Midbrain dopamine neurons bidirectionally regulate CA3-CA1 synaptic drive
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Dopamine (DA) is required for hippocampal-dependent memory and long-term potentiation (LTP) at CA1 Schaffer collateral (SC) synapses. It is therefore surprising that exogenously applied DA has little effect on SC synapses, but suppresses CA1 perforant path (PP) inputs. To examine DA actions under more physiological conditions, we used optogenetics to release DA from ventral tegmental area inputs to hippocampus. Unlike exogenous DA application, optogenetic release of DA caused a bidirectional, activity-dependent modulation of SC synapses, with no effect on PP inputs. Low levels of DA release, simulating tonic DA neuron firing, depressed the SC response through a D4 receptor-dependent enhancement of feedforward inhibition mediated by parvalbumin-expressing interneurons. Higher levels of DA release, simulating phasic firing, increased SC responses through a D1 receptor-dependent enhancement of excitatory transmission. Thus, tonic-phasic transitions in DA neuron firing in response to motivational demands may cause a modulatory switch from inhibition to enhancement of hippocampal information flow.
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Our results confirm recent studies using viral expression of channelrhodopsin in Slc6a3ires-cre/+ mice that labeled relatively sparse dopaminergic axons in the CA1 region.
“Our results also confirm recent studies using viral expression of channelrhodopsin in Slc6a3ires-cre/+ mice that labeled relatively sparse dopaminergic axons in the CA1 region (McNamara et al., 2014; Rosen et al., 2015).”
From Dopamine regulates aversive contextual learning and associated in vivo synaptic plasticity in the Hippocampus (2016) · cites this paper as Rosen et al., 2015
Optogenetic release of dopamine exclusively from the VTA causes a bidirectional, activity-dependent modulation of Schaffer collateral synapses in hippocampal slices.
“In addition, optogenetic release of dopamine exclusively from the VTA was shown to cause a bidirectional, activity-dependent modulation of Schaffer collateral synapses in hippocampal slices (Rosen et al., 2015).”
From Dopamine regulates aversive contextual learning and associated in vivo synaptic plasticity in the Hippocampus (2016) · cites this paper as Rosen et al., 2015
Despite the sparse innervation of the hippocampus by midbrain dopaminergic axons, several lines of evidence indicate a significant functional role for this dopaminergic innervation.
“Despite the sparse innervation of the hippocampus by midbrain dopaminergic axons, several lines of evidence indicate a significant functional role for this dopaminergic innervation.”
From Dopamine regulates aversive contextual learning and associated in vivo synaptic plasticity in the Hippocampus (2016) · cites this paper as Rosen et al., 2015
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Millisecond-timescale, genetically targeted optical control of neural activity
Boyden, E. S., Zhang, F., Bamberg, E., Nagel, G., & Deisseroth, K. A. (2005) · Nature Neuroscience · doi:10.1038/nn1525 · Cited by 4,831 · see citing works
Driving fast-spiking cells induces gamma rhythm and controls sensory responses
Cardin, J. A., Carlén, M., Meletis, K., Knoblich, U., Zhang, F., Deisseroth, K., Tsai, L.-H., & Moore, C. I. (2009) · Nature · doi:10.1038/nature08002 · Cited by 2,603 · see citing works
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 · see citing works
Swanson, L. W. (1982) · Brain Research Bulletin · doi:10.1016/0361-9230(82)90145-9 · Cited by 1,718 · see citing works
Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons
Cobb, S. R., Buhl, E. H., Halasy, K., Paulsen, O., & Somogyi, P. (1995) · Nature · doi:10.1038/378075a0 · Cited by 1,498 · see citing works
Multiple dopamine functions at different time courses
Schultz, W. (2007) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.28.061604.135722 · Cited by 1,415 · see citing works
Hu, H., Gan, J., & Jonas, P. (2014) · Science · doi:10.1126/science.1255263 · Cited by 1,197 · see citing works
Enforcement of Temporal Fidelity in Pyramidal Cells by Somatic Feed-Forward Inhibition
Pouille, F., & Scanziani, M. (2001) · Science · doi:10.1126/science.1060342 · Cited by 1,097 · see citing works
A Developmental Switch in the Response of DRG Neurons to ETS Transcription Factor Signaling
Hippenmeyer, S., Pecho‐Vrieseling, E., Sigrist, M., Portmann, T., Laengle, C., Ladle, D. R., & Arber, S. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0030159 · Cited by 1,059 · see citing works
Regulation of firing of dopaminergic neurons and control of goal-directed behaviors
Grace, A. A., Floresco, S. B., Goto, Y., & Lodge, D. J. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.03.003 · Cited by 1,034 · see citing works
DESENSITIZATION OF G PROTEIN–COUPLED RECEPTORS AND NEURONAL FUNCTIONS
Gainetdinov, R. R., Premont, R. T., Bohn, L., Lefkowitz, R. J., & Caron, M. G. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144206 · Cited by 864 · see citing works
Dopaminergic modulation of synaptic transmission in cortex and striatum
Tritsch, N. X., & Sabatini, B. L. (2012) · Neuron · doi:10.1016/j.neuron.2012.09.023 · Cited by 756 · see citing works
Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition
Royer, S., Zemelman, B. V., Losonczy, A., Kim, J., Chance, F., Magee, J. C., & Buzsáki, G. (2012) · Nature Neuroscience · doi:10.1038/nn.3077 · Cited by 728 · see citing works
Dopaminergic neurons inhibit striatal output through non-canonical release of GABA
Tritsch, N. X., Ding, J. B., & Sabatini, B. L. (2012) · Nature · doi:10.1038/nature11466 · Cited by 576 · see citing works
Huang, Y.-Y., & Kandel, E. R. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.7.2446 · Cited by 544 · see citing works
Localization of dopamine D4 receptors in GABAergic neurons of the primate brain
Mrzljak, L., Bergson, C., Pappy, M., Huff, R., Levenson, R., & Goldman-Rakic, P. S. (1996) · Nature · doi:10.1038/381245a0 · Cited by 494 · see citing works
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 · see citing works
Dopamine controls persistence of long-term memory storage
Rossato, J. I., Bevilaqua, L. R. M., Izquierdo, I., Medina, J. H., & Cammarota, M. (2009) · Science · doi:10.1126/science.1172545 · Cited by 486 · see citing works
Feed-forward inhibition in the hippocampal formation
BUZSAKI, G. (1984) · Progress in Neurobiology · doi:10.1016/0301-0082(84)90023-6 · Cited by 453 · see citing works
Lisman, J. E., & Otmakhova, N. A. (2001) · Hippocampus · doi:10.1002/hipo.1071 · Cited by 402 · see citing works
Lesion to the nigrostriatal dopamine system disrupts stimulus-response habit formation
Faure, A., Haberland, U., Condé, F., & Massioui, N. E. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.3894-04.2005 · Cited by 402 · see citing works
Zakharenko, S. S., Patterson, S. L., Dragatsis, I., Zeitlin, S. O., Siegelbaum, S. A., Kandel, E. R., & Morozov, A. (2003) · Neuron · doi:10.1016/s0896-6273(03)00543-9 · Cited by 334 · see citing works
Dopamine neurons make glutamatergic synapses in vitro
Sulzer, D. L., Joyce, M. P., Lin, L., Geldwert, D., Haber, S. N., Hattori, T., & Rayport, S. (1998) · PubMed Central · doi:10.7916/d8-snm4-r132 · Cited by 316 · see citing works
Dopamine Neurons Make Glutamatergic SynapsesIn Vitro
Sulzer, D. L., Joyce, M. P., Lin, L., Geldwert, D., Haber, S. N., Hattori, T., & Rayport, S. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-12-04588.1998 · Cited by 304 · see citing works
Chemical and Genetic Engineering of Selective Ion Channel–Ligand Interactions
Magnus, C. J., Lee, P. H., Atasoy, D., Su, H. H., Looger, L. L., & Sternson, S. M. (2011) · Science · doi:10.1126/science.1206606 · Cited by 296 · see citing works
The discovery of central monoamine neurons gave volume transmission to the wired brain
Fuxé, K., Dahlström, A. B., JONSSON, G., Marcellino, D. J., Guescini, M., Dam, M., Manger, P. R., & Agnati, L. F. (2009) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2009.10.012 · Cited by 285 · see citing works
Parvalbumin-positive CA1 interneurons are required for spatial working but not for reference memory
Murray, A., Sauer, J., Riedel, G., McClure, C., Ansel-Bollepalli, L., Cheyne, L., Bartos, M., Wisden, W., & Wulff, P. (2011) · Nature Neuroscience · doi:10.1038/nn.2751 · Cited by 276 · see citing works
Bethus, I., Tse, D., & Morris, R. G. M. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.2721-09.2010 · Cited by 270 · see citing works
Gasbarri, A., Packard, M. G., Campana, E., & Pacitti, C. (1994) · Brain Research Bulletin · doi:10.1016/0361-9230(94)90288-7 · Cited by 266 · see citing works
Behavior-dependent specialization of identified hippocampal interneurons
Lapray, D., Lasztóczi, B., Lagler, M., Viney, T. J., Katona, L., Valenti, O., Hartwich, K., Borhegyi, Z., Somogyi, P., & Klausberger, T. (2012) · Nature Neuroscience · doi:10.1038/nn.3176 · Cited by 262 · see citing works
Bolton, M. M., Pittman, A. J., & Lo, D. C. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-09-03221.2000 · Cited by 201 · see citing works
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 182 · see citing works
CNS Dopamine Transmission Mediated by Noradrenergic Innervation
Smith, C. C., & Greene, R. W. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.6486-11.2012 · Cited by 178 · see citing works
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 174 · see citing works
Ventral hippocampal dopamine D1 and D2 systems and spatial working memory in rats
Wilkerson, A., & Levin, E. D. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00346-7 · Cited by 160 · see citing works
Distribution of D4 dopamine receptor in rat brain with sequence-specific antibodies
Defagot, M. C., Malchiodi, E. L., Villar, M. J., & Antonelli, M. C. (1997) · Molecular Brain Research · doi:10.1016/s0169-328x(96)00235-5 · Cited by 153 · see citing works
Basket cell dichotomy in microcircuit function
Armstrong, C., & Soltész, I. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2011.223669 · Cited by 136 · see citing works
Neuregulin-1 regulates LTP at CA1 hippocampal synapses through activation of dopamine D4 receptors
Kwon, O. B., Paredes, D., González, C. M., Neddens, J., Hernandez, L., Vullhorst, D., & Buonanno, A. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0805722105 · Cited by 134 · see citing works
Basu, J., Srinivas, K. V., Cheung, S. K., Taniguchi, H., Huang, Z. J., & Siegelbaum, S. A. (2013) · Neuron · doi:10.1016/j.neuron.2013.07.001 · Cited by 122 · see citing works
NMDA Receptors in Dopaminergic Neurons Are Crucial for Habit Learning
Wang, L. P., Li, F. R., Wang, D., Xie, K., Wang, D., Shen, X., & Tsien, J. Z. (2011) · Neuron · doi:10.1016/j.neuron.2011.10.019 · Cited by 122 · see citing works
Network mechanisms of theta related neuronal activity in hippocampal CA1 pyramidal neurons
Losonczy, A., Zemelman, B. V., Vaziri, A., & Magee, J. C. (2010) · Nature Neuroscience · doi:10.1038/nn.2597 · Cited by 118 · see citing works
Nissen, W., Szabo, A., Somogyi, J., Somogyi, P., & Lamsa, K. P. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.3481-09.2010 · Cited by 105 · see citing works
Andersson, R., Johnston, A. D., Herman, P. A., Winzer‐Serhan, U. H., Karavanova, I. D., Vullhorst, D., Fisahn, A., & Buonanno, A. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1201011109 · Cited by 100 · see citing works
Complementary Modulation of Somatic Inhibition by Opioids and Cannabinoids
Glickfeld, L. L., Atallah, B. V., & Scanziani, M. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.4700-07.2008 · Cited by 88 · see citing works
Fast-spiking non-pyramidal cells in the hippocampal CA3 region, dentate gyrus and subiculum of rats
Kawaguchi, Y., & Hama, K. (1987) · Brain Research · doi:10.1016/0006-8993(87)90518-x · Cited by 77 · see citing works
Hsu, K. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.76.3.1887 · Cited by 77 · see citing works
Homeostatic regulation of glutamatergic transmission by dopamine D <sub>4</sub> receptors
Yuen, E. Y., Zhong, P., & Yan, Z. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1010025108 · Cited by 54 · see citing works
Frequency-dependent signal transmission and modulation by neuromodulators
Ito, H. (2008) · Frontiers in Neuroscience · doi:10.3389/neuro.01.027.2008 · Cited by 38 · see citing works
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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 · see citing works
Kempadoo, K. A., Mosharov, E. V., Choi, S. J., Sulzer, D., & Kandel, E. R. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1616515114 · Cited by 647 · see citing works
Nobili, A., Latagliata, E. C., Viscomi, M. T., Cavallucci, V., Cutuli, D., Giacovazzo, G., Krashia, P., Rizzo, F. R., Marino, R., Federici, M., et al. (2017) · Nature Communications · doi:10.1038/ncomms14727 · Cited by 514 · see citing works
Novelty and Dopaminergic Modulation of Memory Persistence: A Tale of Two Systems
Duszkiewicz, A. J., McNamara, C. G., Takeuchi, T., & Genzel, L. (2018) · Trends in Neurosciences · doi:10.1016/j.tins.2018.10.002 · Cited by 307 · see citing works
Neuromodulation of hippocampal long-term synaptic plasticity
Palacios-Filardo, J., & Mellor, J. R. (2019) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.08.009 · Cited by 184 · see citing works
Broussard, J. I., Yang, K., Levine, A. T., Tsetsenis, T., Jenson, D., Cao, F., Garcia, I., Arenkiel, B. R., Zhou, F.-M., De Biasi, M., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.01.070 · Cited by 180 · see citing works
“Ce rectional, activity-dependent modulation of Schaffer collateral synapses in hippocampal slices (Rosen et al., 2015).”
BackgroundResultInfluentialThe content of hippocampal “replay”
Pfeiffer, B. E. (2017) · Hippocampus · doi:10.1002/hipo.22824 · Cited by 172 · see citing works
Sosa, M., & Giocomo, L. M. (2021) · Nature reviews. Neuroscience · doi:10.1038/s41583-021-00479-z · Cited by 142 · see citing works
Anterograde monosynaptic transneuronal tracers derived from herpes simplex virus 1 strain H129
Zeng, W., Jiang, H., Gang, Y., Song, Y., Shen, Z., Yang, H., Dong, X., Tian, Y., Ni, R., Liu, Y., et al. (2017) · Molecular Neurodegeneration · doi:10.1186/s13024-017-0179-7 · Cited by 140 · see citing works
Chemogenetic Tools for Causal Cellular and Neuronal Biology
Atasoy, D., & Sternson, S. M. (2017) · Physiological Reviews · doi:10.1152/physrev.00009.2017 · Cited by 130 · see citing works
Hippocampal 5-HT Input Regulates Memory Formation and Schaffer Collateral Excitation
Teixeira, C. M., Rosen, Z. B., Suri, D., Sun, Q., Hersh, M. A., Sargin, D., Dincheva, I., Morgan, A. A., Spivack, S., Krok, A. C., et al. (2018) · Neuron · doi:10.1016/j.neuron.2018.04.030 · Cited by 135 · see citing works
Two sources of dopamine for the hippocampus
McNamara, C. G., & Dupret, D. (2017) · Trends in Neurosciences · doi:10.1016/j.tins.2017.05.005 · Cited by 135 · see citing works
Positive reward prediction errors during decision-making strengthen memory encoding
Jang, A. I., Nassar, M. R., Dillon, D. G., & Frank, M. J. (2019) · Nature Human Behaviour · doi:10.1038/s41562-019-0597-3 · Cited by 129 · see citing works
Dopaminergic innervation and modulation of hippocampal networks
Edelmann, E., & Leßmann, V. (2018) · Cell and Tissue Research · doi:10.1007/s00441-018-2800-7 · Cited by 115 · see citing works
Locus Coeruleus and Dopamine-Dependent Memory Consolidation
Yamasaki, M., & Takeuchi, T. (2017) · Neural Plasticity · doi:10.1155/2017/8602690 · Cited by 91 · see citing works
La Barbera, L., Vedele, F., Nobili, A., Krashia, P., Spoleti, E., Latagliata, E. C., Cutuli, D., Cauzzi, E., Marino, R., Viscomi, M. T., et al. (2021) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2021.102031 · Cited by 98 · see citing works
“DA release in the hippocampus promotes spatial memory, reward-associated memory, novel-object recognition and memory consolidation (Broussard et al., 2016; Kempadoo et al., 2016; Mamad et al., 2017; McNamara et al., 2014; Rosen et al., 2015; Rossato et al., 2009; Takeuchi et al., 2016).”
Anatomy and Function of Ventral Tegmental Area Glutamate Neurons
Cai, J., & Tong, Q. (2022) · Frontiers in Neural Circuits · doi:10.3389/fncir.2022.867053 · Cited by 89 · see citing works
Tsetsenis, T., Badyna, J. K., Wilson, J., Zhang, X., Krizman, E. N., Subramaniyan, M., Yang, K., THOMAS, S. A., & Dani, J. A. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2111069118 · Cited by 83 · see citing works
Cordella, A., Krashia, P., Nobili, A., Pignataro, A., La Barbera, L., Viscomi, M. T., Valzania, A., Keller, F., Ammassari-Teule, M., Mercuri, N. B., et al. (2018) · Neurobiology of Disease · doi:10.1016/j.nbd.2018.05.006 · Cited by 82 · see citing works
VTA Projection Neurons Releasing GABA and Glutamate in the Dentate Gyrus
Ntamati, N. R., & Lüscher, C. (2016) · eNeuro · doi:10.1523/eneuro.0137-16.2016 · Cited by 78 · see citing works
Retailleau, A., & Morris, G. (2018) · Current Biology · doi:10.1016/j.cub.2018.01.081 · Cited by 74 · see citing works
Puighermanal, E., Cutando, L., Boubaker-Vitre, J., Honoré, È., Longueville, S., Hervé, D., & Valjent, E. (2016) · Brain Structure and Function · doi:10.1007/s00429-016-1314-x · Cited by 69 · see citing works
Dopaminergic regulation of hippocampal plasticity, learning, and memory
Tsetsenis, T., Broussard, J. I., & Dani, J. A. (2023) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.1092420 · Cited by 68 · see citing works
Modulation of hippocampal plasticity in learning and memory
Fuchsberger, T., & Paulsen, O. (2022) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2022.102558 · Cited by 66 · see citing works
Dahl, M. J., Kulesza, A., Werkle‐Bergner, M., & Mather, M. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105358 · Cited by 62 · see citing works
Spoleti, E., Barbera, L. L., Cauzzi, E., Paolis, M. L. D., Saba, L., Marino, R., Sciamanna, G., Lazzaro, V. D., Keller, F., Nobili, A., et al. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02408-9 · Cited by 61 · see citing works
Yang, K., Broussard, J. I., Levine, A. T., Jenson, D., Arenkiel, B. R., & Dani, J. A. (2017) · European Journal of Neuroscience · doi:10.1111/ejn.13406 · Cited by 58 · see citing works
Integrating the Roles of Midbrain Dopamine Circuits in Behavior and Neuropsychiatric Disease
Chen, A. P. F., Chen, L., Kim, T. A., & Xiong, Q. (2021) · Biomedicines · doi:10.3390/biomedicines9060647 · Cited by 55 · see citing works
Bacon, T., Pickering, A. E., & Mellor, J. R. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa159 · Cited by 54 · see citing works
Neuromodulation of the Feedforward Dentate Gyrus-CA3 Microcircuit
Prince, L. Y., Bacon, T., Tigaret, C. M., & Mellor, J. R. (2016) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2016.00032 · Cited by 51 · see citing works
Lörincz, M. L., & Adamantidis, A. (2016) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2016.09.003 · Cited by 51 · see citing works
Farrell, K., Lak, A., & Saleem, A. B. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111470 · Cited by 57 · see citing works
Barbera, L. L., Nobili, A., Cauzzi, E., Paoletti, I., Federici, M., Saba, L., Giacomet, C., Marino, R., Krashia, P., Melone, M., et al. (2022) · Molecular Neurodegeneration · doi:10.1186/s13024-022-00580-6 · Cited by 49 · see citing works
Sayegh, F. J. P., Moulédous, L., Macri, C., Macedo, J. P., Lejards, C., Rampon, C., Verret, L., & Dahan, L. (2024) · Nature Communications · doi:10.1038/s41467-024-47481-4 · Cited by 54 · see citing works
Coexistence of Multiple Types of Synaptic Plasticity in Individual Hippocampal CA1 Pyramidal Neurons
Edelmann, E., Cepeda-Prado, E., & Leßmann, V. (2017) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2017.00007 · Cited by 48 · see citing works
Dopamine D2R is Required for Hippocampal-dependent Memory and Plasticity at the CA3-CA1 Synapse
Espadas, I., Ortiz, Ó., García‐Sanz, P., Sanz‐Magro, A., Alberquilla, S., Solís, Ó., Delgado-Garcia, J. M., Gruart, A., & Moratalla, R. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa354 · Cited by 49 · see citing works
A flexible hippocampal population code for experience relative to reward
Sosa, M., Plitt, M. H., & Giocomo, L. M. (2025) · Nature Neuroscience · doi:10.1038/s41593-025-01985-4 · Cited by 49 · see citing works
Dopamine Modulates Delta-Gamma Phase-Amplitude Coupling in the Prefrontal Cortex of Behaving Rats
Andino-Pavlovsky, V., Souza, A. C., Scheffer-Teixeira, R., Tort, A. B. L., Etchenique, R., & Ribeiro, S. T. G. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00029 · Cited by 46 · see citing works
Qu, S., Meng, X., Liu, Y., Zhang, X., & Zhang, Y. (2019) · Aging · doi:10.18632/aging.101884 · Cited by 46 · see citing works
Longo, F., Mancini, M., Ibraheem, P. L., Aryal, S., Mesini, C., Patel, J. C., Penhos, E., Rahman, N., Mamcarz, M., Santini, E., et al. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01099-w · Cited by 47 · see citing works
Purkinje cell dopaminergic inputs to astrocytes regulate cerebellar-dependent behavior
Li, C., Saliba, N. B., Martin, H., Losurdo, N. A., Kolahdouzan, K., Siddiqui, R., Medeiros, D., & Li, W. (2023) · Nature Communications · doi:10.1038/s41467-023-37319-w · Cited by 46 · see citing works
Dopamine D2 Receptors in the Paraventricular Thalamus Attenuate Cocaine Locomotor Sensitization
Clark, A. M., Leroy, F., Martyniuk, K. M., Feng, W., McManus, E., Bailey, M. R., Javitch, J. A., Balsam, P. D., & Kellendonk, C. (2017) · eNeuro · doi:10.1523/eneuro.0227-17.2017 · Cited by 43 · see citing works
Amphetamine sensitization alters hippocampal neuronal morphology and memory and learning behaviors
Arroyo‐García, L. E., Tendilla‐Beltrán, H., Vázquez‐Roque, R. A., Jurado-Tapia, E. E., Díaz, A., Aguilar‐Alonso, P., Brambila, E., Monjaraz, E., de la Cruz, F., Moreno, A. R., et al. (2020) · Molecular Psychiatry · doi:10.1038/s41380-020-0809-2 · Cited by 45 · see citing works
Excitatory VTA to DH projections provide a valence signal to memory circuits
Han, Y., Zhang, Y., Kim, H. R., Grayson, V. S., Jovasevic, V., Ren, W., Centeno, M. V., Guedea, A. L., Meyer, M. A. A., Wu, Y., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-15035-z · Cited by 41 · see citing works
The VTA dopaminergic system as diagnostic and therapeutical target for Alzheimer's disease
Krashia, P., Spoleti, E., & D’Amelio, M. (2022) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2022.1039725 · Cited by 39 · see citing works
Expected Reward Value and Reward Uncertainty Have Temporally Dissociable Effects on Memory Formation
Stanek, J. K., Dickerson, K. C., Chiew, K. S., Clement, N. J., & Adcock, R. A. (2019) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_01411 · Cited by 36 · see citing works
Papaleonidopoulos, V., Kouvaros, S., & Papatheodoropoulos, C. (2018) · Synapse · doi:10.1002/syn.22033 · Cited by 34 · see citing works
Brzdąk, P., Wójcicka, O., Zaręba-Kozioł, M., Minge, D., Henneberger, C., Włodarczyk, J., Mozrzymas, J. W., & Wójtowicz, T. (2017) · Cerebral Cortex · doi:10.1093/cercor/bhx324 · Cited by 34 · see citing works
Testing Models of Human Declarative Memory at the Single-Neuron Level
Rutishauser, U. (2019) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2019.03.006 · Cited by 35 · see citing works
Tsetsenis, T., Badyna, J. K., Li, R., & Dani, J. A. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.887679 · Cited by 39 · see citing works
Kourosh‐Arami, M., Komaki, A., & Zarrindast, M. (2022) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/1871527321666220418115503 · Cited by 32 · see citing works
Hernández‐Frausto, M., Bilash, O. M., Masurkar, A. V., & Basu, J. (2023) · Frontiers in Neural Circuits · doi:10.3389/fncir.2023.1223891 · Cited by 33 · see citing works
Kobayashi, K., Imoto, Y., Yamamoto, F., Kawasaki, M., Ueno, M., Segi‐Nishida, E., & Suzuki, H. (2016) · Journal of Neurophysiology · doi:10.1152/jn.00740.2016 · Cited by 32 · see citing works
Social rank-associated stress vulnerability predisposes individuals to cocaine attraction
Yanovich, C., Kirby, M. L., Michaelevski, I., Yadid, G., & Pinhasov, A. (2018) · Scientific Reports · doi:10.1038/s41598-018-19816-x · Cited by 31 · see citing works
The Effects of Non-selective Dopamine Receptor Activation by Apomorphine in the Mouse Hippocampus
Arroyo‐García, L. E., Vázquez‐Roque, R. A., Díaz, A., Treviño, S., de la Cruz, F., Flores, G., & Moreno, A. R. (2018) · Molecular Neurobiology · doi:10.1007/s12035-018-0991-2 · Cited by 30 · see citing works
Neural Signals Related to Outcome Evaluation Are Stronger in CA1 than CA3
Lee, S.-H., Huh, N., Lee, J. W., Ghim, J.-W., Lee, I., & Jung, M. W. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00040 · Cited by 29 · see citing works
Spoleti, E., Krashia, P., Barbera, L. L., Nobili, A., Lupaşcu, C. A., Giacalone, E., Keller, F., Migliore, M., Renzi, M., & D’Amelio, M. (2021) · Experimental Neurology · doi:10.1016/j.expneurol.2021.113969 · Cited by 28 · see citing works
Furth, K. E., McCoy, A. J., Dodge, C., Walters, J. R., Buonanno, A., & Delaville, C. (2017) · PLoS ONE · doi:10.1371/journal.pone.0186732 · Cited by 28 · see citing works
Yang, X., Zou, L., Wang, K., Ye, X.-L., & Huang, T. (2019) · Neural Regeneration Research · doi:10.4103/1673-5374.262593 · Cited by 28 · see citing works
Xu, J., Wu, S., Huo, L., Zhang, Q., Liu, L., Ye, Z., Cao, J., Ma, H., Shang, C., & Ma, C. (2023) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2023.102477 · Cited by 27 · see citing works
Aberg, K. C., Kramer, E. E., & Schwartz, S. (2020) · Nature Communications · doi:10.1038/s41467-020-15542-z · Cited by 24 · see citing works
Long-term plasticity in identified hippocampal GABAergic interneurons in the CA1 area in vivo
Lau, P., Katona, L., Sághy, P., Newton, K., Somogyi, P., & Lamsa, K. P. (2016) · Brain Structure and Function · doi:10.1007/s00429-016-1309-7 · Cited by 25 · see citing works
Pupillo, F., Ortiz-Tudela, J., Bruckner, R., & Shing, Y. L. (2023) · npj Science of Learning · doi:10.1038/s41539-023-00166-x · Cited by 24 · see citing works
Mészáros, J., Cheung, T. H. C., Erler, M. M., Kang, U. J., Sameš, D., Kellendonk, C., & Sulzer, D. L. (2018) · eLife · doi:10.7554/elife.42383 · Cited by 23 · see citing works
Cepeda-Prado, E., Khodaie, B., Quiceno, G. D., Beythien, S., Edelmann, E., & Leßmann, V. (2021) · Cerebral Cortex · doi:10.1093/cercor/bhab306 · Cited by 22 · see citing works
Stöber, T. M., Lehr, A. B., Hafting, T., Kumar, A., & Fyhn, M. (2020) · Hippocampus · doi:10.1002/hipo.23256 · Cited by 20 · see citing works
Dallé, E., Daniels, W. M. U., & Mabandla, M. V. (2020) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2020/1941480 · Cited by 20 · see citing works
The DRD2 Taq1A A1 Allele May Magnify the Risk of Alzheimer’s in Aging African-Americans
Blum, K., Badgaiyan, R. D., Dunston, G. M., Baron, D. A., Modestino, E. J., McLaughlin, T., Steinberg, B., Gold, M. S., & Gondré‐Lewis, M. C. (2017) · Molecular Neurobiology · doi:10.1007/s12035-017-0758-1 · Cited by 21 · see citing works
Neural circuit dynamics of drug-context associative learning in the mouse hippocampus
Sun, Y., & Giocomo, L. M. (2022) · Nature Communications · doi:10.1038/s41467-022-34114-x · Cited by 19 · see citing works
Pramipexole restores depressed transmission in the ventral hippocampus following MPTP-lesion
Castro‐Hernández, J., Adlard, P. A., & Finkelstein, D. I. (2017) · Scientific Reports · doi:10.1038/srep44426 · Cited by 19 · see citing works
Kramar, C. P., Díaz, F. C., Gigante, E. D., Medina, J. H., & Barbano, M. F. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.15076 · Cited by 18 · see citing works
Non-canonical interplay between glutamatergic NMDA and dopamine receptors shapes synaptogenesis
Bénac, N., Saraceno, G. E., Butler, C., Kuga, N., Nishimura, Y., Yokoi, T., Su, P., Sasaki, T., Petit‐Pedrol, M., Galland, R., et al. (2024) · Nature Communications · doi:10.1038/s41467-023-44301-z · Cited by 17 · see citing works
Pham-Lake, C., Aronoff, E. B., Camp, C. R., Vester, A. I., Peters, S. J., & Caudle, W. M. (2017) · Environmental Toxicology and Pharmacology · doi:10.1016/j.etap.2017.02.003 · Cited by 17 · see citing works
Jin, X., Chen, Q., Song, Y., Zheng, J., Xiao, K., Shao, S. H., Fu, Z., Yi, M., Yang, Y., & Huang, Z. (2019) · The Journal of Physiology · doi:10.1113/jp277976 · Cited by 16 · see citing works
Mechanisms of neural organization and rhythmogenesis during hippocampal and cortical ripples
McKenzie, S., Nitzan, N., & English, D. F. (2020) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2019.0237 · Cited by 14 · see citing works
Sonneborn, A., & Greene, R. W. (2020) · Neuroscience Letters · doi:10.1016/j.neulet.2020.135450 · Cited by 17 · see citing works
Making memories last using the peripheral effect of direct current stimulation
Luckey, A. M., McLeod, S. L., Huang, Y., Mohan, A., & Vanneste, S. (2023) · eLife · doi:10.7554/elife.75586 · Cited by 17 · see citing works
Paolis, M. L. D., Loffredo, G., Krashia, P., Barbera, L. L., Nobili, A., Cauzzi, E., Babicola, L., Segni, M. D., Coccurello, R., Puglisi‐Allegra, S., et al. (2025) · Alzheimer s Research & Therapy · doi:10.1186/s13195-025-01736-4 · Cited by 16 · see citing works
Signed and unsigned effects of prediction error on memory: Is it a matter of choice?
Pupillo, F., & Bruckner, R. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105371 · Cited by 16 · see citing works
Rotenone impairs hippocampal neuronal activity in a rat model of Parkinson’s disease
Darbinyan, L., Hambardzumyan, L. E., Սիմոնյան, Կ. Վ., Chavushyan, V. A., Manukyan, L., & Sarkisian, V. H. (2017) · Pathophysiology · doi:10.1016/j.pathophys.2017.01.001 · Cited by 17 · see citing works
Remembering rewarding futures: A simulation‐selection model of the hippocampus
Jung, M. W., Lee, H., Jeong, Y., Lee, J. W., & Lee, I. (2018) · Hippocampus · doi:10.1002/hipo.23023 · Cited by 15 · see citing works
Munzuroğlu, M., Danışman, B., Akçay, G., Yelli, İ., Aslan, M., & Derin, N. (2022) · Brain Research · doi:10.1016/j.brainres.2022.148031 · Cited by 15 · see citing works
Sagheddu, C., Stojanovic, T., Kouhnavardi, S., Savchenko, A. A., Hussein, A. M., Pistis, M., Monje, F. J., Plasenzotti, R., Aufy, M., Studenik, C. R., et al. (2024) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2024.1357347 · Cited by 14 · see citing works
Learning deficits in rats overexpressing the dopamine transporter
Bernhardt, N. R., Lieser, M. K., Hlusicka, E. B., Habelt, B., Wieske, F., Edemann-Callesen, H., Garthe, A., & Winter, C. (2018) · Scientific Reports · doi:10.1038/s41598-018-32608-7 · Cited by 15 · see citing works
Sadeghian, A., Salari, Z., Azizi, H., Raoufy, M. R., Shojaei, A., Kosarmadar, N., Zare, M., Rezaei, M., Barkley, V., Javan, M., et al. (2020) · Brain Research · doi:10.1016/j.brainres.2020.146820 · Cited by 15 · see citing works
Single-trial dynamics of hippocampal spatial representations are modulated by reward value
Michon, F., Krul, E., Sun, J., & Kloosterman, F. (2021) · Current Biology · doi:10.1016/j.cub.2021.07.058 · Cited by 14 · see citing works
Honey and Alzheimer’s Disease—Current Understanding and Future Prospects
Shaikh, A., Ahmad, F., Teoh, S. L., Kumar, J., & Yahaya, M. F. (2023) · Antioxidants · doi:10.3390/antiox12020427 · Cited by 17 · see citing works
Liu, K., Yu, J., Zhao, J., Zhou, Y., Xiong, N., Xu, J., Wang, T., Bell, R. L., Qing, H., & Lin, Z. (2017) · Molecular Neurobiology · doi:10.1007/s12035-017-0781-2 · Cited by 13 · see citing works
Spatial localization of hippocampal replay requires dopamine signalingPreprint
Kleinman, M. R., & Foster, D. J. (2024) · eLife · doi:10.7554/elife.99678 · Cited by 13 · see citing works
Kobayashi, K., Mikahara, Y., Murata, Y., Morita, D., Matsuura, S., Segi‐Nishida, E., & Suzuki, H. (2020) · iScience · doi:10.1016/j.isci.2020.101025 · Cited by 12 · see citing works
A Dual Effect of Dopamine on Hippocampal LTP and Cognitive Functions in Control and Kindled Mice
Ahmadi, M., Rouhi, N., Fathollahi, Y., Shojaei, A., Rezaei, M., Rostami, S., Saab, B. J., & Mirnajafi‐Zadeh, J. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.0926-21.2023 · Cited by 11 · see citing works
suha, A. J., Hosseinmardi, N., & Janahmadi, M. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113547 · Cited by 11 · see citing works
Heer, C. M., & Sheffield, M. E. J. (2024) · eLife · doi:10.7554/elife.95213.4 · Cited by 11 · see citing works
Type 3 adenylyl cyclase in the MOE is involved in learning and memory in mice
Liu, X., Zhou, Y., Yang, D. J., Li, S., Liu, X., & Wang, Z. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.112533 · Cited by 11 · see citing works
McLaughlin, T., Han, D. C., Nicholson, J., Steinberg, B., Blum, K., Febo, M., Braverman, E. R., Li, M., Fried, L., & Badgaiyan, R. D. (2017) · Journal of Systems and Integrative Neuroscience · doi:10.15761/jsin.1000165 · Cited by 10 · see citing works
Apomorphine effects on the hippocampus
Arroyo‐García, L. E., Moreno, A. R., & Flores, G. (2018) · Neural Regeneration Research · doi:10.4103/1673-5374.241443 · Cited by 10 · see citing works
Heer, C. M., & Sheffield, M. E. J. (2024) · eLife · doi:10.7554/elife.95213 · Cited by 9 · see citing works
Ding, M., Tomsick, P. L., Young, R. A., & Jadhav, S. P. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.1670-24.2025 · Cited by 9 · see citing works
Case-Based Decision Neuroscience
Bhui, R. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-812098-9.00004-8 · Cited by 10 · see citing works
Ermine, C. M., Wright, J. L., Parish, C. L., Stanić, D., & Thompson, L. H. (2016) · Frontiers in Biology · doi:10.1007/s11515-016-1404-4 · Cited by 9 · see citing works
- Authors
- Rosen, Z. B., Cheung, S., & Siegelbaum, S. A.
- Affiliations
- Columbia University (US)
- Corresponding author
- Siegelbaum, Steven A
- ORCID
- Siegelbaum, Steven A
- Venue
- Nature Neuroscience
- Published
- 2015-11-02
- Volume
- 18
- Issue
- 12
- Pages
- 1763-1771
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC11186581
- OpenAlex
- W2184138621
- Cited by
- 183
- References
- 48
- Citations by year
- 2026: 11 · 2025: 21 · 2024: 30 · 2023: 15 · 2022: 16 · 2021: 12 · 2020: 16 · 2019: 11 · 2018: 16 · 2017: 21 · 2016: 13 · 2015: 1
- FWCI
- 10.23
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institutes of Health
- National Institute of Mental Health (T32MH015174)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- dopamine, ventral tegmental area, hippocampus, CA1 pyramidal neurons, Schaffer collateral synapses, perforant path, dopamine D1 receptor, dopamine D4 receptor, parvalbumin interneurons, feedforward inhibition, hippocampal-dependent memory, long-term potentiation
- MeSH terms
- Animals, Dopamine, Mesencephalon, Mice, Inbred C57BL, Mice, Transgenic, Neural Pathways, Synapses, Mice, CA1 Region, Hippocampal, CA3 Region, Hippocampal, Dopaminergic Neurons, Optogenetics
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