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01.01.2014 | Original Article

Stimulant drugs trigger transient volumetric changes in the human ventral striatum

verfasst von: Elseline Hoekzema, Susana Carmona, J. Antoni Ramos-Quiroga, Clara Canals, Ana Moreno, Vanesa Richarte Fernández, Marisol Picado, Rosa Bosch, Lurdes Duñó, Juan Carlos Soliva, Mariana Rovira, Antonio Bulbena, Adolf Tobeña, Miguel Casas, Oscar Vilarroya

Erschienen in: Brain Structure and Function | Ausgabe 1/2014

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Abstract

The ventral striatum (VStr) integrates mesolimbic dopaminergic and corticolimbic glutamatergic afferents and forms an essential component of the neural circuitry regulating impulsive behaviour. This structure represents a primary target of psychostimulant medication, the first-choice treatment for attention-deficit/hyperactivity disorder (ADHD), and is biochemically modified by these drugs in animals. However, the effects of stimulants on the human VStr remain to be determined. We acquired anatomical brain MRI scans from 23 never-medicated adult patients with ADHD, 31 adult patients with a history of stimulant treatment and 32 control subjects, and VStr volumes were determined using individual rater-blinded region of interest delineation on high-resolution neuroanatomical scans. Furthermore, we also extracted VStr volumes before and after methylphenidate treatment in a subsample of the medication-naïve adult patients as well as in 20 never-medicated children with ADHD. We observed smaller VStr volumes in adult patients with a history of stimulant treatment in comparison to never-medicated patients. Moreover, our longitudinal analyses uncovered a reduction of grey matter volume in the bilateral VStr in adult patients after exposure to methylphenidate, which was followed by volumetric recovery to control level. In children, the same pattern of VStr volume changes was observed after treatment with methylphenidate. These findings suggest that the altered VStr volumes previously observed in patients with ADHD may represent a transitory effect of stimulant exposure rather than an intrinsic feature of the disorder. More generally, these data show that stimulant drugs can render plastic volume changes in human VStr neuroanatomy.

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Achenbach TM, Ruffle TM (2000) The Child Behavior Checklist and related forms for assessing behavioral/emotional problems and competencies. Pediatr Rev 21:265–271PubMedCrossRef

Adriani W, Canese R, Podo F, Laviola G (2007) 1H MRS-detectable metabolic brain changes and reduced impulsive behavior in adult rats exposed to methylphenidate during adolescence. Neurotoxicol Teratol 29:116–125PubMedCrossRef

Adriani W, Boyer F, Gioiosa L, Macri S, Dreyer JL, Laviola G (2009) Increased impulsive behavior and risk proneness following lentivirus-mediated dopamine transporter over-expression in rats’ nucleus accumbens. Neuroscience 159:47–58PubMedCrossRef

American Psychiatric Association. Task Force on DSM-IV (2000) Diagnostic and statistical manual of mental disorders: DSM IV-TR. American Psychiatric Association, Washington, DC

Arnsten AF (2006) Fundamentals of attention-deficit/hyperactivity disorder: circuits and pathways. J Clin Psychiatry 67(Suppl 8):7–12PubMed

Basar K, Sesia T, Groenewegen H, Steinbusch HW, Visser-Vandewalle V, Temel Y (2010) Nucleus accumbens and impulsivity. Prog Neurobiol 92:533–557PubMedCrossRef

Benedict RH, Ramasamy D, Munschauer F, Weinstock-Guttman B, Zivadinov R (2009) Memory impairment in multiple sclerosis: correlation with deep grey matter and mesial temporal atrophy. J Neurol Neurosurg Psychiatry 80:201–206PubMedCrossRef

Bigler ED, Abildskov TJ, Wilde EA, McCauley SR, Li X, Merkley TL, Fearing MA, Newsome MR, Scheibel RS, Hunter JV, Chu Z, Levin HS (2010) Diffuse damage in pediatric traumatic brain injury: a comparison of automated versus operator-controlled quantification methods. Neuroimage 50:1017–1026PubMedCrossRef

Brandon CL, Steiner H (2003) Repeated methylphenidate treatment in adolescent rats alters gene regulation in the striatum. Eur J Neurosci 18:1584–1592PubMedCrossRef

Cardinal RN, Cheung TH (2005) Nucleus accumbens core lesions retard instrumental learning and performance with delayed reinforcement in the rat. BMC Neurosci 6:9PubMedCentralPubMedCrossRef

Cardinal RN, Howes NJ (2005) Effects of lesions of the nucleus accumbens core on choice between small certain rewards and large uncertain rewards in rats. BMC Neurosci 6:37PubMedCentralPubMedCrossRef

Cardinal RN, Pennicott DR, Sugathapala CL, Robbins TW, Everitt BJ (2001) Impulsive choice induced in rats by lesions of the nucleus accumbens core. Science 292:2499–2501PubMedCrossRef

Cardinal RN, Parkinson JA, Hall J, Everitt BJ (2002) Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci Biobehav Rev 26:321–352PubMedCrossRef

Carey MP, Diewald LM, Esposito FJ, Pellicano MP, Gironi Carnevale UA, Sergeant JA, Papa M, Sadile AG (1998) Differential distribution, affinity and plasticity of dopamine D-1 and D-2 receptors in the target sites of the mesolimbic system in an animal model of ADHD. Behav Brain Res 94:173–185PubMedCrossRef

Carmona S, Proal E, Hoekzema EA, Gispert JD, Picado M, Moreno I, Soliva JC, Bielsa A, Rovira M, Hilferty J, Bulbena A, Casas M, Tobena A, Vilarroya O (2009) Ventro-striatal reductions underpin symptoms of hyperactivity and impulsivity in attention-deficit/hyperactivity disorder. Biol Psychiatry 66:972–977PubMedCrossRef

Cavaliere C, Cirillo G, Bianco MR, Adriani W, De SA, Leo D, Perrone-Capano C, Papa M (2012) Methylphenidate administration determines enduring changes in neuroglial network in rats. Eur Neuropsychopharmacol 22:53–63PubMedCrossRef

Chase TD, Carrey N, Brown RE, Wilkinson M (2005) Methylphenidate regulates c-fos and fosB expression in multiple regions of the immature rat brain. Brain Res Dev Brain Res 156:1–12PubMedCrossRef

Conners CK, Sitarenios G, Parker JD, Epstein JN (1998a) Revision and restandardization of the Conners Teacher Rating Scale (CTRS-R): factor structure, reliability, and criterion validity. J Abnorm Child Psychol 26:279–291PubMedCrossRef

Conners CK, Sitarenios G, Parker JD, Epstein JN (1998b) The revised Conners’ Parent Rating Scale (CPRS-R): factor structure, reliability, and criterion validity. J Abnorm Child Psychol 26:257–268PubMedCrossRef

Conners CK, Erhardt D, Sparrow E (1999) Conners’ Adult ADHD Rating Scales (CAARS): technical manual. MHS Inc, New York

Dabbs K, Becker T, Jones J, Rutecki P, Seidenberg M, Hermann B (2012) Brain structure and aging in chronic temporal lobe epilepsy. Epilepsia 53:1033–1043PubMedCentralPubMedCrossRef

Dewey J, Hana G, Russell T, Price J, McCaffrey D, Harezlak J, Sem E, Anyanwu JC, Guttmann CR, Navia B, Cohen R, Tate DF (2010) Reliability and validity of MRI-based automated volumetry software relative to auto-assisted manual measurement of subcortical structures in HIV-infected patients from a multisite study. Neuroimage 51:1334–1344PubMedCentralPubMedCrossRef

DuPaul GJ (1998) ADHD rating scale-IV: checklists, norms and clinical interpretation. Guilford Press, New York

Epstein J, Johnson D, Conners K (1999) Conners adult ADHD Diagnostic Interview for DSM-IV. Multi-Health Systems, North Tonawanda

First M, Gibbon M, Spitzer R, William BW, Benjamin LS (1997) Interview for DSM-IV Axis II Personality Disorders SCID-II. American Psychiatric Press, Washington, DC

First M, Spitzer R, Gibbon M, Williams JBW (2002) Structured Clinical Interview for DSM-IV-TR Axis I Disorders: research version, patient edition. Biometrics Research, New York State Psychiatric Institute, New York

Fukui R, Svenningsson P, Matsuishi T, Higashi H, Nairn AC, Greengard P, Nishi A (2003) Effect of methylphenidate on dopamine/DARPP signalling in adult, but not young, mice. J Neurochem 87:1391–1401PubMedCrossRef

Guitart-Masip M, Johansson B, Fernandez-Teruel A, Canete T, Tobena A, Terenius L, Gimenez-Llort L (2006) Divergent anatomical pattern of D1 and D3 binding and dopamine- and cyclic AMP-regulated phosphoprotein of 32 kDa mRNA expression in the Roman rat strains: implications for drug addiction. Neuroscience 142:1231–1243PubMedCrossRef

Guitart-Masip M, Bunzeck N, Stephan KE, Dolan RJ, Duzel E (2010) Contextual novelty changes reward representations in the striatum. J Neurosci 30:1721–1726PubMedCentralPubMedCrossRef

Gunduz H, Wu H, Ashtari M, Bogerts B, Crandall D, Robinson DG, Alvir J, Lieberman J, Kane J, Bilder R (2002) Basal ganglia volumes in first-episode schizophrenia and healthy comparison subjects. Biol Psychiatry 51:801–808PubMedCrossRef

Haber SN, Knutson B (2010) The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 35:4–26PubMedCrossRef

Hawken CM, Brown RE, Carrey N, Wilkinson M (2004) Long-term methylphenidate treatment down-regulates c-fos in the striatum of male CD-1 mice. NeuroReport 15:1045–1048PubMedCrossRef

Ikemoto S (2007) Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res Rev 56:27–78PubMedCentralPubMedCrossRef

Izawa E, Zachar G, Yanagihara S, Matsushima T (2003) Localized lesion of caudal part of lobus parolfactorius caused impulsive choice in the domestic chick: evolutionarily conserved function of ventral striatum. J Neurosci 23:1894–1902PubMed

Kaufman J, Birmaher B, Brent D, Rao U, Flynn C, Moreci P, Williamson D, Ryan N (1997) Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL): initial reliability and validity data. J Am Acad Child Adolesc Psychiatry 36:980–988PubMedCrossRef

Kim Y, Teylan MA, Baron M, Sands A, Nairn AC, Greengard P (2009) Methylphenidate-induced dendritic spine formation and DeltaFosB expression in nucleus accumbens. Proc Natl Acad Sci U S A 106:2915–2920PubMedCentralPubMedCrossRef

Knutson B, Cooper JC (2005) Functional magnetic resonance imaging of reward prediction. Curr Opin Neurol 18:411–417PubMedCrossRef

Kuczenski R, Segal DS (1997) Effects of methylphenidate on extracellular dopamine, serotonin, and norepinephrine: comparison with amphetamine. J Neurochem 68:2032–2037PubMedCrossRef

Lee KW, Kim Y, Kim AM, Helmin K, Nairn AC, Greengard P (2006) Cocaine-induced dendritic spine formation in D1 and D2 dopamine receptor-containing medium spiny neurons in nucleus accumbens. Proc Natl Acad Sci U S A 103:3399–3404PubMedCentralPubMedCrossRef

Leo D, Adriani W, Cavaliere C, Cirillo G, Marco EM, Romano E, di Porzio U, Papa M, Perrone-Capano C, Laviola G (2009) Methylphenidate to adolescent rats drives enduring changes of accumbal Htr7 expression: implications for impulsive behavior and neuronal morphology. Genes Brain Behav 8:356–368PubMedCrossRef

Miller DB, O’Callaghan JP, Ali SF (2000) Age as a susceptibility factor in the striatal dopaminergic neurotoxicity observed in the mouse following substituted amphetamine exposure. Ann NY Acad Sci 914:194–207PubMedCrossRef

Moll GH, Hause S, Ruther E, Rothenberger A, Huether G (2001) Early methylphenidate administration to young rats causes a persistent reduction in the density of striatal dopamine transporters. J Child Adolesc Psychopharmacol 11:15–24PubMedCrossRef

Nardelli A, Lebel C, Rasmussen C, Andrew G, Beaulieu C (2011) Extensive deep gray matter volume reductions in children and adolescents with fetal alcohol spectrum disorders. Alcohol Clin Exp Res 35:1404–1417PubMed

Northoff G, Hayes DJ (2011) Is our self nothing but reward? Biol Psychiatry 69:1019–1025PubMedCrossRef

O’Doherty JP (2004) Reward representations and reward-related learning in the human brain: insights from neuroimaging. Curr Opin Neurobiol 14:769–776PubMedCrossRef

O’Doherty J, Dayan P, Schultz J, Deichmann R, Friston K, Dolan RJ (2004) Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science 304:452–454PubMedCrossRef

O’Doherty JP, Buchanan TW, Seymour B, Dolan RJ (2006) Predictive neural coding of reward preference involves dissociable responses in human ventral midbrain and ventral striatum. Neuron 49:157–166PubMedCrossRef

Plichta MM, Vasic N, Wolf RC, Lesch KP, Brummer D, Jacob C, Fallgatter AJ, Gron G (2009) Neural hyporesponsiveness and hyperresponsiveness during immediate and delayed reward processing in adult attention-deficit/hyperactivity disorder. Biol Psychiatry 65:7–14PubMedCrossRef

Pulipparacharuvil S, Renthal W, Hale CF, Taniguchi M, Xiao G, Kumar A, Russo SJ, Sikder D, Dewey CM, Davis MM, Greengard P, Nairn AC, Nestler EJ, Cowan CW (2008) Cocaine regulates MEF2 to control synaptic and behavioral plasticity. Neuron 59:621–633PubMedCentralPubMedCrossRef

Ramos-Quiroga JA, Bosch R, Richarte Fernández V, Valero S, Gómez-Barros N, Nogueira M, Palomar G, Corrales M, Sáez-Francàs N, Corominas M, Real A, Vidal R, Chalita PJ, Casas M (2012) Validez de criterio y concurrente de la versión española de la Conners Adult ADHD Diagnostic Interview for DSM-IV. Rev Psiquiatr Salud Ment (Barc) 5:229–235

Ricaurte GA, Mechan AO, Yuan J, Hatzidimitriou G, Xie T, Mayne AH, McCann UD (2005) Amphetamine treatment similar to that used in the treatment of adult attention-deficit/hyperactivity disorder damages dopaminergic nerve endings in the striatum of adult nonhuman primates. J Pharmacol Exp Ther 315:91–98PubMedCrossRef

Robbins TW, Everitt BJ (1996) Neurobehavioural mechanisms of reward and motivation. Curr Opin Neurobiol 6:228–236PubMedCrossRef

Robinson TE, Kolb B (1997) Persistent structural modifications in nucleus accumbens and prefrontal cortex neurons produced by previous experience with amphetamine. J Neurosci 17:8491–8497PubMed

Robinson TE, Kolb B (2004) Structural plasticity associated with exposure to drugs of abuse. Neuropharmacology 47(Suppl 1):33–46PubMedCrossRef

Robinson TE, Gorny G, Mitton E, Kolb B (2001) Cocaine self-administration alters the morphology of dendrites and dendritic spines in the nucleus accumbens and neocortex. Synapse 39:257–266PubMedCrossRef

Sagvolden T, Johansen EB, Aase H, Russell VA (2005) A dynamic developmental theory of attention-deficit/hyperactivity disorder (ADHD) predominantly hyperactive/impulsive and combined subtypes. Behav Brain Sci 28:397–419PubMedCrossRef

Scheres A, Milham MP, Knutson B, Castellanos FX (2007) Ventral striatal hyporesponsiveness during reward anticipation in attention-deficit/hyperactivity disorder. Biol Psychiatry 61:720–724PubMedCrossRef

Sonuga-Barke EJ (2003) The dual pathway model of AD/HD: an elaboration of neuro-developmental characteristics. Neurosci Biobehav Rev 27:593–604PubMedCrossRef

Sonuga-Barke EJ (2005) Causal models of attention-deficit/hyperactivity disorder: from common simple deficits to multiple developmental pathways. Biol Psychiatry 57:1231–1238PubMedCrossRef

Strohle A, Stoy M, Wrase J, Schwarzer S, Schlagenhauf F, Huss M, Hein J, Nedderhut A, Neumann B, Gregor A, Juckel G, Knutson B, Lehmkuhl U, Bauer M, Heinz A (2008) Reward anticipation and outcomes in adult males with attention-deficit/hyperactivity disorder. Neuroimage 39:966–972PubMedCrossRef

Tricomi E, Rangel A, Camerer CF, O’Doherty JP (2010) Neural evidence for inequality-averse social preferences. Nature 463:1089–1091PubMedCrossRef

Tripp G, Wickens JR (2008) Research review: dopamine transfer deficit: a neurobiological theory of altered reinforcement mechanisms in ADHD. J Child Psychol Psychiatry 49:691–704PubMedCrossRef

Volz TJ, Farnsworth SJ, Hanson GR, Fleckenstein AE (2008) Methylphenidate-induced alterations in synaptic vesicle trafficking and activity. Ann NY Acad Sci 1139:285–290PubMedCentralPubMedCrossRef

Ward MF, Wender PH, Reimherr FW (1993) The Wender Utah Rating Scale: an aid in the retrospective diagnosis of childhood attention deficit hyperactivity disorder. Am J Psychiatry 150:885–890PubMed

Wechsler D (1997) Wechsler Adult Intelligence Scale-III. The Psychological Corporation, San Antonio

Wechsler D (2004) The Wechsler intelligence scale for children-fourth edition. Pearson Assessment, London

Wilens TE (2008) Effects of methylphenidate on the catecholaminergic system in attention-deficit/hyperactivity disorder. J Clin Psychopharmacol 28:S46–S53PubMedCrossRef

Wittmann BC, Daw ND, Seymour B, Dolan RJ (2008) Striatal activity underlies novelty-based choice in humans. Neuron 58:967–973PubMedCentralPubMedCrossRef

Wu Y, Ragin AB, Du H, Sidharthan S, Dunkle EE, Koktzoglou I, Edelman RR (2010) Sub-millimeter isotropic MRI for segmentation of subcortical brain regions and brain visualization. J Magn Reson Imaging 31:980–986PubMedCentralPubMedCrossRef

Titel: Stimulant drugs trigger transient volumetric changes in the human ventral striatum
verfasst von: Elseline Hoekzema
Susana Carmona
J. Antoni Ramos-Quiroga
Clara Canals
Ana Moreno
Vanesa Richarte Fernández
Marisol Picado
Rosa Bosch
Lurdes Duñó
Juan Carlos Soliva
Mariana Rovira
Antonio Bulbena
Adolf Tobeña
Miguel Casas
Oscar Vilarroya
Publikationsdatum: 01.01.2014
Verlag: Springer Berlin Heidelberg
Erschienen in: Brain Structure and Function / Ausgabe 1/2014
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-012-0481-7

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