Cited by 1,593Neurotransmitter Receptor Influence on BehaviorNeuroscience and Neuropharmacology ResearchNeural dynamics and brain function

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Modulation of memory fields by dopamine Dl receptors in prefrontal cortex

Williams, Graham V., Goldman-Rakic, Patricia S.·1995·Nature

DOI 10.1038/376572a0

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Abstract

Dopamine has been implicated in the cognitive process of working memory but the cellular basis of its action has yet to be revealed. By combining iontophoretic analysis of dopamine receptors with single-cell recording during behaviour, we found that D1 antagonists can selectively potentiate the 'memory fields' of prefrontal neurons which subserve working memory. The precision shown for D1 receptor modulation of mnemonic processing indicates a direct gating of selective excitatory synaptic inputs to prefrontal neurons during cognition.

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“Some studies suggest that DA strengthens the effects of strong depolarizing currents and enhances task-related neural activity [ 67 ] through the activation of D1 receptors, which enhances persistent NA + ,L -type Ca 2+ ,a ndN-methyl-D- aspartate currents in PFC pyra-”
Background
Relationship of dopamine D1 receptor binding in striatal and extrastriatal regions to cognitive functioning in healthy humans
Karlsson, S., Rieckmann, A., Karlsson, P., Farde, L., Nyberg, L. H., & Bäckman, L. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.04.047 · Cited by 28
“Much of this work has involved administering D1 receptor agonists or antagonists to both non-human primates (Sawaguchi and Goldman-Rakic, 1994; Wang et al., 2004; Williams and Goldman-Rakic, 1995) and humans (Kimberg and D'Esposito, 2003;Müller et al., 1998).”
Background
Strain differences in profiles of dopaminergic neurotransmission in the prefrontal cortex of the BALB/C vs. C57Bl/6 mice: Consequences of stress and afobazole
Anderzhanova, E. A., Bächli, H., Бунеева, О. А., Narkevich, V. B., Medvedev, A. E., Thoeringer, C. K., Wotjak, C. T., & Кудрин, В. С. (2013) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2013.03.015 · Cited by 28
Selective activation of D 1dopamine receptors impairs sensorimotor gating in L ong– E vans rats
Mosher, L. J., Frau, R., Pardu, A., Pes, R., Devoto, P., & Bortolato, M. (2015) · British Journal of Pharmacology · doi:10.1111/bph.13232 · Cited by 27
“In particular, both overstimulation and suppression of D1 receptors may result in impairments of working memory (Williams and Goldman-Rakic, 1995), a core cognitive deficit of schizophrenia.”
Background
Cellular Mechanisms for Dopamine D4 Receptor-induced Homeostatic Regulation of α-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic Acid (AMPA) Receptors
Yuen, E. Y., & Yan, Z. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.221416 · Cited by 29
N-Methyl-d-aspartate receptor in working memory impairments in schizophrenia: event-related potential study of late stage of working memory process
Ahn, K.-H., Youn, T., Cho, S. S., Ha, T. H., Ha, K., Kim, M., & Kwon, J. S. (2003) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/s0278-5846(03)00159-3 · Cited by 28
“…(NMDA) (Adler et al., 1998; Danysz et al., 1988; Krystal et al., 1994; Li et al., 1997; Wozniak et al., 1990) and dopamine (Goldman-Rakic, 1999; Williams and Goldman-Rakic, 1995), are suggested to be related to pathologic process of WM dysfunction in schizophrenic patients for decreased…”
Background
Genetic Variation in the Dopamine System Influences Intervention Outcome in Children with Cerebral Palsy
Heijtz, R. D., Almeida, R., Eliasson, A., & Forssberg, H. (2018) · EBioMedicine · doi:10.1016/j.ebiom.2017.12.028 · Cited by 28
“Cognition and executive functions reach peak performance at optimal levels of dopamine; too low or too high dopamine levels result in poorer performance (Williams and Goldmanrakic, 1995; Thirugnanasambandam et al., 2011) These results suggest that it is possible to augment treatment outcomes in non-responders with low…”
Background
Dopamine Receptor Expression Among Local and Visual Cortex-Projecting Frontal Eye Field Neurons
Mueller, A. L., Krock, R. M., Shepard, S. B., & Moore, T. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhz078 · Cited by 33
Performance- and task-dependent effects of the dopamine D1/D5 receptor agonist SKF 38393 on learning and memory in the rat
Amico, F., Spowart-Manning, L., Anwyl, R., & Rowan, M. J. (2007) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2007.08.039 · Cited by 29
Chemical neuromodulation of frontal-executive functions in humans and other animals
Robbins, T. W. (2000) · Springer eBooks · doi:10.1007/978-3-642-59794-7_14 · Cited by 27
Dopamine transporter-immunoreactive axons in the mediodorsal thalamic nucleus of the macaque monkey
Melchitzky, D. S., & Lewis, D. A. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00021-5 · Cited by 29
WITHDRAWN: Neurofeedback-mediated self-regulation of the dopaminergic midbrain
Sulzer, J. S., Sitaram, R., Blefari, M. L., Kollias, S., Birbaumer, N., Stephan, K. E., Luft, A. R., & Gassert, R. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.02.041 · Cited by 27
Retracted
Dopamine Beta Hydroxylase Genotype Identifies Individuals Less Susceptible to Bias in Computer-Assisted Decision Making
Parasuraman, R., de Visser, E. J., Lin, M., & Greenwood, P. M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0039675 · Cited by 31
“decisions in working memory tasks [22–24].”
Increased spontaneous gamma power and synchrony in schizophrenia patients having higher minor physical anomalies
Tikka, S. K., Nizamie, S. H., Das, B., Katshu, M. Z. U. H., & Goyal, N. (2012) · Psychiatry Research · doi:10.1016/j.psychres.2012.09.006 · Cited by 29
“The effect of dopamine on gamma activity may be through its known modulation of GABAergic neurons (through DRD1/D2 receptors) and glutamatergic neurons (through DRD1/D5 receptors) (Williams and Goldman-Rakic, 1995; Lavin and Grace, 2001; O’Donnell, 2003; Seamans and Yang, 2004).”
Background
Dopamine D1 and D2 Receptors Make Dissociable Contributions to Dorsolateral Prefrontal Cortical Regulation of Rule-Guided Oculomotor Behavior
Vijayraghavan, S., Major, A. J., & Everling, S. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.06.031 · Cited by 28
Dopaminergic inhibition of excitatory inputs onto pyramidal tract neurons in cat motor cortex
Huda, K., Salunga, T. L., & Matsunami, K. (2001) · Neuroscience Letters · doi:10.1016/s0304-3940(01)01960-7 · Cited by 27
Localization of pontine PGO wave generation sites and their anatomical projections in the rat
Datta, S., Siwek, D. F., Patterson, E. H., & Cipolloni, P. B. (1998) · Synapse · doi:10.1002/(sici)1098-2396(199812)30:4 · Cited by 162
The Schizophrenia Spectrum Personality Disorders
Chemerinski, E., & Siever, L. J. (2010) · Wiley eBooks · doi:10.1002/9781444327298.ch5 · Cited by 27
Seeking Brain Biomarkers for Preventive Therapy in Huntington Disease
Esmaeilzadeh, M., Ciarmiello, A., & Squitieri, F. (2010) · CNS Neuroscience & Therapeutics · doi:10.1111/j.1755-5949.2010.00157.x · Cited by 25
“Proper performance in prefrontal cortex-related cognitive tasks such as working memory and attentional functions require a critical level of dopamine and dopamine D1 receptor stimulation [118,119].”
Background
Association study of dopamine receptor genes polymorphism with cognitive functions in bipolar I disorder patients
Zhao, L., Lin, Y., Lao, G., Wang, Y., Guan, L., Wei, J., Yang, Z., Ni, P., Li, X., Jiang, Z., et al. (2014) · Journal of Affective Disorders · doi:10.1016/j.jad.2014.08.039 · Cited by 30
Intra-nigral MPTP lesion in rats: Behavioral and autoradiography studies
Perry, J. C., Hipólide, D. C., Tufik, S., Martins, R. D., Cunha, C. D., Andreatini, R., & Vital, M. A. B. F. (2005) · Experimental Neurology · doi:10.1016/j.expneurol.2005.05.009 · Cited by 26
Attractor Neural Networks and Spatial Maps in Hippocampus
Tsodyks, M. V. (2005) · Neuron · doi:10.1016/j.neuron.2005.10.006 · Cited by 25
Tolcapone Suppresses Ethanol Intake in Alcohol‐Preferring Rats Performing a Novel Cued Access Protocol
McCane, A. M., Czachowski, C. L., & Lapish, C. C. (2014) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.12515 · Cited by 23
“The relationship between the bioavailability of DA and cognitive performance is hypothesized to follow an inverted-U shaped function (Williams and Goldman-Rakic, 1995).”
Working memory functioning in children with attention-deficit/hyperactivity disorder (ADHD): A comparison between subtypes and normal controls
Cockcroft, K. (2011) · Journal of Child and Adolescent Mental Health · doi:10.2989/17280583.2011.634545 · Cited by 37
“Further, working memory function is dependent on dopamine, which is consistent with the association between ADHD and atypical dopaminergic transmission (Cook et al. 1995, Williams and Goldman-Rakic 1995).”
Result
Amphetamine depresses excitatory synaptic transmission at prefrontal cortical layer V synapses
Mair, R. D., & Kauer, J. A. (2006) · Neuropharmacology · doi:10.1016/j.neuropharm.2006.07.004 · Cited by 26
An inexpensive drivable cannulated microelectrode array for simultaneous unit recording and drug infusion in the same brain nucleus of behaving rats
du Hoffmann, J., Kim, J. J., & Nicola, S. M. (2011) · Journal of Neurophysiology · doi:10.1152/jn.00349.2011 · Cited by 26
Cholinergic depletion in nucleus accumbens impairs mesocortical dopamine activation and cognitive function in rats
Laplante, F., Zhang, Z.-W., Huppé‐Gourgues, F., Dufresne, M. M., Vaucher, E., & Sullivan, R. M. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.07.033 · Cited by 29
“Prefrontal DA is a key regulator of these cognitive functions in rats and monkeys (Brozoski et al., 1979; Granon et al., 2000; Seamans et al., 1998; Williams and Goldman-Rakic, 1995), and best cognitive performance requires an optimal window of cortical DA activity (D1mediated), either too much or too little DA impair…”
Verbal makes it positive, spatial makes it negative: Working memory biases judgments, attention, and moods.
Storbeck, J., & Watson, P. (2014) · Emotion · doi:10.1037/a0037327 · Cited by 28
Levodopa medication improves incidental sequence learning in Parkinson's disease
Beigi, M., Wilkinson, L., Gobet, F. R., Parton, A. D., & Jahanshahi, M. (2016) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2016.09.019 · Cited by 26
“…is described by an inverted U curve, where too little or much dopamine may be detrimental to performance, it is unclear the degree to which patients with PD will be impaired on SRTT learning on or o ﬀ medication (Cools et al., 2001; Goldman-Rakic, 1999; Williams and Goldman-Rakic, 1995).”
Background
Distribution of protein phosphatases‐1α and ‐1γ1 and the D1 dopamine receptor in primate prefrontal cortex: Evidence for discrete populations of spines
Muly, E. C., Greengard, P., & Goldman, P. S. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1384 · Cited by 26
Cognitive slowing in Parkinson's disease resolves after practice
Press, D. Z. (2002) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.73.5.524 · Cited by 26
Processing efficiency of a verbal working memory system is modulated by amphetamine: an fMRI investigation
Tipper, C. M., Cairo, T. A., Woodward, T. S., Phillips, A. G., Liddle, P. F., & Ngan, E. T. C. (2005) · Psychopharmacology · doi:10.1007/s00213-005-0025-4 · Cited by 34
“PFC are optimized within a specific range of DA activity (Arnsten 1998; Williams and Goldman-Rakic 1995; Zahrt et al. 1997).”
Background
The synergy of working memory and inhibitory control: Behavioral, pharmacological and neural functional evidences
Grégoire, S., Rivalan, M., Le Moine, C., & Dellu-Hagedorn, F. (2012) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2011.12.003 · Cited by 30
“This aspect of working memory has been associated with firing in local PFC circuits and is modulated by D1 receptor activity (McNab et al., 2009; Sawaguchi, Matsumura, & Kubota, 1988; Williams & Goldman-Rakic, 1995).”
Background
LP-BM5 infection impairs spatial working memory in C57BL/6 mice in the Morris water maze.
Lee, B., English, J. A., & Paul, I. A. (2000) · Brain Research · doi:10.1016/s0006-8993(99)02381-1 · Cited by 15
Systematic reviews of the acute effects of amphetamine on working memory and other cognitive performances in healthy individuals, with a focus on the potential influence of personality traits
Kassim, F. M. (2023) · Human Psychopharmacology: Clinical and Experimental · doi:10.1002/hup.2856 · Cited by 11
Noise Stress Impairs Prefrontal Cortical Cognitive Function in Monkeys: Evidence for a Hyperdopaminergic Mechanism
Arnsten, A. F. T., & Goldman-Rakic, P. S. (1998) · Archives of General Psychiatry · doi:10.1001/archpsyc.55.4.362 · Cited by 6
Self-citation
The Neurochemical Modulation of Prefrontal Control Processes
Robbins, T. W., & Kehagia, A. A. (2017) · The Wiley Handbook of Cognitive Control · doi:10.1002/9781118920497.ch19 · Cited by 4
Cortico-hippocampal communication by way of parallel parahippocampal-subicular pathways.
Lavenex (2000) · Pure Amsterdam UMC · doi:10.1002/1098-1063(2000)10:4 · Cited by 1
Effects of a secure attachment relationship on right brain development, affect regulation, and infant mental health
Schore, A. N. (2001) · Infant Mental Health Journal · doi:10.1002/1097-0355(200101/04)22:1

Authors: Williams, G. V., & Goldman-Rakic, P. S.
Affiliations: Yale University (US)
ORCID: Williams, Graham V.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 1995-08
Volume: 376
Issue: 6541
Pages: 572-575
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/376572a0
OpenAlex: W2084007108
Cited by: 1,593
References: 42
Citations by year: 2026: 17 · 2025: 13 · 2024: 29 · 2023: 26 · 2022: 36 · 2021: 30 · 2020: 27 · 2019: 27 · 2018: 37 · 2017: 33 · 2016: 48 · 2015: 63 · 2014: 45 · 2013: 78 · 2012: 74
FWCI: 16.39
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Keywords: dopamine D1 receptor, working memory, prefrontal cortex, memory field, dopamine D1 receptor antagonist, synaptic modulation, excitatory synaptic input, iontophoresis, single-unit recording
MeSH terms: Animals, Haplorhini, Dose-Response Relationship, Drug, Iontophoresis, Memory, Neurons, Psychomotor Performance, Prefrontal Cortex, Receptors, Dopamine D1, Receptors, Dopamine D2

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Modulation of memory fields by dopamine Dl receptors in prefrontal cortex

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