Cited by 1,983Memory and Neural MechanismsNeurotransmitter Receptor Influence on BehaviorNeuroscience and Neuropharmacology Research

The DOI matches its Crossref record; 106 of the 107 references it cites were found in a registry or an index.

The Hippocampal-VTA Loop: Controlling the Entry of Information into Long-Term Memory

Open access

Lisman, John E., Grace, Anthony A.·2005·Neuron

DOI 10.1016/j.neuron.2005.05.002

Open this paper in CoChat — free account Open PDF

Abstract

In this article we develop the concept that the hippocampus and the midbrain dopaminergic neurons of the ventral tegmental area (VTA) form a functional loop. Activation of the loop begins when the hippocampus detects newly arrived information that is not already stored in its long-term memory. The resulting novelty signal is conveyed through the subiculum, accumbens, and ventral pallidum to the VTA where it contributes (along with salience and goal information) to the novelty-dependent firing of these cells. In the upward arm of the loop, dopamine (DA) is released within the hippocampus; this produces an enhancement of LTP and learning. These findings support a model whereby the hippocampal-VTA loop regulates the entry of information into long-term memory.

Integrity signals

Registry

Crossref · 10.1016/j.neuron.2005.05.002

Cites

106 of 106 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?

Advances in Neural Information Processing Systems 14
(2002) · The MIT Press eBooks · doi:10.7551/mitpress/1120.001.0001 · Cited by 9,187
The medial temporal lobe
Squire, L. R., Stark, C. E. L., & Clark, R. E. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144130 · Cited by 2,680
The molecular basis of CaMKII function in synaptic and behavioural memory
Lisman, J., Schulman, H., & Cline, H. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn753 · Cited by 1,860
Self-citation
Recognition memory: What are the roles of the perirhinal cortex and hippocampus?
Brown, M. W., & Aggleton, J. P. (2001) · Nature reviews. Neuroscience · doi:10.1038/35049064 · Cited by 1,624
Neuronal Coding of Prediction Errors
Schultz, W., & Dickinson, A. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.473 · Cited by 1,427
Multiple reward signals in the brain
Schultz, W. (2000) · Nature Reviews Neuroscience · doi:10.1038/35044563 · Cited by 1,303
Melanized dopaminergic neurons are differentially susceptible to degeneration in Parkinson's disease
Hirsch, E., Graybiel, A. M., & Agid, Y. A. (1988) · Nature · doi:10.1038/334345a0 · Cited by 1,301 · cited 1×
“However, there is c much less degeneration of the VTA, at least until late r stages of the disease (Hirsch et al., 1988), which may i account for why memory-related problems are not a s major factor in the early stages of the disease.”
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
Afferent modulation of dopamine neuron firing differentially regulates tonic and phasic dopamine transmission
Floresco, S. B., West, A. R., Ash, B., Moore, H., & Grace, A. A. (2003) · Nature Neuroscience · doi:10.1038/nn1103 · Cited by 1,106
Self-citation
Responses of monkey dopamine neurons during learning of behavioral reactions
Ljungberg, T., Apicella, P., & Schultz, W. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.67.1.145 · Cited by 987
Catechol- O -methyltransferase-deficient mice exhibit sexually dimorphic changes in catecholamine levels and behavior
Gogos, J. A., Morgan, M., Luine, V., Santha, M., Ogawa, S., Pfaff, D., & Karayiorgou, M. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.17.9991 · Cited by 864
Contribution of human hippocampal region to novelty detection
Knight, R. T. (1996) · Nature · doi:10.1038/383256a0 · Cited by 848
Synaptic interactions among excitatory afferents to nucleus accumbens neurons: hippocampal gating of prefrontal cortical input
O’Donnell, P., & Grace, A. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-05-03622.1995 · Cited by 760
Self-citation
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
Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex
Petersen, C. C. H., Hahn, T. T. G., Mehta, M. R., Grinvald, A., & Sakmann, B. J. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2235811100 · Cited by 679
Relating Hippocampal Circuitry to Function
Lisman, J. E. (1999) · Neuron · doi:10.1016/s0896-6273(00)81085-5 · Cited by 607
Self-citation
Expression of constitutively active CREB protein facilitates the late phase of long-term potentiation by enhancing synaptic capture.
Barco, A., Alarcon, J. M., & Kandel, E. (2002) · Cell · doi:10.1016/s0092-8674(02)00657-8 · Cited by 595
Age-related defects in spatial memory are correlated with defects in the late phase of hippocampal long-term potentiation in vitro and are attenuated by drugs that enhance the cAMP signaling pathway
Bach, M. E., Barad, M., Son, H., Zhuo, M., Lü, Y.-F., Shih, R., Mansuy, I. M., Hawkins, R. D., & Kandel, E. R. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.9.5280 · Cited by 571
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
Novelty and Familiarity Activations in PET Studies of Memory Encoding and Retrieval
Tulving, E., Markowitsch, H. J., Craik, F. I. M., Habib, R., & Houle, S. (1996) · Cerebral Cortex · doi:10.1093/cercor/6.1.71 · Cited by 564
Neuromodulation and cortical function: modeling the physiological basis of behavior
Hasselmo, M. E. (1995) · Behavioural Brain Research · doi:10.1016/0166-4328(94)00113-t · Cited by 557
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
Self-citation
Hippocampus as comparator: Role of the two input and two output systems of the hippocampus in selection and registration of information
Vinogradova, O. S. (2001) · Hippocampus · doi:10.1002/hipo.1073 · Cited by 550
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
Afferent connections of the laterodorsal and the pedunculopontine tegmental nuclei in the rat: A retro‐ and antero‐grade transport and immunohistochemical study
Semba, K., & Fibiger, H. C. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903230307 · Cited by 544
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
Elements of a neurobiological theory of the hippocampus: the role of activity-dependent synaptic plasticity in memory
Morris, R., Moser, E. I., Riedel, G., Martin, S. J., Sandin, J., Day, M., & O’Carroll, C. (2003) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2002.1264 · Cited by 493
Reversible Inhibition of CREB/ATF Transcription Factors in Region CA1 of the Dorsal Hippocampus Disrupts Hippocampus-Dependent Spatial Memory
Pittenger, C., Huang, Y. Y., Paletzki, R. F., Bourtchouladze, R., Scanlin, H., Vronskaya, S., & Kandel, E. R. (2002) · Neuron · doi:10.1016/s0896-6273(02)00684-0 · Cited by 464
Gating of CaMKII by cAMP-Regulated Protein Phosphatase Activity During LTP
Blitzer, R. D., Connor, J. H., Brown, G. P., Wong, T., Shenolikar, S., Iyengar, R., & Landau, E. M. (1998) · Science · doi:10.1126/science.280.5371.1940 · Cited by 445
Noradrenergic innervation of the adult rat hippocampal formation
Loy, R., Koziell, D. A., Lindsey, J. D., & Moore, R. Y. (1980) · Journal of Comparative Neurology · doi:10.1002/cne.901890406 · Cited by 443
Converging Evidence of NMDA Receptor Hypofunction in the Pathophysiology of Schizophrenia
Coyle, J. T., Tsai, G. E., & GOFF, D. C. (2003) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1300.020 · Cited by 443
A Distinct Role for Norepinephrine in Memory Retrieval
Murchison, C., Zhang, X., Zhang, W., Ouyang, M., Lee, A., & THOMAS, S. A. (2004) · Cell · doi:10.1016/s0092-8674(04)00259-4 · Cited by 421
Dissociation of hippocampus and caudate nucleus memory systems by posttraining intracerebral injection of dopamine agonists.
Packard, M. G., & White, N. M. (1991) · Behavioral Neuroscience · doi:10.1037//0735-7044.105.2.295 · Cited by 416
Storage, recall, and novelty detection of sequences by the hippocampus: Elaborating on the SOCRATIC model to account for normal and aberrant effects of dopamine
Lisman, J. E., & Otmakhova, N. A. (2001) · Hippocampus · doi:10.1002/hipo.1071 · Cited by 414
Self-citation
Hippocampal CA3 region predicts memory sequences: accounting for the phase precession of place cells.Preprint
Jensen, O. B., & Lisman, J. E. (1996) · Learning & Memory · doi:10.1101/lm.3.2-3.279 · Cited by 392
Self-citation
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
Self-citation
Catechol O-methyltransferase mRNA expression in human and rat brain: evidence for a role in cortical neuronal function
Matsumoto, M., Weickert, C. S., Akil, M., Lipska, B. K., Hyde, T. M., Herman, M. M., Kleinman, J. E., & Weinberger, D. R. (2003) · Neuroscience · doi:10.1016/s0306-4522(02)00556-0 · Cited by 365
Late-associativity, synaptic tagging, and the role of dopamine during LTP and LTD
Sajikumar, S. (2004) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2004.03.003 · Cited by 345
Free recall and recognition in a network model of the hippocampus: simulating effects of scopolamine on human memory function
Hasselmo, M. E., & Wyble, B. (1997) · Behavioural Brain Research · doi:10.1016/s0166-4328(97)00048-x · Cited by 338
Functional Organization of the Limbic System in the Process of Registration of Information: Facts and Hypotheses
Vinogradova, O. S. (1975) · Springer eBooks · doi:10.1007/978-1-4684-2979-4_1 · Cited by 335
Dopaminergic antagonists prevent long-term maintenance of posttetanic LTP in the CA1 region of rat hippocampal slices
Frey, U., Schroeder, H., & Matthies, H. (1990) · Brain Research · doi:10.1016/0006-8993(90)91578-5 · Cited by 333
Origin of dopaminergic innervation of the rat hippocampal formation
Scatton, B., Simon, H., Le Moal, M., & Bischoff, S. (1980) · Neuroscience Letters · doi:10.1016/0304-3940(80)90314-6 · Cited by 323
The effect of dopaminergic D1 receptor blockade during tetanization on the expression of long-term potentiation in the rat CA1 region in vitro
Frey, U., Matthies, H., Reymann, K. G., & Matthies, H. (1991) · Neuroscience Letters · doi:10.1016/0304-3940(91)90732-9 · Cited by 314
Novel dopamine receptors half a decade later
Sokoloff, P., & Schwartz, J.-C. (1995) · Trends in Pharmacological Sciences · doi:10.1016/s0165-6147(00)89044-6 · Cited by 295
The dopaminergic mesencephalic projections to the hippocampal formation in the rat
Gasbarri, A., Sulli, A., & Packard, M. G. (1997) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/s0278-5846(96)00157-1 · Cited by 285
Dopamine-cell depolarization block as a model for the therapeutic actions of antipsychotic drugs
Grace, A. A., Bunney, B. S., Moore, H. M., & Todd, C. L. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)10064-3 · Cited by 284
Self-citation
Burst activity of ventral tegmental dopamine neurons is elicited by sensory stimuli in the awake cat
Horvitz, J. C., Stewart, T., & Jacobs, B. L. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00265-5 · Cited by 283
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
Self-citation
Anterograde and retrograde tracing of projections from the ventral tegmental area to the hippocampal formation in the rat
Gasbarri, A., Packard, M. G., Campana, E., & Pacitti, C. (1994) · Brain Research Bulletin · doi:10.1016/0361-9230(94)90288-7 · Cited by 272
The role of hippocampal subregions in detecting spatial novelty
Lee, I., Hunsaker, M. R., & Kesner, R. P. (2005) · Behavioral Neuroscience · doi:10.1037/0735-7044.119.1.145 · Cited by 270
Opposite Influences of Endogenous Dopamine D1and D2Receptor Activation on Activity States and Electrophysiological Properties of Striatal Neurons: Studies CombiningIn VivoIntracellular Recordings and Reverse Microdialysis
West, A. R., & Grace, A. A. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-01-00294.2002 · Cited by 252
Self-citation
Dopaminergic stimulation of local protein synthesis enhances surface expression of GluR1 and synaptic transmission in hippocampal neurons
Smith, W. B., Starck, S. R., Roberts, R. W., & Schuman, E. M. (2005) · Neuron · doi:10.1016/j.neuron.2005.01.015 · Cited by 252
Levodopa: Faster and better word learning in normal humans
Knecht, S., Breitenstein, C., Bushuven, S., Wailke, S., Kamping, S., Flöel, A., Zwitserlood, P., & Ringelstein, E. B. (2004) · Annals of Neurology · doi:10.1002/ana.20125 · Cited by 252
Rap1 Couples cAMP Signaling to a Distinct Pool of p42/44MAPK Regulating Excitability, Synaptic Plasticity, Learning, and Memory
Morozov, A., Muzzio, I. A., Bourtchouladze, R., Van-Strien, N., Lapidus, K. A. B., Yin, D., Winder, D. G., Adams, J. P., Sweatt, J. D., & Kandel, E. R. (2003) · Neuron · doi:10.1016/s0896-6273(03)00404-5 · Cited by 236
Stimulation of the Ventral Subiculum of the Hippocampus Evokes Glutamate Receptor‐mediated Changes in Dopamine Efflux in the Rat Nucleus Accumbens
Blaha, C. D., Yang, C. R., Floresco, S., Barr, A. M., & Phillips, A. G. (1997) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1997.tb01441.x · Cited by 207
Rapid Prefrontal-Hippocampal Habituation to Novel Events
Yamaguchi, S. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.4587-03.2004 · Cited by 205
Hippocampal and prefrontal cortical inputs monosynaptically converge with individual projection neurons of the nucleus accumbens
French, S. J., & Totterdell, S. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10191 · Cited by 202
Chemical Stimulation of the Ventral Hippocampus Elevates Nucleus Accumbens Dopamine by Activating Dopaminergic Neurons of the Ventral Tegmental Area
Legault, M., Rompré, P.-P., & Wise, R. A. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-04-01635.2000 · Cited by 200
Hippocampal Neurons Responding to First-Time Dislocation of a Target Object
Fyhn, M., Molden, S., Hollup, S., Moser, M., & Moser, E. I. (2002) · Neuron · doi:10.1016/s0896-6273(02)00784-5 · Cited by 199
Integrating Schizophrenia
Gray, J. A. (1998) · Schizophrenia Bulletin · doi:10.1093/oxfordjournals.schbul.a033324 · Cited by 196
Novelty‐evoked elevations of nucleus accumbens dopamine: dependence on impulse flow from the ventral subiculum and glutamatergic neurotransmission in the ventral tegmental area
Legault, M., & Wise, R. A. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2000.01448.x · Cited by 191
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
Dopamine Selectively Inhibits the Direct Cortical Pathway to the CA1 Hippocampal Region
Otmakhova, N. A., & Lisman, J. E. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-04-01437.1999 · Cited by 186
Self-citation
Individual nucleus accumbens-projection neurons receive both basolateral amygdala and ventral subicular afferents in rats
French, S. J., & Totterdell, S. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00150-7 · Cited by 180
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
Distribution of D5 dopamine receptor mRNA in rat brain
Meador‐Woodruff, J. H., Mansour, A., Grandy, D. K., Damask, S. P., Civelli, O., & Watson, S. J. (1992) · Neuroscience Letters · doi:10.1016/0304-3940(92)90024-2 · Cited by 177
D1/D5 Dopamine Receptors Inhibit Depotentiation at CA1 Synapses via cAMP-Dependent Mechanism
Otmakhova, N. A., & Lisman, J. E. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-04-01270.1998 · Cited by 176
Self-citation
A double dissociation within the hippocampus of dopamine D1/D5 receptor and β-adrenergic receptor contributions to the persistence of long-term potentiation
Swanson-Park, J. L., Coussens, C. M., Mason-Parker, S. E., Raymond, C. R., Hargreaves, E. L., Dragunow, M., Cohen, A. S., & Abraham, W. C. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00010-x · Cited by 175
Post-pubertal Emergence of Prefrontal Cortical Up States Induced by D1-NMDA Co-activation
Tseng, K. Y. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhh107 · Cited by 169
Hippocampal signal transmission to the pedunculopontine nucleus and its regulation by dopamine D2 receptors in the nucleus accumbens: An electrophysiological and behavioural study
Yang, C., & Mogenson, G. J. (1987) · Neuroscience · doi:10.1016/0306-4522(87)90179-5 · Cited by 168
Verbal novelty detection within the human hippocampus proper
Grünwald, T., Lehnertz, K., Heinze, H. J., Helmstaedter, C., & Elger, C. E. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.6.3193 · Cited by 160
Requirement of β‐adrenergic receptor activation and protein synthesis for LTP‐reinforcement by novelty in rat dentate gyrus
Straube, T., Korz, V., Balschun, D., & Frey, J. U. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.049452 · Cited by 157
Comparison of dopamine and noradrenaline release in mouse prefrontal cortex, striatum and hippocampus using microdialysis
Ihalainen, J. A., Riekkinen Jr, P., & Feenstra, M. G. P. (1999) · Neuroscience Letters · doi:10.1016/s0304-3940(99)00840-x · Cited by 148
Novelty‐elicited, Noradrenaline‐dependent Enhancement of Excitability in the Dentate Gyrus
Kitchigina, V. F., Vankov, A., Harley, C. W., & Sara, S. J. (1997) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1997.tb01351.x · Cited by 145
COMT Gene Polymorphism Is Associated with Declarative Memory in Adulthood and Old Age
de Frias, C. M., Annerbrink, K., Westberg, L., Eriksson, E., Adolfsson, R., & Nilsson, L.-G. (2004) · Behavior Genetics · doi:10.1023/b:bege.0000038491.06972.8c · Cited by 145
A Review of EEG and Blood Flow Data
Knight, R. T., & Nakada, T. (1998) · Reviews in the Neurosciences · doi:10.1515/revneuro.1998.9.1.57 · Cited by 129
Novel spatial arrangements of familiar visual stimuli promote activity in the rat hippocampal formation but not the parahippocampal cortices: a c-fos expression study
Jenkins, T. A., Amin, E., Pearce, J. M. S., Brown, M. W., & Aggleton, J. P. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2003.11.024 · Cited by 128
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
Hippocampal Lesions Disrupt an Associative Mismatch Process
Honey, R. C., Watt, A., & Good, M. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-06-02226.1998 · Cited by 124
Hyperlocomotion and increased dopamine efflux in the rat nucleus accumbens evoked by electrical stimulation of the ventral subiculum: role of ionotropic glutamate and dopamine D 1 receptors
Taepavarapruk, P., Floresco, S., & Phillips, A. G. (2000) · Psychopharmacology · doi:10.1007/s002130000376 · Cited by 121
Autoradiographic distribution of [3H]YM‐09151‐2, a high‐affinity and selective antagonist ligand for the dopamine D2 receptor group, in the rat brain and spinal cord
Yokoyama, C., Okamura, H., Nakajima, T., Taguchi, J., & Ibata, Y. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903440109 · Cited by 119
Reversible inhibition of
Velumian, A. A., Zhang, L., Pennefather, P., & Carlen, P. L. (1996) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s004240050286 · Cited by 118
Visualization of dopamine D1, D2 and D3 receptor mRNA's in human and rat brain
Mengod, G., Villaró, M. T., Landwehrmeyer, G. B., Martinez-Mir, M. I., Niznik, H. B., Sunahara, R. K., Seeman, P. M., O’Dowd, B. F., Probst, A., & Palacios, J. M. (1992) · Neurochemistry International · doi:10.1016/0197-0186(92)90208-9 · Cited by 117
Adaptive anterior hippocampal responses to oddball stimuli
Strange, B. A., & Dolan, R. J. (2001) · Hippocampus · doi:10.1002/hipo.1084 · Cited by 117
Contribution of Pedunculopontine Tegmental Nucleus Neurons to Performance of Visually Guided Saccade Tasks in Monkeys
Kobayashi, Y., Inoue, Y., Yamamoto, M., Isa, T., & Aizawa, H. (2002) · Journal of Neurophysiology · doi:10.1152/jn.2002.88.2.715 · Cited by 104
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
Integrated systems of the CNS
Björklund, A., Hökfelt, T. G. M., & Swanson, L. W. (1987) · Cited by 94
Autoradiographic localization of dopamine uptake sites in the rat brain with3H-GBR 12935
Mennicken, F., Savasta, M., Peretti‐Renucci, R., & Feuerstein, C. (1992) · Journal of Neural Transmission · doi:10.1007/bf01253106 · Cited by 91
Hippocampal place fields: Relationship between degree of field overlap and cross-correlations within ensembles of hippocampal neurons
Hampson, R. E., Byrd, D. R., Konstantopoulos, J. K., Bunn, T., & Deadwyler, S. A. (1996) · Hippocampus · doi:10.1002/(sici)1098-1063(1996)6:3 · Cited by 82
Sensory responsiveness of “Broad-spike” neurons in the laterodorsal tegmental nucleus, locus coeruleus and dorsal raphe of awake rats: Implications for cholinergic and monoaminergic neuron-specific responses
Koyama, Y., Jodo, E., & Kayama, Y. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90569-x · Cited by 81
Extracellular dopamine dynamics in rat caudate–putamen during experimenter-delivered and intracranial self-stimulation
Kilpatrick, M., Rooney, M. B., MICHAEL, D., & Wightman, R. M. (2000) · Neuroscience · doi:10.1016/s0306-4522(99)00578-3 · Cited by 80
Opioid and GABA modulation of accumbens-evoked ventral pallidal activity
Chrobak, J. J., & Napier, T. C. (1993) · Journal of Neural Transmission · doi:10.1007/bf01245342 · Cited by 78
Response of dopaminergic neurons in cat to auditory stimuli presented across the sleep-waking cycle
Steinfels, G. F., Heym, J. H., Strecker, R. E., & Jacobs, B. L. (1983) · Brain Research · doi:10.1016/0006-8993(83)90917-4 · Cited by 60
Phencyclidine interferes with the hippocampal gating of nucleus accumbens neuronal activity in vivo
O’Donnell, P., & Grace, A. A. (1998) · Neuroscience · doi:10.1016/s0306-4522(98)00190-0 · Cited by 59
Self-citation
Behavior during hippocampal microinfusions. II. Muscarinic locomotor activation
Flicker, C., & Geyer, M. A. (1982) · Brain Research Reviews · doi:10.1016/0165-0173(82)90007-8 · Cited by 48
Heterogeneous tissue-specific transcription of dopamine receptor subtype messenger RNA in rat brain
Laurier, L. G., O’Dowd, B. F., & George, S. R. (1994) · Molecular Brain Research · doi:10.1016/0169-328x(94)90170-8 · Cited by 44
Activation of the retrohippocampal region in the rat causes dopamine release in the nucleus accumbens: disruption by fornix section
Mitchell, S. N., Yee, B. K., Feldon, J., Gray, J. A., & Rawlins, J. N. P. (2000) · European Journal of Pharmacology · doi:10.1016/s0014-2999(00)00741-x · Cited by 43
The Hippocampus in Schizophrenia
Heckers, S. (2004) · American Journal of Psychiatry · doi:10.1176/appi.ajp.161.11.2138-a · Cited by 41
Behavior-Dependent States of the Hippocampal Network Affect Functional Clustering of Neurons
Hirase, H., Leinekugel, X., Csicsvari, J. L., Czurkó, A., & Buzsáki, G. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-10-j0003.2001 · Cited by 40
Localization of dopamine D2 receptor mRNA with non-radioactive in situ hybridization histochemistry
Brouwer, N., van Dijken, H., Ruiters, M. H. J., van Willigen, J. D., & Horst, G. J. T. (1992) · Neuroscience Letters · doi:10.1016/0304-3940(92)90378-k · Cited by 28
Dissociation of core and shell single-unit activity in the nucleus accumbens in free-choice novelty
Wood, D. (2003) · Behavioural Brain Research · doi:10.1016/j.bbr.2003.09.038 · Cited by 23
Location and molecular cloning of D1 dopamine receptor
Gingrich, J. A., Dearry, A., Falardeau, P., Bates, M. D., Fremeau, R. T., & Caron, M. G. (1992) · Neurochemistry International · doi:10.1016/0197-0186(92)90204-5 · Cited by 21
Behavioral and hippocampal evoked responses in an auditory oddball situation when an unconditioned stimulus is paired with deviant tones in the cat: Experiment II
Ruusuvirta, T., Korhonen, T., Penttonen, M., Arikoski, J., & Kivirikko, K. (1995) · International Journal of Psychophysiology · doi:10.1016/0167-8760(95)00025-n · Cited by 14
Re-examination of the ontogeny in the gene expression of DARPP-32 in the rat brain
Sakagami, H., Ebina, K., & Kondo, H. (1994) · Molecular Brain Research · doi:10.1016/0169-328x(94)90279-8 · Cited by 6
3 State Neurons for Contextual Processing
Kepecs, Á., & Raghavachari, S. (2002) · The MIT Press eBooks · doi:10.7551/mitpress/1120.003.0034 · Cited by 4
Untitled work
Finch (1996) · doi:10.1002/(sici)1098-1063(1996)6:5

Flagged first, then by citations

1 of the 107 references couldn’t be matched to a known paper.

Research works printed but not linked: 1

Mogenson, 1993, From motivation to action: A review of dopaminergic regulation of limbic to nucleus accumbens to ventral pallidum to pedunculopontine nucleus circuitries involved in limbic-motor integration, 193

Sorted by citations

Dopamine in motivational control: rewarding, aversive, and alerting
Bromberg-Martin, E. S., Matsumoto, M., & Hikosaka, O. (2010) · Neuron · doi:10.1016/j.neuron.2010.11.022 · Cited by 2,396
The critical role of retrieval practice in long-term retention
Roediger, H. L., & Butler, A. C. (2011) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2010.09.003 · Cited by 1,796
Stress, Depression, and Neuroplasticity: A Convergence of Mechanisms
Pittenger, C., & Duman, R. S. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301574 · Cited by 1,795
The role of phase synchronization in memory processes
Fell, J., & Axmacher, N. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn2979 · Cited by 1,620
Reconsidering anhedonia in depression: Lessons from translational neuroscience
Treadway, M. T., & Zald, D. H. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.06.006 · Cited by 1,579

See all 1,983

Authors: Lisman, J. E., & Grace, A. A.
Affiliations: Brandeis University (US)
University of Pittsburgh (US)
Corresponding author: Lisman, John E.
ORCID: Lisman, John E.
Grace, Anthony A.
Venue: Neuron
Publisher: Elsevier BV
Published: 2005-06
Volume: 46
Issue: 5
Pages: 703-713
ISSN: 0896-6273 (ISSN-L)
DOI: 10.1016/j.neuron.2005.05.002
OpenAlex: W2121007598
Cited by: 1,983
References: 107
Citations by year: 2026: 105 · 2025: 97 · 2024: 139 · 2023: 97 · 2022: 99 · 2021: 115 · 2020: 122 · 2019: 92 · 2018: 97 · 2017: 93 · 2016: 97 · 2015: 120 · 2014: 103 · 2013: 103 · 2012: 96
FWCI: 5.53
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 2968 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)
Funders: National Alliance for Research on Schizophrenia and Depression
National Institutes of Health
W. M. Keck Foundation
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: hippocampus, ventral tegmental area, dopamine, long-term memory consolidation, novelty detection, subiculum, ventral pallidum, accumbens, long-term potentiation, learning, salience, dopaminergic neurons
MeSH terms: Animals, Hippocampus, Humans, Memory, Nerve Net, Time Factors, 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

The Hippocampal-VTA Loop: Controlling the Entry of Information into Long-Term Memory

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