Effects of lowered serotonin transmission on cocaine-induced striatal dopamine response: PET [11C]raclopride study in humans

Background Low serotonin transmission is thought to increase susceptibility to a wide range of substance use disorders and impulsive traits. Aims To investigate the effects of lowered serotonin on cocaine-induced (1.0 mg/kg cocaine, self-administered intranasally) dopamine responses and drug craving. Method In non-dependent cocaine users, serotonin transmission was reduced using the acute tryptophan depletion method. Striatal dopamine responses were measured using positron emission tomography with [11C]raclopride. Results Acute tryptophan depletion increased drug craving and striatal dopamine responses to cocaine. These acute tryptophan depletion-induced increases did not occur in the absence of cocaine. Conclusions The results suggest that low serotonin transmission can increase dopaminergic and appetitive responses to cocaine. These findings might identify a mechanism by which individuals with low serotonin are at elevated risk for both substance use disorders and comorbid conditions.

[1]  N. Volkow,et al.  Neurocircuitry of Addiction , 2010, Neuropsychopharmacology.

[2]  M. Leyton.  The neurobiology of desire: Dopamine and the regulation of mood and motivational states in humans. , 2010 .

[3]  D. Louis Collins,et al.  Motion correction of multi-frame PET data in neuroreceptor mapping: Simulation based validation , 2009, NeuroImage.

[4]  Sylvia M. L. Cox,et al.  Striatal Dopamine Responses to Intranasal Cocaine Self-Administration in Humans , 2009, Biological Psychiatry.

[5]  K. Berridge,et al.  The incentive sensitization theory of addiction: some current issues , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[6]  C. Patrick,et al.  Role of Serotonin and Dopamine System Interactions in the Neurobiology of Impulsive Aggression and its Comorbidity with other Clinical Disorders. , 2008, Aggression and violent behavior.

[7]  A. Phillips,et al.  A top-down perspective on dopamine, motivation and memory , 2008, Pharmacology Biochemistry and Behavior.

[8]  A. Grace,et al.  Regulation of firing of dopaminergic neurons and control of goal-directed behaviors , 2007, Trends in Neurosciences.

[9]  W. Schultz.  Behavioral dopamine signals , 2007, Trends in Neurosciences.

[10]  S. Haber,et al.  Reward-Related Cortical Inputs Define a Large Striatal Region in Primates That Interface with Associative Cortical Connections, Providing a Substrate for Incentive-Based Learning , 2006, The Journal of Neuroscience.

[11]  M. Collu,et al.  Augmented cocaine-induced accumbal dopamine efflux, motor activity and place preference in rats fed with a tryptophan-deficient diet , 2006, Neuroscience Letters.

[12]  F. Fadda,et al.  Tryptophan-deficient diet increases the neurochemical and behavioral response to amphetamine , 2006, Brain Research.

[13]  HighWire Press,et al.  The British Journal of Psychiatry , 2006, British Journal of Psychiatry.

[14]  T. Robbins,et al.  Neural systems of reinforcement for drug addiction: from actions to habits to compulsion , 2005, Nature Neuroscience.

[15]  C. McDougle,et al.  Serotonergic mechanisms of cocaine effects in humans , 1995, Psychopharmacology.

[16]  R. Peltier,et al.  Effects of serotonergic manipulations on cocaine self-administration in rats , 2005, Psychopharmacology.

[17]  Doree Sitkoff,et al.  models homology modeling : From sequence alignments to structural A comparative study of available software for high-accuracy , 2005 .

[18]  R. Pihl,et al.  Tryptophan depletion causes a rapid lowering of mood in normal males , 2004, Psychopharmacology.

[19]  L. Howell,et al.  Serotonergic attenuation of the reinforcing and neurochemical effects of cocaine in squirrel monkeys. , 2002, The Journal of pharmacology and experimental therapeutics.

[20]  N. Volkow,et al.  L-tryptophan attenuation of the dopaminergic and behavioral responses to cocaine. , 2001, Life sciences.

[21]  Joel Paris,et al.  Brain Regional α-[11C]Methyl-l-Tryptophan Trapping in Impulsive Subjects With Borderline Personality Disorder , 2001 .

[22]  M Diksic,et al.  Brain Regional alpha-[11C]methyl-L-tryptophan trapping in impulsive subjects with borderline personality disorder. , 2001, The American journal of psychiatry.

[23]  K. Worsley,et al.  A Statistical Method for the Analysis of Positron Emission Tomography Neuroreceptor Ligand Data , 2000, NeuroImage.

[24]  C. Rouillard,et al.  Dorsal raphe stimulation differentially modulates dopaminergic neurons in the ventral tegmental area and substantia nigra , 2000, Synapse.

[25]  M. Laruelle.  Imaging Synaptic Neurotransmission with in Vivo Binding Competition Techniques: A Critical Review , 2000, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[26]  P. Fletcher,et al.  Selective destruction of brain serotonin neurons by 5,7-dihydroxytryptamine increases responding for a conditioned reward , 1999, Psychopharmacology.

[27]  Alan C. Evans,et al.  A nonparametric method for automatic correction of intensity nonuniformity in MRI data , 1998, IEEE Transactions on Medical Imaging.

[28]  Vincent J. Cunningham,et al.  Parametric Imaging of Ligand-Receptor Binding in PET Using a Simplified Reference Region Model , 1997, NeuroImage.

[29]  S. Walsh,et al.  Serotonergic mechanisms involved in the discriminative stimulus, reinforcing and subjective effects of cocaine , 1997, Psychopharmacology.

[30]  S. Kapur,et al.  Serotonin-dopamine interaction and its relevance to schizophrenia. , 1996, The American journal of psychiatry.

[31]  Y. Minabe,et al.  The depletion of brain serotonin levels by para‐chlorophenylalanine administration significantly alters the activity of midbrain dopamine cells in rats: An extracellular single cell recording study , 1996, Synapse.

[32]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

[33]  D. Collins,et al.  Automatic 3D Intersubject Registration of MR Volumetric Data in Standardized Talairach Space , 1994, Journal of computer assisted tomography.

[34]  C. Nemeroff,et al.  CSF biochemistries, glucose metabolism, and diurnal activity rhythms in alcoholic, violent offenders, fire setters, and healthy volunteers. , 1994, Archives of general psychiatry.

[35]  R. J. McDonald,et al.  A triple dissociation of memory systems: hippocampus, amygdala, and dorsal striatum. , 1993, Behavioral neuroscience.

[36]  Alan C. Evans,et al.  Anatomical mapping of functional activation in stereotactic coordinate space , 1992, NeuroImage.

[37]  L. Kozlowski,et al.  The Fagerström Test for Nicotine Dependence: a revision of the Fagerström Tolerance Questionnaire. , 1991, British journal of addiction.

[38]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[39]  W. Mcbride,et al.  Serotonin microinfusion into the ventral tegmental area increases accumbens dopamine release , 1989, Brain Research Bulletin.

[40]  A. Beaudet,et al.  Serotonin axon terminals in the ventral tegmental area of the rat: fine structure and synaptic input to dopaminergic neurons , 1987, Brain Research.

[41]  H. Fibiger,et al.  An anatomical and electrophysiological investigation of the serotonergic projection from the dorsal raphe nucleus to the substantia nigra in the rat , 1977, Neuroscience.