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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Novak, G., & Seeman, P. (2010) · Synapse · doi:10.1002/syn.20786 · Cited by 37
“This type of dopamine release is the hallmark of not only animal models of schizophrenia but also of schizophrenia pathology in humans (Breier et al., 1997, 1998; Laruelle et al., 1996, 1997).”
Background
Nicotine Normalizes Increased Prefrontal Cortical Dopamine D1 Receptor Binding and Decreased Working Memory Performance Produced by Repeated Pretreatment with MK-801: A PET Study in Conscious Monkeys
Tsukada, H., Miyasato, K., Nishiyama, S., Fukumoto, D., Kakiuchi, T., & Domino, E. F. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300745 · Cited by 36
A meta-analysis of the response to chronic l-dopa in patients with schizophrenia: therapeutic and heuristic implications
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“Manipulations that increase or decrease endogenous DA levels, respectively, lower or increase DA antagonist binding to striatal DA receptors in schizophrenia (Breier et al. 1997; Laruelle and Abi-Dargham 1999; Abi-Dargham et al. 2000).”
BackgroundInfluential
Biomarkers for the Development of New Medications for Cocaine Dependence
Bough, K. J., Amur, S., Lao, G., Hemby, S. E., Tannu, N. S., Kampman, K. M., Schmitz, J. M., Martínez, D., Merchant, K., Green, C., et al. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.210 · Cited by 36
“The D2 receptors are imaged before and after the administration of a stimulant, which causes the dopamine neurons to release dopamine (Breier et al, 1997; Laruelle et al, 1997; Volkow et al, 1994).”
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Glutamate and Psychosis Risk
Egerton, A., Fusar-Poli, P., & M. Stone, J. (2012) · Current Pharmaceutical Design · doi:10.2174/138161212799316244 · Cited by 36
“Modern in vivo neuroimaging studies in schizophrenia have now shown elevated synthesis and storage of presynaptic dopamine [41-48], amphetamine-stimulated dopamine release [49-51], and baseline occupancy of D2/3 receptors by dopamine [52, 53] in the striatum, and that around 60% occupancy of striatal D2 receptors is r…”
Background
Treatment resistant schizophrenia and neurological soft signs may converge on the same pathology: Evidence from explanatory analysis on clinical, psychopathological, and cognitive variables
de Bartolomeis, A., Prinzivalli, E., Callovini, G., D'Ambrosio, L., Altavilla, B., Avagliano, C., & Iasevoli, F. (2018) · Progress in Neuro-psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.09.002 · Cited by 36
“considered a crucial alteration in schizophrenia molecular pathophysiology (Breier et al., 1997).”
Differential effects of paroxetine on raphe and cortical 5-HT1A binding: A PET study in monkeys
Giovacchini, G., Lang, L., Ma, Y., Herscovitch, P., Eckelman, W., & Carson, R. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.05.042 · Cited by 36
“On this basis, dynamic changes in dopamine concentration elicited by pharmacological displacement studies have been assessed in control and clinical populations with neuroimaging techniques (Farde et al., 1990; Dewey et al., 1993; Laruelle et al., 1996, 1999; Breier et al., 1997).”
MethodSelf-citation
The use of PET and knockout mice in the drug discovery process.
Eckelman, W. (2003) · Drug Discovery Today · doi:10.1016/s1359-6446(03)02678-3 · Cited by 36
Self-citation
Presynaptic dopamine deficit in minimally conscious state patients following traumatic brain injury
Fridman, E. A., Osborne, J. R., Mozley, P. D., Victor, J. D., & Schiff, N. D. (2019) · Brain · doi:10.1093/brain/awz118 · Cited by 46
The dopaminergic stabiliser ACR16 counteracts the behavioural primitivization induced by the NMDA receptor antagonist MK-801 in mice: implications for cognition
Nilsson, M. K. L., Carlsson, A., Markinhuhta, K. R., Sonesson, C., Pettersson, F., Gullme, M., & Carlsson, M. L. (2004) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2004.05.004 · Cited by 34
“…dopamine release is elevated in drug-naive schizophrenic patients, and that this elevation correlates to the induction of positive psychotic symptoms (Abi-Dargham et al., 1998; Breier et al., 1997; Hietala et al., 1995; Laruelle et al., 1996; Lindström et al., 1999; Reith et al., 1994).”
Background
Applications of SPECT imaging of dopaminergic neurotransmission in neuropsychiatric disorders
Kugaya, A., Fujita, M., & Innis, R. B. (2000) · Annals of Nuclear Medicine · doi:10.1007/bf02990472 · Cited by 35
A sequential view of neurotransmitter release.
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Acute anxiety disorder, major depressive disorder, bipolar disorder and schizophrenia are related to different patterns of nigrostriatal and mesolimbic dopamine dysfunction
Nikolaus, S., Mamlins, E., Hautzel, H., & Müller, H.-W. (2019) · Reviews in the Neurosciences · doi:10.1515/revneuro-2018-0037 · Cited by 35
Elevated endogenous GDNF induces altered dopamine signalling in mice and correlates with clinical severity in schizophrenia
Mätlik, K., Garton, D. R., Montaño-Rodriguez, A., Olfat, S., Eren, F., Casserly, L., Damdimopoulos, A. E., Panhelainen, A. E., Porokuokka, L. L., Kopra, J. J., et al. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01554-2 · Cited by 40
GABA Transporter-1 Deficiency Confers Schizophrenia-Like Behavioral Phenotypes
Yu, Z., Fang, Q., Xiao, X., Wang, Y., Cai, Y.-Q., Cao, H., Hu, G., Chen, Z., Fei, J., Gong, N., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0069883 · Cited by 34
“studies [65,66,67].”
Neurobiology of Addiction
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The amphetamine sensitization model of schizophrenia: relevance beyond psychotic symptoms?
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“…16, Schwerzenbach 8603, Switzerland e-mail: daria.peleg@behav.biol.ethz.ch which postulates that a sensitized dopamine system is intrinsic to the disease and is responsible for the genesis of psychotic symptoms (Abi-Dargham et al. 1998; Breier et al. 1997; Laruelle 2000; Lieberman et al. 1997).”
Background
Synaptic differences in the patch matrix compartments of subjects with schizophrenia: a postmortem ultrastructural study of the striatum.
Roberts, R., Roche, J. K., & Conley, R. (2005) · Neurobiology of Disease · doi:10.1016/j.nbd.2005.03.015 · Cited by 34
“…augmentation of presynaptic dopamine function, indicating an increase in dopamine synthesis capacity and an increase in presynaptic dopamine stores (Abi-Dargham et al., 1998, 2000; Breier et al., 1997; Dao-Castellana et al., 1997; Hietala et al., 1994, 1995, 1999; Laruelle et al., 1996, 1999).”
Background
Symptom provocation studies in psychiatric disorders: scientific value, risks, and future
D’Souza, D. C., Berman, R., Krystal, J. H., & Charney, D. S. (1999) · Biological Psychiatry · doi:10.1016/s0006-3223(99)00209-7 · Cited by 32
The 5-HT 1A Receptor
Banerjee, P., Kanjilal, B., & Mehta, M. (2007) · Frontiers in neuroscience · doi:10.1201/9781420005752.ch7 · Cited by 12
Measuring Neurotransmitter Release with PET: Methodological Issues
Dagher, A., Gunn, R., Lockwood, G., Cunningham, V., Grasby, P., & Brooks, D. (1998) · Elsevier eBooks · doi:10.1016/b978-012161340-2/50069-x · Cited by 34
Could psychedelic drugs have a role in the treatment of schizophrenia? Rationale and strategy for safe implementation
Wolf, G., Singh, S., Blakolmer, K., Lerer, L. B., Lifschytz, T., Heresco‐Levy, U., Lotan, A., & Lerer, B. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01832-z · Cited by 51
“Increases in both psychotic symptoms and in amphetamine-induced synaptic dopamine concentrations were larger among schizophrenia patients compared to controls [130, 131].”
Result
Allosteric Modulators of Metabotropic Glutamate Receptors as Novel Therapeutics for Neuropsychiatric Disease
Luessen, D. J., & Conn, P. J. (2022) · Pharmacological Reviews · doi:10.1124/pharmrev.121.000540 · Cited by 42
“In support of this model, in vivo neuroimaging studies show increased subcortical dopamine release after amphetamine challenge in individuals with schizophrenia (Laruelle et al., 1996; Breier et al., 1997; Abi-Dargham et al., 1998).”
Background
From apathy to addiction: Insights from neurology and psychiatry
Kirschner, M., Rabinowitz, A. G., Singer, N., & Dagher, A. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.109926 · Cited by 37
Regional brain volume changes following chronic antipsychotic administration are mediated by the dopamine D2 receptor
Guma, E., Rocchetti, J., Devenyi, G. A., Tanti, A., Mathieu, A., Lerch, J., Elgbeili, G., Courcot, B., Mechawar, N., Chakravarty, M., et al. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.04.054 · Cited by 33
Increase of striatal dopamine transmission in first episode drug-naive schizophrenic patients as demonstrated by [(123)I]IBZM SPECT.
Schmitt, G., Meisenzahl, E., Frodl, T., la Fougére, C., Hahn, K., Möller, H., & Dresel, S. (2009) · Psychiatry Research · doi:10.1016/j.pscychresns.2008.11.001 · Cited by 33
“Studies using dopamine stimulationprotocols,whichprovide baseline radioligandbindingdata from mostly mixed samples of drug-naïve and antipsychotic-free, acute and chronic schizophrenic patients, found no significant differences in baseline D2 receptor availability (Laruelle et al., 1996; Breier et al., 1997; Abi-Dargh…”
Background
Differential synaptic changes in the striatum of subjects with undifferentiated versus paranoid schizophrenia
Roberts, R. C., Roche, J. K., & Conley, R. R. (2008) · Synapse · doi:10.1002/syn.20534 · Cited by 33
“The caudate and/or putamen in subjects with schizophrenia display abnormal dopamine (DA) function (Breier et al., 1997; Hietala et al., 1994, 1995; Laruelle et al., 1996), diminished metabolic rate (Buchsbaum et al., 1992; DeLisi et al., 1985; Resnick et al., 1988), a correlation between formal…”
Background
The role of dopamine in cognition
Rémy, P., & Samson, Y. (2003) · Current Opinion in Neurology · doi:10.1097/00019052-200312002-00007 · Cited by 34
Normalization of cytochrome-c oxidase activity in the rat brain by neuroleptics after chronic treatment with PCP or methamphetamine.
Prince, J. A., Yassin, M. S., & Oreland, L. (1997) · Neuropharmacology · doi:10.1016/s0028-3908(97)00152-4 · Cited by 33
Amphetamine-Induced Dopamine Release
Carson, R., Channing, M., Vuong, B., Watabe, H., Herscovitch, P., & Eckelman, W. (2001) · Elsevier eBooks · doi:10.1016/b978-012285751-5/50034-x · Cited by 33
Self-citation
Atlas of type 2 dopamine receptors in the human brain: Age and sex dependent variability in a large PET cohort
Malén, T., Karjalainen, T., Isojärvi, J., Vehtari, A., Bürkner, P., Putkinen, V., Kaasinen, V., Hietala, J. A., Nuutila, P., Rinne, J. O., et al. (2022) · NeuroImage · doi:10.1016/j.neuroimage.2022.119149 · Cited by 40
“Patients with schizophrenia show striatal hyperactivity of dopaminergic function (12) and”
Background
Amphetamine Induced Striatal Dopamine Release Measured with an Agonist Radiotracer in Schizophrenia
Frankle, W., Paris, J., Himes, M. L., Mason, N. S., Mathis, C. A., & Narendran, R. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.11.032 · Cited by 32
“Relative to healthy controls, subjects with schizophrenia show significant increases in the displacement of dopamine (DA) D2/3 receptor radiotracers in the striatum in response to psychostimulants during positron emission tomography (PET) or single photon emission computed tomography (SPECT) studies (1-4).”
Background
Consensus paper of the WFSBP Task Force on Biological Markers: Criteria for biomarkers and endophenotypes of schizophrenia part II: Cognition, neuroimaging and genetics
Schmitt, A., Rujescu, D., Gawlik, M., Hasan, A., Hashimoto, K., Iceta, S., Jarema, M., Kambeitz, J. P., Kasper, S. F., Keeser, D., et al. (2016) · The World Journal of Biological Psychiatry · doi:10.1080/15622975.2016.1183043 · Cited by 39
“(B) After a baseline period (pre-injection) to allow for establishment of radioligand–DA equilibrium, amphetamine is injected (denoted with dotted line) and levels of specifically bound radioligand (post-injection) decrease in the striatum (red line) due to displacement by DA, while they remain constant in the cerebel…”
BackgroundResultInfluential
Kappa-Opioid Receptor Signaling in the Striatum as a Potential Modulator of Dopamine Transmission in Cocaine Dependence
Trifilieff, P., & Martínez, D. (2013) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2013.00044 · Cited by 35
“Previous studies in non-human primates have shown that ∆BPND correlates linearly with changes in extracellular dopamine, measured with microdialysis (Breier et al., 1997; Endres et al., 1997; Laruelle et al., 1997).”
Background
Subchronic elevation of brain kynurenic acid augments amphetamine-induced locomotor response in mice
Olsson, S., Larsson, M., & Erhardt, S. (2012) · Journal of neural transmission · doi:10.1007/s00702-011-0706-6 · Cited by 32
“…with the hyper-responsiveness to d-amphetamine observed in brain imaging studies of both patients with schizophrenia (Abi-Dargham et al. 1998; Breier et al. 1997; Laruelle et al. 1996) and healthy volunteers following the pretreatment with NMDA receptor antagonists (Breier et al. 1998;…”
BackgroundResultInfluential
Season of birth in schizophrenia: a maternal-fetal chronobiological hypothesis.
Schwartz, P. (2011) · Medical Hypotheses · doi:10.1016/j.mehy.2011.02.019 · Cited by 32
Socially isolated rats exhibit changes in dopamine homeostasis pertinent to schizophrenia
Fabricius, K., Steiniger‐Brach, B., Helboe, L., Fink‐Jensen, A., & Wörtwein, G. (2010) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2010.09.003 · Cited by 31
“, 2004) and following amphetamine administration (Breier et al., 1997; Laruelle et al., 1996).”
BackgroundResultInfluential
The genetics of schizophrenia
Bertolino, A., & Blasi, G. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.04.038 · Cited by 63
Amphetamine‐induced dopamine release: Duration of action as assessed with the D2/3 receptor agonist radiotracer (––)‐N‐[11C]propyl‐norapomorphine ([11C]NPA) in an anesthetized nonhuman primate
Narendran, R., Slifstein, M., Hwang, D., Hwang, Y., Scher, E., Reeder, S. A., Martinez, D., & Laruelle, M. (2007) · Synapse · doi:10.1002/syn.20346 · Cited by 32
“While nonhuman primate studies have demonstrated a linear relationship between DA concentration and the percent decrease in radiotracer binding potential (BP) (Breier et al., 1997; Laruelle et al., 1997), several factors remain unexplained by the classical occupancy model (for detailed review see Laruelle, 2000).”
Electrical stimulation of the hippocampus disrupts prepulse inhibition in rats: frequency- and site-dependent effects
Howland, J. G., MacKenzie, E. M., Yim, T. T.-L., Taepavarapruk, P., & Phillips, A. G. (2003) · Behavioural Brain Research · doi:10.1016/j.bbr.2003.10.001 · Cited by 33
“A large body of research suggests that schizophrenic patients show abnormalities in cortico-limbic-striatal circuitry, in areas such as the frontal cortex, nucleus accumbens (NAc), and hippocampus [8,28,46,75] likely involving alterations in dopamine (DA) and glutamate (Glu) transmission [11,16,25,39,44].”
Background
Studies on dopaminergic and GABAergic markers in striatum reveals a decrease in the dopamine transporter in schizophrenia.
Dean, B., & Hussain, T. (2001) · Schizophrenia Research · doi:10.1016/s0920-9964(00)00096-7 · Cited by 32
Absolute Quantification by Positron Emission Tomography of the Endogenous Ligand
Delforge, J., Bottlaender, M., Pappatá, S., Loc'h, C., & Syrota, A. (2001) · Journal of Cerebral Blood Flow and Metabolism · doi:10.1097/00004647-200105000-00016 · Cited by 32
“For example, several studies reported that the binding of [ 11 C]raclopride decreases significantly after an amphetamine-induced dopamine elevation (Breier et al., 1997; Carson et al., 1997) and increases after a reserpine-induced dopamine depletion (Ginovart et al., 1997).”
Background
Schizophrenia: elevated mRNA for calcium-calmodulin-dependent protein kinase IIbeta in frontal cortex.
Novak, G., Seeman, P., & Tallerico, T. (2000) · Brain Research. Molecular Brain Research · doi:10.1016/s0169-328x(00)00188-1 · Cited by 32
Imaging of Seasonal Affective Disorder and Seasonality Effects on Serotonin and Dopamine Function in the Human Brain
Praschak-Rieder, N., & Willeit, M. (2011) · Current topics in behavioral neurosciences · doi:10.1007/7854_2011_174 · Cited by 36
Developmental markers of psychiatric disorders as identified by sensorimotor gating
Powell, S. B., & Geyer, M. A. (2002) · Neurotoxicity Research · doi:10.1080/10298420290030578 · Cited by 40
Self-Entropic Broadening Theory: Toward a New Understanding of Self and Behavior Change Informed by Psychedelics and Psychosis
Dourron, H. M., Strauss, C. K., & Hendricks, P. S. (2022) · Pharmacological Reviews · doi:10.1124/pharmrev.121.000514 · Cited by 35
“If the dopamine hypothesis of schizophrenia originates primarily out of the efficacy of D2 antagonism (Seeman, 2021) and the hypersensitivity of people with schizophrenia to dopaminergic drugs (Lieberman et al., 1987; Breier et al., 1997; Seeman, 2011, 2021; Weidenauer et al., 2016), we cannot use the same logic to pu…”
Background
Dopamine Receptor Activation Reorganizes Neuronal Ensembles during Hippocampal Sharp Waves In Vitro
Miyawaki, T., Norimoto, H., Ishikawa, T., Watanabe, Y., Matsuki, N., & Ikegaya, Y. (2014) · PLoS ONE · doi:10.1371/journal.pone.0104438 · Cited by 32
“increased in patients with schizophrenia [57], and an experimental”
Background
Mice lacking collapsin response mediator protein 1 manifest hyperactivity, impaired learning and memory, and impaired prepulse inhibition
Yamashita, N., Takahashi, A., Takao, K., Yamamoto, T., Kolattukudy, P., Miyakawa, T., & Goshima, Y. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00216 · Cited by 31
“Most rodent models of schizophrenia tend to replicate aspects of the positive symptoms of schizophrenia, such as hyperactivity, probably reflecting enhanced mesolimbic dopamine function (Breier et al., 1997; Laruelle et al., 1999).”
Background

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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