyce, J. N. (1994) · Hippocampus · doi:10.1002/hipo.450040318 · Cited by 96
Encoding and retrieval in human medial temporal lobes: An empirical investigation using functional magnetic resonance imaging (fMRI)
Dolan, R. J., & Fletcher, P. C. (1999) · Hippocampus · doi:10.1002/(sici)1098-1063(1999)9:1 · Cited by 87
Self-citation
DNA targeting of rhinal cortex D2 receptor protein reversibly blocks learning of cues that predict reward
Liu, Z., Richmond, B. J., Murray, E. A., Saunders, R. C., Steenrod, S. C., Stubblefield, B. K., Montague, D. M., & Ginns, E. I. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0403639101 · Cited by 77
The Dopaminergic Innervation of Monkey Entorhinal Cortex
Akil, M., & Lewis, D. A. (1993) · Cerebral Cortex · doi:10.1093/cercor/3.6.533 · Cited by 76
Catecholaminergic innervation of the hippocampus in the cynomolgus monkey
Samson, Y., Wu, J. J., Friedman, A. H., & Davis, J. N. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902980209 · Cited by 64
Amygdalar Recruitment during Anticipation of Monetary Rewards
Hommer, D. W., Knutson, B. D., Fong, G., Bennett, S. M., ADAMS, C. M., & VARNERA, J. L. (2003) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2003.tb07103.x · Cited by 62
Self-citation
Dopamine depresses cholinergic oscillatory network activity in rat hippocampus
Weiß, T., Veh, R. W., & Heinemann, U. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02970.x · Cited by 52
The distribution of tyrosine hydroxylase-immunoreactive fibers in the human entorhinal cortex
Akil, M., & Lewis, D. A. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90268-2 · Cited by 46
Apomorphine and glycoprotein synthesis during consolidation
Jork, R., Grecksch, G., & Matthies, H. J. G. (1982) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(82)90254-4 · Cited by 11
Untitled work
(2000) · doi:10.1002/1098-1063(2000)10:6

Flagged first, then by citations

Sorted by citations

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
Self-citation
Untitled work
(2009) · Cited by 2,013
Neuroplasticity Subserving Motor Skill Learning
Dayan, E., & Cohen, L. G. (2011) · Neuron · doi:10.1016/j.neuron.2011.10.008 · Cited by 1,408
Item, context and relational episodic encoding in humans
Davachi, L. (2006) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2006.10.012 · Cited by 1,138
Ventral tegmental area: cellular heterogeneity, connectivity and behaviour
Morales, M., & Margolis, E. B. (2017) · Nature reviews. Neuroscience · doi:10.1038/nrn.2016.165 · Cited by 1,108

See all 977

Authors: Adcock, R. A., Thangavel, A., Whitfield-Gabrieli, S., Knutson, B., & Gabrieli, J. D. E.
Affiliations: University of California, San Francisco (US)
Stanford University (US)
Corresponding author: Adcock, R. Alison
ORCID: Adcock, R. Alison
Knutson, Brian
Gabrieli, John D.E.
Venue: Neuron
Publisher: Elsevier BV
Published: 2006-05
Volume: 50
Issue: 3
Pages: 507-517
ISSN: 0896-6273 (ISSN-L)
DOI: 10.1016/j.neuron.2006.03.036
OpenAlex: W2111873046
Cited by: 977
References: 50
Citations by year: 2026: 22 · 2025: 45 · 2024: 55 · 2023: 73 · 2022: 52 · 2021: 55 · 2020: 64 · 2019: 55 · 2018: 56 · 2017: 52 · 2016: 57 · 2015: 61 · 2014: 55 · 2013: 49 · 2012: 44
FWCI: 14.09
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, 2634 d)
Locations: Neuron (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of Mental Health (MH59940, R01MH059940)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords: memory formation, reward anticipation, mesolimbic system, ventral tegmental area, nucleus accumbens, hippocampus, dopamine release, declarative memory, financial incentives
MeSH terms: Adolescent, Adult, Brain Mapping, Cues, Dopamine, Female, Hippocampus, Humans, Learning, Magnetic Resonance Imaging, Male, Memory, Motivation, Neural Pathways, Synaptic Transmission, Neuropsychological Tests, Nucleus Accumbens, Reward, Ventral Tegmental Area

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

Reward-Motivated Learning: Mesolimbic Activation Precedes Memory Formation

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks