[en] Dopamine (DA) is a powerful neuromodulator for a wide variety of behaviors. Considerable evidence accumulated from rodent and monkey experiments over the last two decades suggests that DA activity in the frontal cortex is reciprocally linked to that in functionally related basal ganglia (BG) structures. However, the functional importance of this in humans is still unknown. To address this issue, we measured endogenous DA release using positron emission tomography in 15 healthy subjects as they practiced the first training session of a finger sequence learning task. Significant results were observed not only in striatal areas but also in extrastriatal "motor" regions, bilaterally. Faster learning was specifically coupled to lower DA release in the sensorimotor part of the globus pallidus pars interna (GPi) contralateral to the moving hand, which was paralleled by a higher increase in DA levels in the pre-supplementary motor area (pre-SMA). This finding provides original evidence supporting a motor-learning-related interaction between DA release in left GPi and pre-SMA, a mechanism that may also apply to other anatomically and functionally interconnected BG and frontal cortical areas as a function of behavior.
Disciplines :
Neurosciences & behavior Radiology, nuclear medicine & imaging
Author, co-author :
Garraux, Gaëtan ; Université de Liège -& Human Motor Control Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, USA
Peigneux, Philippe ; Université de Liège - ULiège > Département des sciences cognitives > Département des sciences cognitives
Carson, Richard E; Positron Emission Tomography Department, Clinical Center, National Institutes of Health, Bethesda, Maryland, USA
Hallett, Mark; Human Motor Control Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, USA
Language :
English
Title :
Task-related interaction between basal ganglia and cortical dopamine release.
Publication date :
2007
Journal title :
Journal of Neuroscience
ISSN :
0270-6474
eISSN :
1529-2401
Publisher :
Society for Neuroscience, Washington, United States - District of Columbia
NINDS - National Institute of Neurological Disorders and Stroke F.R.S.-FNRS - Fonds de la Recherche Scientifique BAEF - Belgian American Educational Foundation Fonds Léon Fredericq Horlait-Dapsens Foundations
Boecker H, Dagher A, Ceballos-Baumann AO, Passingham RE, Samuel M, Friston KJ, Poline JB, Dettmers C, Conrad B, Brooks DJ (1998) Role of the human rostral supplementary motor area and the basa ganglia in motor sequence control: investigations with H2 15O PET. J Neurophysiol 79:1070-1080.
Bunge SA (2004) How we use rules to select actions: a review of evidence from cognitive neuroscience. Cogn Affect Behav Neurosci 4:564-579.
Carbon M, Ghilardi MF, Feigin A, Fukuda M, Silvestri G, Mentis MJ, Ghez C, Moeller JR, Eidelberg D (2003) Learning networks in health and Parkinson's disease: reproducibility and treatment effects. Hum Brain Mapp 19:197-211.
Carlsson A, Waters N, Waters S, Carlsson ML (2000) Network interactions in schizophrenia - therapeutic implications. Brain Res Brain Res Rev 31:342-349.
Carr DB, Sesack SR (2000) Projections from the rat prefrontal cortex to the ventral tegmental area: target specificity in the synaptic associations with mesoaccumbens and mesocortical neurons. J Neurosci 20:3864-3873.
Carson RE (2000) PET physiological measurements using constant infusion. Nucl Med Biol 27:657-660.
Cheramy A, Romo R, Godeheu G, Baruch P, Glowinski J (1986) In vivo presynaptic control of dopamine release in the cat caudate nucleus - II Facilitatory or inhibitory influence of L-Glutamate. Neuroscience 19:1081-1090.
Cragg SJ, Hille CJ, Greenfield SA (2002) Functional domains in dorsal striatum of the nonhuman primate are defined by the dynamic behavior of dopamine. J Neurosci 22:5705-5712.
Duvauchelle CL, Levitin M, MacConell LA, Lee LK, Ettenberg A (1992) Opposite effects of prefrontal cortex and nucleus accumbens infusions of flupenthixol on stimulant-induced locomotion and brain stimulation reward. Brain Res 576:104-110.
Endres CJ, Carson RE (1998) Assessment of dynamic neurotransmitter changes with bolus or infusion delivery of neuroreceptor ligands. J Cereb Blood Flow Metab 18: 1196-1210.
Endres CJ, Kolachana BS, Saunders RC, Su T, Weinberger D, Breier A, Eckelman WC, Carson RE (1997) Kinetic modeling of [11C]raclopride: combined PET-microdialysis studies. J Cereb Blood Flow Metab 17:932-942.
Fujii N, Graybiel AM (2005) Time-varying covariance of neural activities recorded in striatum and frontal cortex as monkeys perform sequential-saccade tasks. Proc Natl Acad Sci USA 102:9032-9037.
Garris PA, Wightman RM (1994) Different kinetics govern dopaminergic transmission in the amygdala, prefrontal cortex, and striatum: an in vivo voltammetric study. J Neurosci 14:442-450.
Gaspar P, Berger B, Febvret A, Vigny A, Henry JP (1989) Catecholamine innervation of the human cerebral cortex as revealed by comparative immunohistochemistry of tyrosine hydroxylase and dopamine-betahydroxylase. J Comp Neurol 279:249-271.
Goerendt IK, Messa C, Lawrence AD, Grasby PM, Piccini P, Brooks DJ (2003) Dopamine release during sequential finger movements in health and Parkinson's disease: a PET study. Brain 126:312-325.
Grafton ST, Mazziotta JC, Presty S, Friston KJ, Frackowiak RS, Phelps ME (1992) Functional anatomy of human procedural learning determined with regional cerebral blood flow and PET. J Neurosci 12:2542-2548.
Grafton ST, Woods RP, Tyszka JM (1994) Functional imaging of procedural motor learning: relating cerebral blood flow with individual subject performance. Hum Brain Mapp 1:221-234.
Grafton ST, Waters C, Sutton J, Lew MF, Couldwell W (1995) Pallidotomy increases activity of motor association cortex in Parkinson's disease: a positron emission tomographic study. Ann Neurol 37:776-783.
Iwano H, Yamamuro Y, Hori K, Yamauchi T, Nomura M (1997) Effects of discrimination learning on the rat striatal dopaminergic activity: a microdialysis study. Neuroreport 8:1095-1098.
Jackson ME, Frost AS, Moghaddam B (2001) Stimulation of prefrontal cortex at physiologically relevant frequencies inhibits dopamine release in the nucleus accumbens. J Neurochem 78:920-923.
Jan C, Francois C, Tande D, Yelnik J, Tremblay L, Agid Y, Hirsch E (2000) Dopaminergic innervation of the pallidum in the normal state, in MPTP-treated monkeys and in parkinsonian patients. Eur J Neurosci 12:4525-4535.
Jiménez L, Mendez C, Cleeremans A (1996) Comparing direct and indirect measures of sequence learning. J Exp Psychol Learn Mem Cogn 22:948-969.
Joel D, Weiner I (2000) The connections of the dopaminergic system with the striatum in rats and primates: an analysis with respect to the functional and compartmental organization of the striatum. Neuroscience 96:451-474.
Karni A, Meyer G, Rey-Hipolito C, Jezzard P, Adams MM, Turner R, Ungerleider LG (1998) The acquisition of skilled motor performance: fast and slow experience-driven changes in primary motor cortex. Proc Natl Acad Sci USA 95:861-868.
Keele SW, Ivry R, Mayr U, Hazeltine E, Heuer H (2003) The cognitive and neural architecture of sequence representation. Psychol Rev 110:316-339.
Koepp MJ, Gunn RN, Lawrence AD, Cunningham DA, Jones T, Brooks DJ, Bench CJ, Grasby PM (1998) Evidence for striatal dopamine release during a video game. Nature 393:266-268.
Kolachana BS, Saunders RC, Weinberger DR (1995) Augmentation of prefrontal cortical monoaminergic activity inhibits dopamine release in the caudate nucleus: an in vivo neurochemical assessment in the rhesus monkey. Neuroscience 69:859-868.
Laruelle M (2000) Imaging synaptic neurotransmission with in vivo binding competition techniques: a critical review. J Cereb Blood Flow Metab 20:423-451.
Lungu OV, Wachter T, Liu T, Willingham DT, Ashe J (2004) Probability detection mechanisms and motor learning. Exp Brain Res 159:135-150.
Marenco S, Carson RE, Berman KF, Herscovitch P, Weinberger DR (2004) Nicotine-induced dopamine release in primates measured with [11C]raclopride PET. Neuropsychopharmacology 29:259-268.
Matsumoto N, Hanakawa T, Maki S, Graybiel AM, Kimura M (1999) Role of nigrostriatal dopamine system in learning to perform sequential motor tasks in a predictive manner. J Neurophysiol 82:978-998.
Mawlawi O, Martinez D, Slifstein M, Broft A, Chatterjee R, Hwang DR, Huang Y, Simpson N, Ngo K, Van Heertum R, Laruelle M (2001) Imaging human mesolimbic dopamine transmission with positron emission tomography: I. Accuracy and precision of D2 receptor parameter measurements in ventral striatum. J Cereb Blood Flow Metab 21:1034-1057.
Meyer JH, Gunn RN, Myers R, Grasby PM (1999) Assessment of spatial normalization of PET ligand images using ligand-specific templates. Neuroimage 9:545-553.
Nissen MJ, Bullemer P (1987) Attentional requirements of learning: evidence from performances measures. Cogn Psychol 19:1-32.
O'Donnell P (2003) Dopamine gating of forebrain neural ensembles. Eur J Neurosci 17:429-435.
Oldfield RC (1970) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97-113.
Peigneux P, Maquet P, Meulemans T, Destrebecqz A, Laureys S, Degueldre C, Delfiore G, Aerts J, Luxen A, Franck G, Van der Linden M, Cleeremans A (2000) Striatum forever, despite sequence learning variability: a random effect analysis. Hum Brain Mapp 10:179-194.
Picard N, Strick PL (1996) Motor areas of the medial wall: a review of their location and functional activation. Cereb Cortex 6:342-353.
Piccini P, Pavese N, Brooks DJ (2003) Endogenous dopamine release after pharmacological challenges in Parkinson's disease. Ann Neurol 53:647-653.
Pycock CJ, Carter CJ, Kerwin RW (1980) Effect of 6-hydroxydopamine lesions of the medial prefrontal cortex on neurotransmitter systems in subcortical sites in the rat. J Neurochem 34:91-99.
Reynolds JN, Hyland BI, Wickens JR (2001) A cellular mechanism of reward-related learning. Nature 413:67-70.
Roberts AC, De Salvia MA, Wilkinson LS, Collins P, Muir JL, Everitt BJ, Robbins TW (1994) 6-Hydroxydopamine lesions of the prefrontal cortex in monkeys enhance performance on an analog of the Wisconsin Card Sort Test: possible interactions with subcortical dopamine. J Neurosci 14:2531-2544.
Rushworth MF, Walton ME, Kennerley SW, Bannerman DM (2004) Action sets and decisions in the medial frontal cortex. Trends Cogn Sci 8:410-417.
Sakai ST, Stepniewska I, Qi HX, Kaas JH (2000) Pallidal and cerebellar afferents to pre-supplementary motor area thalamocortical neurons in the owl monkey: a multiple labeling study. J Comp Neurol 417:164-180.
Sesack SR, Carr DB, Omelchenko N, Pinto A (2003) Anatomical substrates for glutamate-dopamine interactions: evidence for specificity of connections and extrasynaptic actions. Ann NY Acad Sci 1003:36-52.
Strafella A, Paus T, Barrett J, Dagher A (2001) Repetitive transcranial stimulation of the human prefrontal cotex induces dopamine release in the caudate nucleus. J Neurosci 21: RC157.
Strafella AP, Paus T, Fraraccio M, Dagher A (2003) Striatal dopamine release induced by repetitive transcranial magnetic stimulation of the human motor cortex. Brain 126:2609-2615.
Thieben MJ, Duggins AJ, Good CD, Gomes L, Mahant N, Richards F, McCusker E, Frackowiak RS (2002) The distribution of structural neuropathology in pre-clinical Huntington's disease. Brain 125:1815-1828.
Thompson R, Huestis PW, Yu J (1987) Motor learning: nonspecific subcortical mechanisms in rats. Arch Phys Med Rehabil 68:419-422.
Watabe H, Endres CJ, Breier A, Schmall B, Eckelman WC, Carson RE (2000) Measurement of dopamine release with continuous infusion of [11C]raclopride: optimization and signal-to-noise considerations. J Nucl Med 41:522-530.
Westerink BH, Tuntler J, Damsma G, Rollema H, de Vries JB (1987) The use of tetrodotoxin for the characterization of drug-enhanced dopamine release in conscious rats studied by brain dialysis. Naunyn Schmiedebergs Arch Pharmacol 336:502-507.
Whone AL, Moore RY, Piccini PP, Brooks DJ (2003) Plasticity of the nigropallidal pathway in Parkinson's disease. Ann Neurol 53:206-213.
Wilkinson LS, Humby T, Killcross AS, Torres EM, Everitt BJ, Robbins TW (1998) Dissociations in dopamine release in medial prefrontal cortex and ventral striatum during the acquisition and extinction of classical aversive conditioning in the rat. Eur J Neurosci 10:1019-1026.
Williams D, Tijssen M, Van Bruggen G, Bosch A, Insola A, Di L, V, Mazzone P, Oliviero A, Quartarone A, Speelman H, Brown P (2002) Dopamine-dependent changes in the functional connectivity between basal ganglia and cerebral cortex in humans. Brain 125:1558 -1569.
Williams SM, Goldman-Rakic PS (1998) Widespread origin of the primate mesofrontal dopamine system. Cereb Cortex 8:321-345.
Zald DH, Boileau I, El Dearedy W, Gunn R, McGlone F, Dichter GS, Dagher A (2004) Dopamine transmission in the human striatum during monetary reward tasks. J Neurosci 24:4105- 4112.
Zhang H, Sulzer D (2003) Glutamate spillover in the striatum depresses dopaminergic transmission by activating group I metabotropic glutamate receptors. J Neurosci 23:10585-10592.