Cited by 1,154Schizophrenia research and treatmentNeurotransmitter Receptor Influence on BehaviorParkinson's Disease Mechanisms and Treatments

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Schizophrenia is associated with elevated amphetamine-induced synaptic dopamine concentrations: Evidence from a novel positron emission tomography method

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Breier, A., Su, T.-P., Saunders, R., Carson, R. E., Kolachana, B. S., de Bartolomeis, A., Weinberger, D. R., Weisenfeld, N., Malhotra, A. K., Eckelman, W. C., Pickar, D.·1997·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.94.6.2569PMC PMC20129

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Abstract

A major line of evidence that supports the hypothesis of dopamine overactivity in schizophrenia is the psychomimetic potential of agents such as amphetamine that stimulate dopamine outflow. A novel brain imaging method provides an indirect measure of in vivo synaptic dopamine concentration by quantifying the change in dopamine receptor radiotracer binding produced by agents that alter dopamine release but do not themselves bind to dopamine receptors. The purpose of this investigation is (i) to determine the sensitivity (i.e., amount of dopamine reflected in radiotracer binding changes) of this method by examining the relationship between amphetamine-induced changes in simultaneously derived striatal extracellular dopamine levels with in vivo microdialysis and striatal binding levels with the dopamine D2/D3 positron-emission tomography radioligand [11C]raclopride in nonhuman primates, and (ii) to test the hypothesis of elevated amphetamine-induced synaptic dopamine levels in schizophrenia. In the nonhuman primate study (n = 4), doubling the amphetamine dose produced a doubling in [11C]raclopride specific binding reductions. In addition, the ratio of percent mean dopamine increase to percent mean striatal binding reduction for amphetamine (0.2 mg/kg) was 44:1, demonstrating that relatively small binding changes reflect large changes in dopamine outflow. In the clinical study, patients with schizophrenia (n = 11) compared with healthy volunteers (n = 12) had significantly greate…

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Background
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Background
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Background
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Result
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BackgroundMethodInfluential
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Method
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Background
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Background
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Background
Long-term stability of measuring D(2) receptors in schizophrenia patients treated with antipsychotics.
Uchida, H., Graff-Guerrero, A., Mulsant, B., Pollock, B., & Mamo, D. (2009) · Schizophrenia Research · doi:10.1016/j.schres.2008.12.022 · Cited by 16
“In schizophrenia, [(11)C]raclopride has contributed to understanding the basic mechanism of this illness (Breier et al., 1997) and the mechanism of action and dosing of antipsychotics in younger adults (Farde et al.”
Cortical cholinergic deficiency enhances amphetamine-induced dopamine release in the accumbens but not striatum
Mattsson, A., Olson, L., Svensson, T. H., & Schilström, B. (2007) · Experimental Neurology · doi:10.1016/j.expneurol.2007.07.012 · Cited by 15
Neonatal functional blockade of the entorhinal cortex results in disruption of accumbal dopaminergic responses observed in latent inhibition paradigm in adult rats
Peterschmitt, Y., Meyer, F., & Louilot, A. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05503.x · Cited by 16
“…dopamine (DA) release than in healthy subjects and is associated with the emergence or aggravation of the positive symptoms (Laruelle et al., 1996; Breier et al., 1997; Abi-Dargham et al., 1998) lend support to the common assumption that there is a functional disturbance of the mesencephalic…”
Background
Dopamine presynaptically depresses fast inhibitory synaptic transmission via D4 receptor-protein kinase A pathway in the rat dorsolateral septal nucleus.
Asaumi, Y., Hasuo, H., & Akasu, T. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00966.2005 · Cited by 16
Tyrosine‐free amino acid mixture attenuates amphetamine‐induced displacement of [11C]raclopride in striatum in vivo: A rat PET study
Masurier, M. L., Houston, G., Cowen, P., Grasby, P., Sharp, T., & Hume, S. (2004) · Synapse · doi:10.1002/syn.10285 · Cited by 16
“…[11C]raclopride decreases following electrical stimulation of dopamine neurones (Ginovart et al., 1998), or administration of dopamine-releasing drugs such as amphetamine (Breier et al., 1997; Dewey et al., 1993; Hume et al., 1992; Laruelle et al., 1996) and NMDA antagonists (Breier et al., 1998).”
Influential
PET Measurement of rCBF in the presence of a neurochemical tracer.
Converse, A., Barnhart, T., Dabbs, K., Dejesus, O., Larson, J. A., Nickles, R., Schneider, M., & Roberts, A. (2004) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2003.09.006 · Cited by 16
“Support was also provided by the University of Wisconsin HealthEmotions Research Institute.”
BackgroundMethod
Demonstration of competition between endogenous dopamine and [11C]raclopride binding in in vitro brain slices using a dynamic autoradiography technique
Sasaki, T., Ishiwata, K., Murata, T., & Senda, M. (2002) · Synapse · doi:10.1002/syn.10051 · Cited by 13
“…decreased [11C]raclopride-specific binding in patients with schizophrenia and healthy volunteers and the reduction was greater in the patients (Breier et al., 1997); amphetamine decreased [11C]raclopride-specific binding in rhesus monkey with an increase of DA concentration, as determined by…”
Influential
Neural models of schizophrenia
Heckers, S. (2000) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2000.2.3/sheckers · Cited by 16
“Two groups have independently reported that the intrasynaptic content of dopamine after treatment with amphetamine is increased in schizophrenia.(146-148) Thus, not a tonic increase of dopamine release but an increased phasic release of dopamine could be involved in the pathophysiology of schizophrenia.”
Background
Dopaminhypothese der Schizophrenien Neue Befunde für eine alte Theorie
Heinz, A. (2000) · Der Nervenarzt · doi:10.1007/s001150050008 · Cited by 16
The Enduring Centrality of Dopamine in the Pathophysiology of Schizophrenia
Bonoldi, I., & Howes, O. D. (2013) · Advances in pharmacology · doi:10.1016/b978-0-12-411512-5.00010-5 · Cited by 19
Chapter IX Human forebrain dopamine systems: Characterization of the normal brain and in relation to psychiatric disorders
Hurd, Y. L., & Hall, H. (2005) · Handbook of chemical neuroanatomy · doi:10.1016/s0924-8196(05)80013-2 · Cited by 14
A consideration of the dopamine D2 receptor monomer-dimer equilibrium and the anomalous binding properties of the dopamine D2 receptor ligand, N-methyl spiperone
Logan, J., Fowler, J., Dewey, S., Volkow, N., & Gatley, S. (2001) · Journal of neural transmission · doi:10.1007/s007020170073 · Cited by 16
Brain dopamine responses to ultra-processed milkshakes are highly variable and not significantly related to adiposity in humans
Darcey, V. L., Guo, J., Chi, M., Chung, S. T., Courville, A. B., Gallagher, I., Herscovitch, P., Joseph, P. V., Howard, R., LaNoire, M., et al. (2025) · Cell Metabolism · doi:10.1016/j.cmet.2025.02.002 · Cited by 22
Clinical correlation but no elevation of striatal dopamine synthesis capacity in two independent cohorts of medication-free individuals with schizophrenia
Eisenberg, D. P., Kohn, P. D., Hegarty, C. E., Smith, N. R., Grogans, S. E., Czarapata, J. B., Gregory, M. D., Apud, J. A., & Berman, K. F. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01337-1 · Cited by 17
Psychotic like experiences as part of a continuum of psychosis: Associations with effort-based decision-making and reward responsivity
Ermel, J. A., Moran, E. K., Culbreth, A. J., & Barch, D. M. (2018) · Schizophrenia Research · doi:10.1016/j.schres.2018.10.026 · Cited by 18
“There is also evidence that people with schizophrenia have increased activity in their dopaminergic pathways when not on medications, including enhanced presynaptic dopamine availability and greater release of dopamine when given amphetamine (Breier et al., 1997; Fusar-Poli and Meyer-Lindenberg, 2013a, 2013b; Howes et…”
Background
Chronic hyperdopaminergic activity of schizophrenia is associated with increased ΔFosB levels and cdk-5 signaling in the nucleus accumbens
Cantrup, R., Sathanantham, K., Rushlow, W. J., & Rajakumar, N. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.07.027 · Cited by 18
Truncation of human dopamine transporter by protease calpain
Franekova, V., Baliova, M., & Jurský, F. (2008) · Neurochemistry International · doi:10.1016/j.neuint.2008.04.001 · Cited by 14
“Most recent studies are therefore focused on the potential roles of dopamine transporter in CNS disorders, including Parkinson disease, drug abuse, Tourette’s syndrome, schizophrenia and attention deficit hyperactivity disorder (ADHD) (Crocker et al., 2003; Trifiletti and Bandele, 2000; Breier et al., 1997; Winterer a…”
Are there lessons to be learned from drug development that will accelerate the use of molecular imaging probes in the clinic?
Eckelman, W., Rohatagi, S., Krohn, K., & Vera, D. (2005) · Nuclear Medicine and Biology · doi:10.1016/j.nucmedbio.2005.06.004 · Cited by 15
Self-citation
Ligand-receptor interactions as studied by PET: implications for drug development.
Hietala, J. (1999) · Annals medicus · doi:10.3109/07853899908998802 · Cited by 15
Addressing brain metabolic connectivity in treatment-resistant schizophrenia: a novel graph theory-driven application of 18F-FDG-PET with antipsychotic dose correction
Simone, G. D., Iasevoli, F., Barone, A., Gaudieri, V., Cuocolo, A., Ciccarelli, M., Pappatà, S., & de Bartolomeis, A. (2024) · Schizophrenia · doi:10.1038/s41537-024-00535-4 · Cited by 12
Endogenous dopamine release in the human brain as a pharmacodynamic biomarker: evaluation of the new GPR139 agonist TAK-041 with [11C]PHNO PET
Rabiner, E., Uz, T., Mansur, A., Brown, T. F., Chen, G., Wu, J., Atienza, J., Schwarz, A., Yin, W., Lewis, Y., et al. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-021-01204-1 · Cited by 14
GRK3 deficiency elicits brain immune activation and psychosis
Sellgren, C., Imbeault, S., Larsson, M., Oliveros, A., Nilsson, I. A. K., Codeluppi, S., Orhan, F., Bhat, M., Tufvesson-Alm, M., Gracias, J., et al. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01106-0 · Cited by 14
Comparison of electroencephalogram (EEG) response to MDPV versus the hallucinogenic drugs MK‐801 and ketamine in rats
Shokry, I., Sinha, V., da Silva, G. J., Park, S.-B., Callanan, J., & Tao, R. (2019) · Experimental Neurology · doi:10.1016/j.expneurol.2018.12.001 · Cited by 14
“, striatum and NAcc) and hypodopamine in the cortex of schizophrenia patients (Breier et al., 1997; Abi-Dargham et al., 1998; Thompson et al., 2013).”
Sex and Laterality Differences in Parkinsonian Impairment and Transcranial Ultrasound in Never-Treated Schizophrenics and Their First Degree Relatives in an Andean population
Kamis, D., Stratton, L., Calvó, M., Padilla, E. G., Florenzano, N., Guerrero, G., Rangeon, B. M., Molina, J. L., & de Erausquin, G. D. (2015) · Schizophrenia Research · doi:10.1016/j.schres.2015.01.035 · Cited by 14
“…showing that impairment in executive function and working memory correlates with lower dopamine availability in the prefrontal cortex (Egan et al., 2001), whereas the acute psychotic symptoms correlate with excessive release of endogenous dopamine in the basal ganglia (Breier et al., 1997).”
Background
unc5c haploinsufficient phenotype: striking similarities with the dcc haploinsufficiency model
Auger, M. L., Schmidt, E. R. E., Manitt, C., Dal-Bo, G., Pasterkamp, R., & Flores, C. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12270 · Cited by 14
“…observed in putative developmental animal models of schizophrenia (Tseng et al., 2009; Boksa, 2010), in the disease itself (Lieberman et al., 1987; Breier et al., 1997; Akil et al., 1999; MeyerLindenberg et al., 2002; Abi-Dargham et al., 2009; Howes et al., 2012), or following repeated exposure…”
Background
Dual-isotope SPECT imaging of striatal dopamine: a comparative study between never-treated and haloperidol-treated first-episode schizophrenic patients
Schmitt, G., Dresel, S., Frodl, T., la Fougére, C., Boerner, R., Hahn, K., Möller, H., & Meisenzahl, E. (2012) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-011-0269-4 · Cited by 14
“This result confirms findings of earlier studies that used dopamine stimulation protocols to obtain baseline radioligand binding data from mostly mixed samples of drug-naı̈ve and neuroleptic-free, acute and chronic schizophrenic patients and also found no significant differences in baseline D2 receptor availability [1…”
Environment makes amphetamine‐induced dopamine release in the nucleus accumbens totally impulse‐dependent
Ventura, R., & Puglisi-Allegra, S. (2005) · Synapse · doi:10.1002/syn.20197 · Cited by 14
“…at subsequent exposures, has been postulated to have a major role in the development of dopaminergic abnormalities associated with different pathologies including schizophrenia and drug abuse (Berridge and Robinson, 2003; Breier et al., 1997; Kalivas and Stewart, 1991; Laruelle, 2000; Wise, 2002).”
Background
Gene therapy for Parkinson’s disease using recombinant adeno-associated viral vectors
Muramatsu, S., Tsukada, H., Nakano, I., & Ozawa, K. (2005) · Expert Opinion on Biological Therapy · doi:10.1517/14712598.5.5.663 · Cited by 13
“A 1% change in striatal [11C]raclopride binding corresponds to at least an 8% change in synaptic DA levels [99].”
Background
Effects of Atypical Antipsychotic Drug Treatment on Amphetamine-Induced Striatal Dopamine Release in Patients with Psychotic Disorders
Breier, A., Su, T.-P., Malhotra, A., Elman, I., Adler, C., Weisenfeld, N., & Pickar, D. (1999) · Neuropsychopharmacology · doi:10.1016/s0893-133x(98)00126-2 · Cited by 14
“Our brain imaging method, which has been previously validated (Breier et al. 1997; Carson et al. 1997; Endres et al. 1997), involves determining changes in the specific binding of the D-2/D-3 PET ligand 11 C-raclopride following administration of amphetamine (0.”
BackgroundMethodInfluentialSelf-citation
The role of the D3 dopamine receptor and its partial agonist cariprazine in patients with schizophrenia and substance use disorder
Grunze, H. (2023) · Expert Opinion on Pharmacotherapy · doi:10.1080/14656566.2023.2266359 · Cited by 13
“On the contrary, if dopamine concentration in the synapse is high in the process of neurotransmission (i.e. while consuming drugs), that D2 binding of antipsychotics binding of D2 is low, as the mass effect of dopamine overcomes its lower affinity [62–64].”
Background
DNA Origami-Templated Bimetallic Nanostar Assemblies for Ultra-Sensitive Detection of Dopamine
Kaur, V., Sharma, M., & Sen, T. (2021) · Frontiers in Chemistry · doi:10.3389/fchem.2021.772267 · Cited by 13
“, 2019), schizophrenia (Breier et al., 1997), and Huntington’s disease (Chen et al.”
Background
Behavioural sensitization to alcohol: Bridging the gap between preclinical research and human models
Nona, C. N., Hendershot, C. S., & Lê, A. D. (2018) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2018.08.003 · Cited by 20
Imaging DA release in a rat model of L-DOPA-induced dyskinesias: A longitudinal in vivo PET investigation of the antidyskinetic effect of MDMA
Lettfuss, N. Y., Fischer, K., Sossi, V., Pichler, B., & von Ameln-Mayerhofer, A. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.06.051 · Cited by 13
Assessing Dopaminergic Neurotransmission with PET: Basic Theory and Applications in Alcohol Research
Yoder, K., Kareken, D., & Morris, E. (2011) · Current Medical Imaging Formerly Current Medical Imaging Reviews · doi:10.2174/157340511795445694 · Cited by 13
Striatal dopaminergic responses observed in latent inhibition are dependent on the hippocampal ventral subicular region
Peterschmitt, Y., Hoeltzel, A., & Louilot, A. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04366.x · Cited by 13
Multi-locus association study of schizophrenia susceptibility genes with a posterior probability method
Sun, X.-Q., Jia, Y.-B., Zhang, X.-G., Xu, Q., Shen, Y., & Li, Y.-D. (2005) · Science in China Series C Life Sciences · doi:10.1007/bf03183620 · Cited by 13
“with worsening of positive psychotic symptoms in schizophrenic subjects [ 2 ] . Based on this hypothesis,”
Background
Dopamine, the prefrontal cortex and a genetic mechanism of schizophrenia
Weinberger, D. R. (2003) · CRC Press eBooks · doi:10.3109/9780203427347-8 · Cited by 11
Self-citation
Neuroimaging and Drug Development: An Algorithm for Decision Making
Kapur, S. (2001) · Journal of clinical pharmacology · doi:10.1177/0091270001417010 · Cited by 13
Brain Imaging in Behavioral Neuroscience
Carter, C., & Dalley, J. (2012) · Current topics in behavioral neurosciences · doi:10.1007/978-3-642-28711-4 · Cited by 13
“These decreases in [(11)C]raclopride binding are proportional to the DA increases (Breier et al. 1997).”
Background
Behavioral Sensitization to Addictive Drugs: Clinical Relevance and Methodological Aspects
Phillips, T. J., Pastor, R., Scibelli, A. C., Reed, C. L., & Tarragón, E. (2010) · Neuromethods · doi:10.1007/978-1-60761-883-6_11 · Cited by 12
Understanding the Placebo Effect: Contributions from Neuroimaging
Lidstone, S. C., & Stoessl, A. J. (2007) · Molecular Imaging and Biology · doi:10.1007/s11307-007-0086-3 · Cited by 75
Elevated synaptic PKA activity and abnormal striatal dopamine signaling in Akap11 mutant mice, a genetic model of schizophrenia and bipolar disorder
Song, B. J., Ge, Y., Nicolella, A. A., Kwon, M. J., Lodder, B., Bonanno, K., Valle-Tojeiro, A., Hartley, N. D., Mandell, K. P., Adeleye, J., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-66504-2 · Cited by 18
Measuring amphetamine‐induced dopamine release in humans: A comparative meta‐analysis of [11C]‐raclopride and [11C]‐(+)‐PHNO studies
Caravaggio, F., Porco, N., Kim, J., Torres‐Carmona, E., Brown, E. E., Iwata, Y., Nakajima, S., Gerretsen, P., Remington, G. J., & Graff‐Guerrero, A. (2021) · Synapse · doi:10.1002/syn.22195 · Cited by 12
“…2012, 2015; Wai et al., 2019; Wang et al., 2012), (b) 9 studies did not delineate all the major subregions of the striatum (Bertolino et al., 2000; Breier et al., 1997, 1998; Busto et al., 2009; Cárdenas et al., 2004; Denys et al., 2013; Piccini et al., 1999, 2003; Singer et al., 2002), (c) 2…”
No association between polymorphisms in the promoter region of dopamine receptor D2 gene and schizophrenia in the northern Chinese Han population: A case–control study
Zhang, X., Ding, M., Adnan, A., Liu, Y., Liu, Y.-P., Xing, J., Xuan, J., Xia, X., Yao, J., & Wang, B.-J. (2019) · Brain and Behavior · doi:10.1002/brb3.1193 · Cited by 12
“Previous studies which includes the autopsy results of patients with schizophrenia (Camps, Cortes, Gueye, Probst, & Palacios, 1989; Hess, Bracha, Kleinman, & Creese, 1987), findings from PET studies (Breier et al., 1997; Laruelle et al., 1996, 1997), and phar‐ macological evidence (Seeman, 2002; Worrel, Marken, Beckma…”
Nardostachys jatamansi Targets BDNF-TrkB to Alleviate Ketamine-Induced Schizophrenia-Like Symptoms in Rats
Janardhanan, A., Sadanand, A., & Vanisree, A. J. (2017) · Neuropsychobiology · doi:10.1159/000454985 · Cited by 12
Retracted

Authors: Breier, A., Su, T.-P., Saunders, R., Carson, R. E., Kolachana, B. S., de Bartolomeis, A., Weinberger, D. R., Weisenfeld, N., Malhotra, A. K., Eckelman, W. C., & Pickar, D.
Affiliations: National Institutes of Health (US)
ORCID: Su, T.-P.
Saunders, R.
Carson, R. E.
Kolachana, B. S.
de Bartolomeis, A.
Weinberger, D. R.
Malhotra, A. K.
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 1997-03-18
Volume: 94
Issue: 6
Pages: 2569-2574
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.94.6.2569
PMC: PMC20129
OpenAlex: W2150760506
Cited by: 1,154
References: 43
Citations by year: 2026: 8 · 2025: 12 · 2024: 19 · 2023: 9 · 2022: 17 · 2021: 22 · 2020: 20 · 2019: 26 · 2018: 29 · 2017: 27 · 2016: 34 · 2015: 35 · 2014: 44 · 2013: 51 · 2012: 54
FWCI: 36.57
Type: journal article
Language: en
Open access: green
europepmc.org
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Health Sciences › Medicine › Clinical Neurology › Parkinson's Disease Mechanisms and Treatments
Keywords: schizophrenia, synaptic dopamine, amphetamine, [11C]raclopride, striatum, dopamine release, microdialysis, non-human primates
MeSH terms: Amphetamine, Animals, Carbon Radioisotopes, Corpus Striatum, Dopamine, Humans, Macaca mulatta, Reference Values, Regression Analysis, Salicylamides, Schizophrenia, Synapses, Tomography, Emission-Computed, Microdialysis, Raclopride

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Schizophrenia is associated with elevated amphetamine-induced synaptic dopamine concentrations: Evidence from a novel positron emission tomography method

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