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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BackgroundInfluential
Alcohol dependence is associated with blunted dopamine transmission in the ventral striatum
Martinez, D., Gil, R., Slifstein, M., Hwang, D.-R., Huang, Y., Perez, A., Kegeles, L., Talbot, P., Evans, S., Krystal, J., et al. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.04.044 · Cited by 445
Striatal dopaminergic function in restless legs syndrome
Turjanski, N., Lees, A., & Brooks, D. (1999) · Neurology · doi:10.1212/wnl.52.5.932 · Cited by 445
Noise Reduction in the Simplified Reference Tissue Model for Neuroreceptor Functional Imaging
Wu, Y., & Carson, R. (2002) · Journal of Cerebral Blood Flow and Metabolism · doi:10.1097/01.wcb.0000033967.83623.34 · Cited by 440
“The [(11)C]raclopride input function was determined from human data derived from bolus/infusion (B/I) administration (Breier et al., 1997).”
MethodInfluentialSelf-citation
Cortical cholinergic inputs mediating arousal, attentional processing and dreaming: differential afferent regulation of the basal forebrain by telencephalic and brainstem afferents
Sarter, M. F., & Bruno, J. P. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00487-x · Cited by 417
Glutamate, Dopamine, and Schizophrenia: From Pathophysiology to Treatment
LARUELLE, M., KEGELES, L. S., & ABI‐DARGHAM, A. (2003) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1300.063 · Cited by 437
The role of dendrites in auditory coincidence detection
Agmon-Snir, H., Carr, C. E., & Rinzel, J. (1998) · Nature · doi:10.1038/30505 · Cited by 409
Reinforcing Effects of Psychostimulants in Humans Are Associated with Increases in Brain Dopamine and Occupancy of D2Receptors
Volkow, N. D., Wang, G., Fowler, J. S., Logan, J., Gatley, S. J., Wong, C., Hitzemann, R., & Pappas, N. R. (1999) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)35115-8 · Cited by 422
“, 1993), differences in binding between placebo and MP predominantly reflect MP-induced changes in synaptic DA, which occupies DA D2 receptors (Volkow et al., 1994; Breier et al., 1997).”
Modulation of amphetamine-induced striatal dopamine release by ketamine in humans: implications for schizophrenia.
Kegeles, L., Abi-Dargham, A., Zea-Ponce, Y., Rodenhiser-Hill, J., Mann, J., Heertum, R. V. V., Cooper, T. B., Carlsson, A., & Laruelle, M. (2000) · Biological Psychiatry · doi:10.1016/s0006-3223(00)00976-8 · Cited by 425
“In three independent cohorts, the amphetamineinduced reduction in radiotracer BP was found to be significantly increased in patients with schizophrenia, as compared with matched healthy control subjects (Abi- Dargham et al 1998; Breier et al 1997b; Laruelle et al 1996).”
Result
Dopaminergic dysfunction in schizophrenia: Salience attribution revisited
Heinz, A., & Schlagenhauf, F. (2010) · Schizophrenia Bulletin · doi:10.1093/schbul/sbq031 · Cited by 412
Role of dopamine in drug reinforcement and addiction in humans: results from imaging studies
Volkow, N. D., Fowler, J. S., & Wang, G.-J. (2002) · Behavioural Pharmacology · doi:10.1097/00008877-200209000-00008 · Cited by 398
“A limitation of these studies is that, although the changes in [(11)C]raclopride binding are linearly related to extracellular DA in animal experiments (Breier et al., 1997), the precise relationship with synaptic DA is not understood.”
Review: Glutamate and dopamine dysregulation in schizophrenia — a synthesis and selective review
Stone, J. M., Morrison, P. D., & Pilowsky, L. S. (2007) · Journal of Psychopharmacology · doi:10.1177/0269881106073126 · Cited by 362
Dopamine D2 receptors and their role in atypical antipsychotic action: still necessary and may even be sufficient
Kapur, S., & Remington, G. J. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01251-3 · Cited by 390
Corticolimbic Dopamine Neurotransmission Is Temporally Dissociated from the Cognitive and Locomotor Effects of Phencyclidine
Adams, B. W., & Moghaddam, B. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-14-05545.1998 · Cited by 388
The "two-headed" latent inhibition model of schizophrenia: modeling positive and negative symptoms and their treatment
Weiner, I. (2003) · Psychopharmacology · doi:10.1007/s00213-002-1313-x · Cited by 398
Do we still believe in the dopamine hypothesis? New data bring new evidence.
Abi-Dargham, A. (2004) · International Journal of Neuropsychopharmacology · doi:10.1017/s1461145704004110 · Cited by 373
“Dopamine transmission in patients with schizophrenia has been investigated in many studies using the paradigm described above (Abi-Dargham et al., 1998 ; Breier et al., 1997 ; Laruelle et al., 1999).”
Method
Neurobiology of Dopamine in Schizophrenia
Guillin, O., Abi‐Dargham, A., & Laruelle, M. (2007) · International Review of Neurobiology · doi:10.1016/s0074-7742(06)78001-1 · Cited by 365
“Three out of three studies (Abi-Dargham et al. 1998b; Breier et al. 1997a; Laruelle et al. 1996a) showed that the amphetamineinduced decrease in [ 11 C]raclopride or [ 123 I]IBZM binding is elevated in untreated patients with schizophrenia compared to well matched controls (Table 3).”
BackgroundMethod
Sex Differences in Striatal Dopamine Release in Healthy Adults
Munro, C. A., McCaul, M. E., Wong, D. F., Oswald, L. M., Zhou, Y., Brašić, J. R., Kuwabara, H., Kumar, A., Alexander, M., Ye, W., et al. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.01.008 · Cited by 361
Neurochemical Sensitization in the Pathophysiology of Schizophrenia: Deficits and Dysfunction in Neuronal Regulation and Plasticity
Lieberman, J. A. (1997) · Neuropsychopharmacology · doi:10.1016/s0893-133x(97)00045-6 · Cited by 335
Mechanism of action of methylphenidate: Insights from PET imaging studies
Volkow, N. D., Fowler, J. S., Wang, G., Ding, Y., & Gatley, S. J. (2002) · Journal of Attention Disorders · doi:10.1177/070674370200601s05 · Cited by 353
Amphetamine-induced dopamine release: markedly blunted in cocaine dependence and predictive of the choice to self-administer cocaine
Martinez, D., Narendran, R., Foltin, R. W., Slifstein, M., Hwang, D.-R., Broft, A., Huang, Y., Cooper, T. B., Fischman, M. W., Kleber, H. D., et al. (2007) · American Journal of Psychiatry · doi:10.1176/ajp.2007.164.4.622 · Cited by 351
“It should be noted that amphetamine, rather than cocaine, was chosen for challenge because amphetamine can be administered to healthy subjects and since the correlation between dopamine and radiotracer displacement has been established in microdialysis studies on nonhuman primates (30, 31).”
Background
Antipsychotics: Mechanisms underlying clinical response and side-effects and novel treatment approaches based on pathophysiology
Kaar, S. J., Natesan, S., McCutcheon, R. A., & Howes, O. D. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.107704 · Cited by 404
Anatomical Substrates for Glutamate‐Dopamine Interactions
Sesack, S. R., CARR, D. B., Omelchenko, N., & Pinto, A. (2003) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1300.066 · Cited by 372
The neonatal ventral hippocampal lesion as a heuristic neurodevelopmental model of schizophrenia
Tseng, K. Y., Chambers, R. A., & Lipska, B. K. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.11.039 · Cited by 355
The role of endogenous sensitization in the pathophysiology of schizophrenia: Implications from recent brain imaging studies
Laruelle, M. A. (2000) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00054-5 · Cited by 360
Increased dopamine synthesis rate in medial prefrontal cortex and striatum in schizophrenia indicated by L-(beta-11C) DOPA and PET.
Lindström, L., Gefvert, O., Hagberg, G., Lundberg, T., Bergström, M., Hartvig, P., & Långström, B. (1999) · Biological Psychiatry · doi:10.1016/s0006-3223(99)00109-2 · Cited by 332
Probabilistic reversal learning impairments in schizophrenia: Further evidence of orbitofrontal dysfunction
Waltz, J. A., & Gold, J. M. (2007) · Schizophrenia Research · doi:10.1016/j.schres.2007.03.010 · Cited by 331
“Schizophrenia has also been associated with excessive dopaminergic tone in the basal ganglia (Breier et al., 1997; Abi-Dargham et al., 1998), along with reduced stimulus-evoked activity in the ventral striatum (Juckel et al.”
Background
Depressed Dopamine Activity in Caudate and Preliminary Evidence of Limbic Involvement in Adults With Attention-Deficit/Hyperactivity Disorder
Volkow, N. D., Wang, G.-J., Newcorn, J., Telang, F., Solanto, M. V., Fowler, J. S., Logan, J., Ma, Y., Schulz, K., Pradhan, K., et al. (2007) · Archives of General Psychiatry · doi:10.1001/archpsyc.64.8.932 · Cited by 331
“First, although changes in [(11)C]raclopride binding are related to extracellular DA, the precise relationship with extracellular DA is not understood.(33,53) The poor temporal resolution of PET allowed us to detect DA changes only over a 20- to 30-minute period, reflecting mostly tonic DA activity, and thus we could…”
Background
Dopamine, psychosis and schizophrenia: the widening gap between basic and clinical neuroscience
Kesby, J. P., Eyles, D. W., McGrath, J. J., & Scott, J. G. (2018) · Translational Psychiatry · doi:10.1038/s41398-017-0071-9 · Cited by 382
Models of schizophrenia in humans and animals based on inhibition of NMDA receptors
Bubeníková‐Valešová, V., Horáček, J., Vrajová, M., & Höschl, C. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.03.012 · Cited by 346
“Similar changes in the glutamatergic and dopaminergic systems were found in patients with schizophrenia (Kim et al., 1980; Tsai et al., 1995; Breier et al., 1997).”
Result
Dopamine release in human ventral striatum and expectation of reward.
de la Fuente-Fernández, R., Phillips, A., Zamburlini, M., Sossi, V., Calne, D., Ruth, T. J., & Stoessl, A. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00130-4 · Cited by 329
Relationship between blockade of dopamine transporters by oral methylphenidate and the increases in extracellular dopamine: therapeutic implications
Volkow, N. D., Wang, G., Fowler, J. S., Logan, J., Franceschi, D., Maynard, L., Ding, Y., Gatley, S. J., Gifford, A., Zhu, W., et al. (2002) · Synapse · doi:10.1002/syn.10038 · Cited by 321
“These relatively small changes reflect the limited sensitivity of the [11C]raclopride displacement method; it has been estimated that an 8-fold increase in extracellular DA will decrease [11C]raclopride specific binding by less than 1% (Breier et al., 1997).”
BackgroundInfluential
Comparative and Interactive Human Psychopharmacologic Effects of Ketamine and Amphetamine: Implications for Glutamatergic and Dopaminergic Model Psychoses and Cognitive Function
Krystal, J. H., Perry, E. B., Gueorguieva, R., Belger, A., Madonick, S. H., Abi-Dargham, A., Cooper, T. B., MacDougall, L., Abi-Saab, W., & D’Souza, D. C. (2005) · Archives of General Psychiatry · doi:10.1001/archpsyc.62.9.985 · Cited by 317
“This study used a relatively high dose of amphetamine, in the range that worsened psychosis in patients diagnosed as having schizophrenia.(28,29) As a result, a relatively low subanesthetic dose of ketamine was used to minimize the cardiovascular risk to the research participants.”
Result
Imaging studies on the role of dopamine in cocaine reinforcement and addiction in humans
Volkow, N. D., Fowler, J. S., & Wang, G.-J. (1999) · Journal of Psychopharmacology · doi:10.1177/026988119901300406 · Cited by 315
“induced by psychostimulants as assessed with microdialysis and those obtained using PET or SPECT (Breier et al., 1997; Laruelle et al., 1997a).”
BackgroundMethodInfluential
Defining the locus of dopaminergic dysfunction in schizophrenia: A meta-analysis and test of the mesolimbic hypothesis
McCutcheon, R., Beck, K., Jauhar, S., & Howes, O. D. (2018) · Schizophrenia Bulletin · doi:10.1093/schbul/sbx180 · Cited by 305
Modeling Sensitization to Stimulants in Humans: An [ 11 C]Raclopride/Positron Emission Tomography Study in Healthy Men
Boileau, I., Dagher, A., Leyton, M., Gunn, R. N., Baker, G. B., Diksic, M., & Benkelfat, C. (2006) · Archives of General Psychiatry · doi:10.1001/archpsyc.63.12.1386 · Cited by 305
Video Games and Rehabilitation
Lohse, K. R., Shirzad, N., Verster, A., Hodges, N. J., & der Loos, H. F. M. V. (2013) · Neurology Report · doi:10.1097/npt.0000000000000017 · Cited by 339
Reviewing the ketamine model for schizophrenia
Frohlich, J., & Van Horn, J. D. (2014) · Journal of Psychopharmacology · doi:10.1177/0269881113512909 · Cited by 303
“This enhanced sensitivity to the dopaminergic effects of amphetamine challenge is also characteristic of schizophrenia patients, as revealed by PET and SPECT imaging (Breier et al., 1997; Laruelle et al., 1996).”
Result
Molecular Imaging of the Dopaminergic System and its Association with Human Cognitive Function
Cropley, V., Fujita, M., Innis, R. B., & Nathan, P. J. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.03.004 · Cited by 287
Neurotransmitter interactions in schizophrenia–therapeutic implications
Carlsson, A., Waters, N., & Carlsson, M. L. (1999) · Biological Psychiatry · doi:10.1016/s0006-3223(99)00117-1 · Cited by 298
Schizophrenia: from phenomenology to neurobiology
Wong, A. H. C., & Tol, H. H. M. V. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(03)00035-6 · Cited by 292
“[103] Breier A, Su TP, Saunders R, Carson RE, Kolachana BS, de Bartolomeis A, Weinberger DR, Weisenfeld N, Malhotra AK, Eckelman WC, Pickar D.”
Background
Towards a muscarinic hypothesis of schizophrenia
Raedler, T. J., Bymaster, F. P., Tandon, R., Copolov, D., & Dean, B. (2006) · Molecular Psychiatry · doi:10.1038/sj.mp.4001924 · Cited by 298
Hyperactivity, elevated dopaminergic transmission, and response to amphetamine in M1 muscarinic acetylcholine receptor-deficient mice
Gerber, D., Sotnikova, T. D., Gainetdinov, R., Huang, S., Caron, M., & Tonegawa, S. (2001) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.261583798 · Cited by 282
Evidence That Methylphenidate Enhances the Saliency of a Mathematical Task by Increasing Dopamine in the Human Brain
Volkow, N. D., Wang, G.-J., Fowler, J. S., Telang, F., Maynard, L., Logan, J., Gatley, S. J., Pappas, N., Wong, C., Vaska, P., et al. (2004) · American Journal of Psychiatry · doi:10.1176/appi.ajp.161.7.1173 · Cited by 281
“We used PET imaging with [11C]raclopride, a dopamine D2 receptor ligand sensitive to competition with endogenous dopamine (10), to measure the relative changes in extracellular dopamine induced by methylphenidate when administered before the mathematical task and before the neutral task.”
BackgroundMethod
Schizophrenia: More dopamine, more D 2 receptors
Seeman, P., & Kapur, S. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.14.7673 · Cited by 279
Pathway-Specific Dopamine Abnormalities in Schizophrenia
Weinstein, J. J., Chohan, M. O., Slifstein, M., Kegeles, L. S., Moore, H. M., & Abi‐Dargham, A. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.03.2104 · Cited by 308
“Using D2 radiotracers and a psychostimulant challenge, four studies showed higher release in the striatum of antipsychotic-free (Rx-free) patients compared to healthy controls (HC) (52-55).”
Genetics, Cognition, and Neurobiology of Schizotypal Personality: A Review of the Overlap with Schizophrenia
Ettinger, U., Meyhöfer, I., Steffens, M., Wagner, M., & Koutsouleris, N. (2014) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2014.00018 · Cited by 300
“Imaging studies have shown that patients with schizophrenia, both in the acute phase and in remission, show amphetamine-induced reductions in D2 and D3 dopamine receptor binding potential in the striatum (177, 178).”
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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