Effect of the nigrostriatal dopamine system on acquired neural responses in the striatum of behaving monkeys
Abstract
Dysfunction of the nigrostriatal dopamine system results in marked disorders of movement such as occur in Parkinson's disease. Functions of this dopamine-containing projection system were examined in monkeys trained in a classical conditioning task, and the effects of striatal dopamine depletion were tested. Unilateral dopamine loss substantially reduced the acquired sensory responsiveness of striatal neurons monitored electrophysiologically. This effect was ipsilateral and selective, and could be reversed by apomorphine. These results suggest that the primate nigrostriatal system modulates expression of neuronal response plasticity in the striatum during sensorimotor learning.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Dopamine depletion prevents the acquisition of sensory responses in striatal cells.
“As this model predicts, sensory responses are acquired in striatal cells over the course of reinforcement learning, and dopamine depletion prevents the acquisition of these responses [37, 39].”
From Cortical and basal ganglia contributions to habit learning and automaticity (2010) · cites this paper as [39]
Sensory responses are acquired in striatal cells over the course of reinforcement learning.
“As this model predicts, sensory responses are acquired in striatal cells over the course of reinforcement learning, and dopamine depletion prevents the acquisition of these responses [37, 39].”
From Cortical and basal ganglia contributions to habit learning and automaticity (2010) · cites this paper as [39]
Cites
Reversal of experimental parkinsonism by lesions of the subthalamic nucleus.
Bergman, H., Wichmann, T., & Delong, M. (1990) · Science · doi:10.1126/science.2402638 · Cited by 2,003 · see citing works
Grace, A. A. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90196-u · Cited by 1,831 · see citing works
Moore, R. Y., & Bloom, F. E. (1979) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.02.030179.000553 · Cited by 1,378 · see citing works
Schultz, W., Apicella, P., & Ljungberg, T. (1993) · The Journal of Neuroscience · doi:10.1523/jneurosci.13-03-00900.1993 · Cited by 1,291 · see citing works
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 · see citing works
Central Catecholamine Neuron Systems: Anatomy and Physiology of the Dopamine Systems
Moore, R. Y., & Bloom, F. E. (1978) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.01.030178.001021 · Cited by 931 · see citing works
A triple dissociation of memory systems: Hippocampus, amygdala, and dorsal striatum.
McDonald, R. J., & White, N. M. (1993) · Behavioral Neuroscience · doi:10.1037/0735-7044.107.1.3 · Cited by 885 · see citing works
Long-term synaptic depression in the striatum: physiological and pharmacological characterization
Calabresi, P., Maj, R., Pisani, A., Mercuri, N. B., & Bernardi, G. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-11-04224.1992 · Cited by 673 · see citing works
The Effect of Deprenyl (Selegiline) on the Natural History of Parkinson's Disease
Tetrud, J. W., & Langston, J. W. (1989) · Science · doi:10.1126/science.2502843 · Cited by 635 · see citing works
Aosaki, T., Tsubokawa, H., Ishida, A., Watanabe, K., Graybiel, A. M., & Kimura, M. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-06-03969.1994 · Cited by 600 · see citing works
Self-citationPROCEDURAL LEARNING AND NEOSTYRIAL DYSFUNCTION IN MAN
Saint‐Cyr, J. A., TAYLOR, A. E., & Lang, A. E. (1988) · Brain · doi:10.1093/brain/111.4.941 · Cited by 531 · see citing works
Wilson, C. J., Chang, H., & Kitai, S. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-02-00508.1990 · Cited by 511 · see citing works
TEMPORAL DISCRIMINATION IS ABNORMAL IN PARKINSON'S DISEASE
Artieda, J., Pastor, M. A., Lacruz, F. A., & Obeso, J. A. (1992) · Brain · doi:10.1093/brain/115.1.199 · Cited by 416 · see citing works
FLOWERS, K. A. (1976) · Brain · doi:10.1093/brain/99.2.269 · Cited by 382 · see citing works
Cognitive and motor shifting aptitude disorder in Parkinson's disease.
Cools, A. R., van den Bercken, J. H., Horstink, M. W. I. M., van Spaendonck, K. P. M., & Berger, H. J. C. (1984) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.47.5.443 · Cited by 371 · see citing works
Biochemistry and pharmacology of the basal ganglia
Yahr, M. D. (1965) · International Journal of Neuropharmacology · doi:10.1016/0028-3908(65)90018-3 · Cited by 294 · see citing works
Carli, M., Evenden, J. L., & Robbins, T. W. (1985) · Nature · doi:10.1038/313679a0 · Cited by 284 · see citing works
Tonically discharging putamen neurons exhibit set-dependent responses.
Kimura, M., Rajkowski, J., & Evarts, E. V. (1984) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.81.15.4998 · Cited by 276 · see citing works
Self-citationOpponent process theory of motivation: Neurobiological evidence from studies of opiate dependence
Koob, G. F., Stinus, L., Moal, M. L., & Bloom, F. E. (1989) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(89)80022-3 · Cited by 268 · see citing works
Voigtlander, P. F. V., & Moore, K. E. (1973) · Neuropharmacology · doi:10.1016/0028-3908(73)90061-0 · Cited by 207 · see citing works
Brotchie, J. M., Mitchell, I. J., Sambrook, M. A., et al. (1991) · Movement Disorders · doi:10.1002/mds.870060208 · Cited by 203 · see citing works
Calabresi, P., Maj, R., Mercuri, N. B., & Bernardi, G. (1992) · Neuroscience Letters · doi:10.1016/0304-3940(92)90628-k · Cited by 201 · see citing works
Schultz, W. (1982) · Progress in Neurobiology · doi:10.1016/0301-0082(82)90015-6 · Cited by 199 · see citing works
Sawaguchi, T., Matsumura, M., & Kubota, K. (1990) · Journal of Neurophysiology · doi:10.1152/jn.1990.63.6.1401 · Cited by 199 · see citing works
Kawaguchi, Y. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.67.6.1669 · Cited by 186 · see citing works
Tonically discharging neurons of monkey striatum respond to preparatory and rewarding stimuli
Apicella, P., Scarnati, E., & Schultz, W. (1991) · Experimental Brain Research · doi:10.1007/bf00230981 · Cited by 183 · see citing works
Sawaguchi, T., Matsumura, M., & Kubota, K. (1990) · Journal of Neurophysiology · doi:10.1152/jn.1990.63.6.1385 · Cited by 169 · see citing works
A triple dissociation of memory systems: Hippocampus, amygdala, and dorsal striatum.
McDonald, R., & White, N. (1993) · Behavioral Neuroscience · doi:10.1037/a0034883 · Cited by 146 · see citing works
Graybiel, A. M., Hirsch, É. C., & Agid, Y. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.1.303 · Cited by 145 · see citing works
Self-citationPhysiological properties of projection neurons in the monkey striatum to the globus pallidus
Kimura, M., Kato, M., & Shimazaki, H. (1990) · Experimental Brain Research · doi:10.1007/bf00228811 · Cited by 114 · see citing works
Self-citationImai, H., Nakamura, T., Endo, K., et al. (1988) · Brain Research · doi:10.1016/0006-8993(88)90446-5 · Cited by 58 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience?
Berridge, K. C., & Robinson, T. E. (1998) · Brain Research Reviews · doi:10.1016/s0165-0173(98)00019-8 · Cited by 4,127 · see citing works
Depue, R. A., & Collins, P. F. (1999) · Behavioral and Brain Sciences · doi:10.1017/s0140525x99002046 · Cited by 2,046 · see citing works
Habits, Rituals, and the Evaluative Brain
Graybiel, A. M. (2008) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.29.051605.112851 · Cited by 1,697 · see citing works
Self-citationLearning and Memory Functions of the Basal Ganglia
Packard, M. G., & Knowlton, B. J. (2002) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.25.112701.142937 · Cited by 1,717 · see citing works
The primate basal ganglia: Parallel and integrative networks
Haber, S. N. (2003) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2003.10.003 · Cited by 1,479 · 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
The Basal Ganglia and Adaptive Motor Control
Graybiel, A. M., Aosaki, T., Flaherty, A. W., & Kimura, M. (1994) · Science · doi:10.1126/science.8091209 · Cited by 1,324 · see citing works
Self-citationNeuronal Reward and Decision Signals: From Theories to Data
Schultz, W. (2015) · Physiological Reviews · doi:10.1152/physrev.00023.2014 · Cited by 1,126 · see citing works
The Basal Ganglia and Chunking of Action Repertoires
Graybiel, A. M. (1998) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1998.3843 · Cited by 1,042 · see citing works
Dopamine reward prediction-error signalling: A two-component response
Schultz, W. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2015.26 · Cited by 1,036 · see citing works
depue, R. A., & morrone-strupinsky, J. V. (2005) · Behavioral and Brain Sciences · doi:10.1017/s0140525x05000063 · Cited by 958 · see citing works
Toward a neurobiology of obsessive-compulsive disorder
Graybiel, A. M., & Rauch, S. L. (2000) · Neuron · doi:10.1016/s0896-6273(00)00113-6 · Cited by 864 · see citing works
Self-citationA cellular mechanism of reward-related learning
Reynolds, J. N. J., Hyland, B. I., & Wickens, J. R. (2001) · Nature · doi:10.1038/35092560 · Cited by 879 · see citing works
Dopamine-mediated regulation of corticostriatal synaptic plasticity
Calabresi, P., Picconi, B., Tozzi, A., & Di Filippo, M. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.03.001 · Cited by 865 · see citing works
Striatal Dopamine Release Is Triggered by Synchronized Activity in Cholinergic Interneurons
Threlfell, S., Lalic, T., Platt, N. J., Jennings, K. A., Deisseroth, K., & Cragg, S. J. (2012) · Neuron · doi:10.1016/j.neuron.2012.04.038 · Cited by 845 · 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
Dissociable Neural Responses in Human Reward Systems
Elliott, R., Friston, K. J., & Dolan, R. J. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-16-06159.2000 · Cited by 740 · see citing works
Distinct basal ganglia territories are engaged in early and advanced motor sequence learning
Lehéricy, S., Benali, H., Van de Moortele, P.-F., Pélégrini-Issac, M., Waechter, T., Ugurbil, K., & Doyon, J. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0502762102 · Cited by 634 · see citing works
Physiology and pharmacology of striatal neurons
Kreitzer, A. C. (2009) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.051508.135422 · Cited by 530 · see citing works
Functional diversity and specificity of neostriatal interneurons
Tepper, J. M., & Bolam, J. P. (2004) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2004.10.003 · Cited by 526 · see citing works
Cortical and basal ganglia contributions to habit learning and automaticity
Ashby, F. G., Turner, B. O., & Horvitz, J. C. (2010) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2010.02.001 · Cited by 481 · 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
Correlated Coding of Motivation and Outcome of Decision by Dopamine Neurons
Satoh, T., Nakai, S., Sato, T., & Kimura, M. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-30-09913.2003 · Cited by 298 · see citing works
Self-citationNeural mechanisms of reward-related motor learning
Wickens, J. R., Reynolds, J. N., & Hyland, B. I. (2003) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2003.10.013 · Cited by 284 · see citing works
Mnemonic functions of the basal ganglia
White, N. M. (1997) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(97)80004-9 · Cited by 204 · see citing works
Functional Specificity of Ventral Striatal Compartments in Appetitive Behaviors
KELLEY, A. E. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb09262.x · Cited by 198 · see citing works
McKinley, J. W., Shi, Z., Kawikova, I., Hur, M., Bamford, I. J., Sudarsana Devi, S. P., Vahedipour, A., Darvas, M., & Bamford, N. S. (2019) · Neuron · doi:10.1016/j.neuron.2019.06.013 · Cited by 130 · see citing works
Multiphasic modulation of cholinergic interneurons by nigrostriatal afferents
Straub, C., Tritsch, N. X., Hagan, N. A., Gu, C., & Sabatini, B. L. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0589-14.2014 · Cited by 130 · see citing works
Leckman, J. F., & Riddle, M. A. (2000) · Neuron · doi:10.1016/s0896-6273(00)00114-8 · Cited by 121 · see citing works
Verschueren, S. M. P., Swinnen, S. P., Dom, R., & De Weerdt, W. (1997) · Experimental Brain Research · doi:10.1007/pl00005602 · Cited by 96 · see citing works
Regulation of striatal cells and goal-directed behavior by cerebellar outputs
Xiao, L., Bornmann, C., Hatstatt-Burklé, L., & Scheiffele, P. (2018) · Nature Communications · doi:10.1038/s41467-018-05565-y · Cited by 82 · see citing works
Stimulus-response and response-outcome learning mechanisms in the striatum
Horvitz, J. C. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.12.014 · Cited by 58 · see citing works
- Authors
- Aosaki, T., Graybiel, A. M., & Kimura, M.
- Affiliations
- Massachusetts Institute of Technology (US)
- The University of Osaka (JP)
- Venue
- Science
- Published
- 1994-07-15
- Volume
- 265
- Issue
- 5170
- Pages
- 412-415
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W2076464393
- Cited by
- 427
- References
- 31
- Citations by year
- 2026: 12 · 2025: 16 · 2024: 10 · 2023: 4 · 2022: 18 · 2021: 9 · 2020: 10 · 2019: 12 · 2018: 10 · 2017: 13 · 2016: 15 · 2015: 13 · 2014: 9 · 2013: 9 · 2012: 12
- FWCI
- 4.24
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (R01 NS25529, R01NS025529)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Health Sciences › Medicine › Neurology › Neurological disorders and treatments
- Keywords
- nigrostriatal dopamine system, striatum, dopamine depletion, sensorimotor learning, classical conditioning, apomorphine, Parkinson's disease, primate behavior
- MeSH terms
- Action Potentials, Animals, Apomorphine, Behavior, Animal, Conditioning, Classical, Corpus Striatum, Dopamine, Haloperidol, Macaca, Male, Neuronal Plasticity, Neurons, Substantia Nigra, 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine
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