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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Erritzøe, D., Talbot, P. S., Frankle, W. G., & Abi‐Dargham, A. (2003) · Neuroimaging Clinics of North America · doi:10.1016/s1052-5149(03)00089-3 · Cited by 31
CURRENT PERSPECTIVES ON THE PATHOPHYSIOLOGY OF SCHIZOPHRENIA, DEPRESSION, AND ANXIETY DISORDERS
Krystal, J. H., D’Souza, D. C., Sanacora, G., Goddard, A. W., & Charney, D. S. (2001) · Medical Clinics of North America · doi:10.1016/s0025-7125(05)70329-1 · Cited by 36
Test–retest reliability of 11C-ORM-13070 in PET imaging of α2C-adrenoceptors in vivo in the human brain
Lehto, J., Virta, J., Oikonen, V., Roivainen, A., Luoto, P., Arponen, E., Helin, S., Hietamäki, J., Holopainen, A., Kailajärvi, M., et al. (2014) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-014-2899-z · Cited by 26
“Whether [ C]-ORM13070 could be used to indirectly reflect changes in endogenous synaptic noradrenaline concentrations induced by various pharmacological or other challenges could also be explored, in a manner analogous to the use of [C]-raclopride PET to investigate dopamine release in the human brain [25–27].”
Result
Neurochemical dysfunction in treated and nontreated schizophrenia – a retrospective analysis of in vivo imaging studies
Nikolaus, S., Hautzel, H., & Müller, H. (2014) · Reviews in the Neurosciences · doi:10.1515/revneuro-2013-0063 · Cited by 26
Dopamine Dynamics and Neurobiology of Non-Response to Antipsychotics, Relevance for Treatment Resistant Schizophrenia: A Systematic Review and Critical Appraisal
Iasevoli, F., Avagliano, C., D’Ambrosio, L., Barone, A., Ciccarelli, M., Simone, G. D., Mazza, B., Vellucci, L., & de Bartolomeis, A. (2023) · Biomedicines · doi:10.3390/biomedicines11030895 · Cited by 22
Aberrant large-scale brain modules in deficit and non-deficit schizophrenia
Fan, L., Yu, M., Pinkham, A. E., Zhu, Y., Tang, X., Wang, X., Zhang, X., Ma, J., Zhang, J., Zhang, X., et al. (2021) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2021.110461 · Cited by 25
Neuronal traffic signals in tardive dyskinesia: not enough “stop” in the motor striatum
Stahl, S. M. (2017) · CNS Spectrums · doi:10.1017/s109285291700061x · Cited by 30
“What’s Wrong with Dopamine and Its Receptors in Schizophrenia? Before considering what are the effects of acute and chronic D2 receptor blockade, we need to answer the question: what is the cause of dopamine hyperactivity in untreated schizophrenia—too many supersensitive dopamine receptors or too much dopamine releas…”
Background
Maternal nicotine exposure during lactation alters food preference, anxiety-like behavior and the brain dopaminergic reward system in the adult rat offspring
Pinheiro, C. R., de Moura, E. G., Manhães, A. C., Fraga, M. C., Claudio-Neto, S., Younes-Rapozo, V., Santos-Silva, A. P., Denucci, B. L., Oliveira, E., & Lisboa, P. C. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2015.05.040 · Cited by 30
Adaptive evolution and elucidating the potential inhibitor against schizophrenia to target DAOA (G72) isoforms
Sehgal, S. A., Mannan, S., Kanwal, S., Naveed, I., & Mir, A. (2015) · Drug Design, Development and Therapy · doi:10.2147/dddt.s63946 · Cited by 25
Proton magnetic resonance spectroscopy of the substantia nigra in schizophrenia
Reid, M. A., Kraguljac, N. V., Avsar, K. B., White, D. M., den Hollander, J. A., & Lahti, A. C. (2013) · Schizophrenia Research · doi:10.1016/j.schres.2013.04.036 · Cited by 22
“These disruptions include increased amphetamineinduced dopamine release (Abi-Dargham et al., 1998; Breier et al., 1997; Laruelle et al., 1996) and elevated 18F- and 11C-DOPA, a precursor of dopamine, accumulation in the striatum (Dao-Castellana et al., 1997; Hietala et al., 1995; Lindstrom et al.,…”
Background
Alterations in prefrontal glutamatergic and noradrenergic systems following MK-801 administration in rats prenatally exposed to methylazoxymethanol at gestational day 17
Léna, I., Chessel, A., Pen, G. L., Krebs, M., & Garcia, R. (2007) · Psychopharmacology · doi:10.1007/s00213-007-0719-x · Cited by 23
“(2004) have demonstrated that acute systemic injection of amphetamine induced an exaggerated increase of dopamine (DA) release in the nucleus accumbens (NAcc) of MAM-exposed rats in line with the striatal dopaminergic hyper-reactivity observed in schizophrenic patients (Laruelle et al. 1996; Breier et al. 1997; Abi-Da…”
Influential
Differential involvement of dopamine in the anterior and posterior parts of the dorsal striatum in latent inhibition
Jeanblanc, J., Hoeltzel, A., & Louilot, A. (2003) · Neuroscience · doi:10.1016/s0306-4522(02)00823-0 · Cited by 25
“Recently, it has been shown that striatal DA release induced by d-amphetamine is increased in patients with schizophrenia (Laruelle et al., 1996; Breier et al., 1997).”
Background
Parkinson's disease: imaging update
de la Fuente-Fernández, R., & Stoessl, A. (2002) · Current Opinion in Neurology · doi:10.1097/00019052-200208000-00012 · Cited by 25
Influence of the entorhinal cortex on accumbal and striatal dopaminergic responses in a latent inhibition paradigm
Jeanblanc, J., Peterschmitt, Y., Hoeltzel, A., & Louilot, A. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.06.022 · Cited by 29
Positron Emission Tomography Study of the Effects of Tryptophan Depletion on Brain Serotonin2Receptors in Subjects Recently Remitted From Major Depression
Yatham, L. N., Liddle, P. F., Sossi, V., Erez, J., Vafai, N., Lam, R. W., & Blinder, S. (2012) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2011.1493 · Cited by 25
“Fourth, the binding of some PET ligands to receptors is affected by changes in the levels of endogenous neurotransmitter.(35,36) Therefore, one could argue that changes in brain serotonin levels during the tryptophan depletion session might have accounted for the reduction in serotonin2 binding observed in the present…”
Sustained striatal dopamine levels following intestinal levodopa infusions in Parkinson's disease patients
Politis, M., Sauerbier, A., Loane, C., Pavese, N., Martin, A., Corcoran, B., Brooks, D. J., Ray-Chaudhuri, K., & Piccini, P. (2017) · Movement Disorders · doi:10.1002/mds.26848 · Cited by 24
PET translates neurophysiology into images: A review to stimulate a network between neuroimaging and basic research
Giovacchini, G., Squitieri, F., Esmaeilzadeh, M., Milano, A., Mansi, L., & Ciarmiello, A. (2010) · Journal of Cellular Physiology · doi:10.1002/jcp.22451 · Cited by 22
“Studies in humans showed that amphetamine challenge induced a greater decrease in 11Craclopride or 123IBZM binding potential in schizophrenic patients compared to healthy controls (Laruelle et al., 1996; Breier et al., 1997).”
Background
Postnatal functional inactivation of the entorhinal cortex or ventral subiculum has different consequences for latent inhibition‐related striatal dopaminergic responses in adult rats
Meyer, F., Peterschmitt, Y., & Louilot, A. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06755.x · Cited by 24
“…dopaminergic dysfunctioning in this disease is supported by several cerebral imaging studies (Hietala et al., 1995, 1999; Laruelle et al., 1996; Breier et al., 1997; Dao-Castellana et al., 1997; Abi-Dargham et al., 1998; Lindström et al., 1999) and may be consecutive to a cortico-subcortical…”
Enhanced locomotor activity in rats with excitotoxic lesions of the entorhinal cortex, a neurodevelopmental animal model of schizophrenia: Behavioral and in vivo microdialysis studies
Sumiyoshi, T., Tsunoda, M., Uehara, T., Tanaka, K., Itoh, H., Sumiyoshi, C., & Kurachi, M. (2004) · Neuroscience Letters · doi:10.1016/j.neulet.2004.04.027 · Cited by 20
Redox Dysregulation in Schizophrenia: Genetic Susceptibility and Pathophysiological Mechanisms
Do, K. Q., Bovet, P., Cabungcal, J.-H., Conus, P., Gysin, R., Lavoie, S., Steullet, P., & Cuénod, M. (2009) · Springer eBooks · doi:10.1007/978-0-387-30410-6_8 · Cited by 22
From "bedside" to "bench" and back: A translational approach to studying dopamine dysfunction in schizophrenia.
Abi-Dargham, A. (2020) · Neuroscience and Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.12.003 · Cited by 23
Molecular imaging as a guide for the treatment of central nervous system disorders
Kim, E., Howes, O. D., & Kapur, S. (2013) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2013.15.3/ekim · Cited by 22
Patients with schizophrenia show increased aversion to angry faces in an associative learning task
Evans, S., Shergill, S., Chouhan, V., Bristow, E., Collier, T., & Averbeck, B. (2010) · Psychological Medicine · doi:10.1017/s0033291710001960 · Cited by 23
“Although excessive striatal dopamine has been implicated consistently in schizophrenia (Laruelle et al. 1996 ; Breier et al. 1997 ; Abi-Dargham et al. 1998 ; Bortolozzi et al. 2007) and modelling and experimental work has suggested that striatal dopamine levels are related to differences in…”
Background
Ventral and dorsal striatal dopamine efflux and behavior in rats with simple vs. co-morbid histories of cocaine sensitization and neonatal ventral hippocampal lesions
Chambers, R. A., Sentir, A. M., & Engleman, E. A. (2010) · Psychopharmacology · doi:10.1007/s00213-010-1929-1 · Cited by 24
Cerebrospinal fluid kynurenic acid in male patients with schizophrenia – correlation with monoamine metabolites
Nilsson-Todd, L. K., Nordin, C., Jönsson, E. G., Skogh, E., & Erhardt, S. (2007) · Acta Neuropsychiatrica · doi:10.1111/j.1601-5215.2006.00170.x · Cited by 21
Effects of birth insult and stress at adulthood on excitatory amino acid receptors in adult rat brain
El-Khodor, B., Flores, G., Srivastava, L. K., & Boksa, P. (2004) · Synapse · doi:10.1002/syn.20073 · Cited by 23
Regulation of central dopamine-2 receptor sensitivity by a proportional control thermostat in humans.
Schwartz, P., & Erk, S. (2004) · Psychiatry Research · doi:10.1016/j.psychres.2004.03.004 · Cited by 23
Impact of neuroinflammation on brain glutamate and dopamine signalling in schizophrenia: an update
Nayak, U. Y., Manikkath, J., Arora, D. S., & Mudgal, J. (2025) · Metabolic Brain Disease · doi:10.1007/s11011-025-01548-3 · Cited by 29
“An in vivo study using four rhesus monkeys has shown enhanced striatal extra-synaptic dopamine levels in schizophrenic condition using photon emission tomography studies (Breier et al. 1997).”
Recent Advances in Photo-mediated-Radiofluorination.
Bui, T., & Kim, H.-K. (2021) · Chemistry - An Asian Journal · doi:10.1002/asia.202100399 · Cited by 22
120th Anniversary of the Kraepelinian Dichotomy of Psychiatric Disorders
Rybakowski, J. (2019) · Current Psychiatry Reports · doi:10.1007/s11920-019-1048-6 · Cited by 22
Enhanced Dopamine in Prodromal Schizophrenia (EDiPS): a new animal model of relevance to schizophrenia
Petty, A., Cui, X.-Y., Tesiram, Y., Kirik, D., Howes, O., & Eyles, D. (2019) · npj Schizophrenia · doi:10.1038/s41537-019-0074-z · Cited by 22
“There is evidence that patients with schizophrenia show increased baseline levels of DA(33) as well as an enhanced response to low doses of AMPH.(1,34,35) EDiPS animals replicate this with increased DA release in response to a low AMPH dose.”
BackgroundInfluential
A review of positron emission tomography studies exploring the dopaminergic system in substance use with a focus on tobacco as a co-variate
Thiruchselvam, T., Malik, S., & Foll, B. L. (2016) · The American Journal of Drug and Alcohol Abuse · doi:10.1080/00952990.2016.1257633 · Cited by 19
“This conceptualization has acquired support through micro-dialysis studies in animals (5,6).”
Background
Catechol-O-methyltransferase (COMT) genotype biases neural correlates of empathy and perceived personal distress in schizophrenia
Poletti, S., Radaelli, D., Cavallaro, R., Bosia, M., Lorenzi, C., Pirovano, A., Smeraldi, E., & Benedetti, F. (2012) · Comprehensive Psychiatry · doi:10.1016/j.comppsych.2012.06.008 · Cited by 20
“Patients with schizophrenia showed enhanced dopamine (DA) release both in basal condition and in response to DA stimulating challenges [20,21].”
Background
Dexamphetamine-induced reduction of P3a and P3b in healthy participants
Albrecht, M. A., Martin-Iverson, M. T., Price, G. W., Lee, J., & Iyyalol, R. (2010) · Journal of Psychopharmacology · doi:10.1177/0269881110376686 · Cited by 23
“People with schizophrenia demonstrate a greater increase in the release of dopamine after amphetamine than controls (Abi-Dargham et al., 1998; Breier et al., 1997).”
Background
Enhanced cortical dopamine output and antipsychotic-like effect of raclopride with adjunctive low-dose L-dopa.
Eltayb, A., Wadenberg, M.-L. G., & Svensson, T. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.03.038 · Cited by 22
Preclinical effects of conventional and atypical antipsychotic drugs: defining the mechanisms of action
Svensson, T. H. (2003) · Clinical Neuroscience Research · doi:10.1016/s1566-2772(03)00017-3 · Cited by 20
Does dopamine sensitization underlie the association between schizophrenia and drug abuse?
Tsapakis, E., Guillin, O., & Murray, R. (2003) · Current Opinion in Psychiatry · doi:10.1097/00001504-200304002-00008 · Cited by 22
Schizophrenia, the prefrontal cortex, and a mechanism of genetic susceptibility
Weinberger, D. (2002) · European psychiatry · doi:10.1016/s0924-9338(03)00080-4 · Cited by 22
Self-citation
Muscarinic mechanisms in psychotic disorders.
McKinzie, D., & Bymaster, F. (2012) · Handbook of Experimental Pharmacology · doi:10.1007/978-3-642-25758-2_9 · Cited by 22
Imaging the nigrostriatal system to monitor disease progression and treatment-induced complications.
Kuriakose, R., & Stoessl, A. (2010) · Progress in Brain Research · doi:10.1016/s0079-6123(10)84009-9 · Cited by 22
Schizotypy trait and striatal dopamine receptors in healthy volunteers
Chen, K. C., Lee, I. H., Yeh, T. L., Chiu, N. T., Chen, P. S., Yang, Y. K., Lu, R.-B., & Chen, C. C. (2012) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2011.07.003 · Cited by 21
“Positive symptoms, which may be induced by the increase in synaptic DA concentration in the striatum (Breier et al., 1997; de Haan et al., 2004; Yang et al., 2004; Buchsbaum et al., 2006; Schmitt et al., 2008), play an important part in the diagnosis of schizophrenia.”
Background
MicroRNAs in schizophrenia: implications for synaptic plasticity and dopamine–glutamate interaction at the postsynaptic density. New avenues for antipsychotic treatment under a theranostic perspective
de Bartolomeis, A., Iasevoli, F., Tomasetti, C., & Buonaguro, E. F. (2015) · Molecular Neurobiology · doi:10.1007/s12035-014-8962-8 · Cited by 21
Pharmacoinformatics, Adaptive Evolution, and Elucidation of Six Novel Compounds for Schizophrenia Treatment by Targeting DAOA (G72) Isoforms
Sehgal, S. A. (2017) · BioMed Research International · doi:10.1155/2017/5925714 · Cited by 21
Multimodal predictive modeling of individual treatment outcome in cocaine dependence with combined neuroimaging and behavioral predictors
Luo, S. X., Martínez, D., Carpenter, K. M., Slifstein, M., & Nunes, E. V. (2014) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2014.04.030 · Cited by 22
Sequential Versus Nonsequential Measurement of Density and Affinity of Dopamine D2 Receptors with [11C]raclopride: Effect of Methamphetamine
Doudet, D., & Holden, J. (2003) · Journal of Cerebral Blood Flow and Metabolism · doi:10.1097/01.wcb.0000093325.88757.92 · Cited by 21
“In contrast, combined PET-microdialysis studies by Breier et al. (1997) and Laruelle et al. (1997) showed that during the time frame of imaging studies, the concentrations of extracellular DA peaked shortly (within 15 to 30 minutes) after amphetamine and returned towards baseline levels within a…”
Result

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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