Pharmacopsychiatry 2010; 43: S32-S41
DOI: 10.1055/s-0030-1248300

© Georg Thieme Verlag KG Stuttgart · New York

Dopamine Release in the Prefrontal Cortex and Striatum: Temporal and Behavioural Aspects

W. Hauber1
  • 1Department of Animal Physiology, Institute of Biology, University of Stuttgart, Germany
Further Information

Publication History

Publication Date:
17 May 2010 (online)


Dopamine (DA) neurons originating in the substantia nigra and ventral tegmental area project to a variety of forebrain structures thereby forming a complex neuromodulatory system that is essential for numerous motor, cognitive and motivational processes. DA neurons can operate in distinct temporal modes, i. e. they display responses across varying timescales including fast phasic changes of DA release on a seconds time scale and slower phasic changes in a minutes to hour range. Furthermore, tonic levels of DA provide a DA receptor ‘tone’. Here we briefly highlight findings indicating that temporally distinct responses of DA neurons in the prefrontal cortex and striatum are related to different kinds of information and may serve dissociable behavioural functions. Furthermore we consider how DA neuronal activity and temporarily distinct patterns of DA release are regulated and summarize some relevant findings on the basic neuroanatomy of ascending DA systems. A better understanding of the specific functions of phasic and tonic DA signals will be critical for determining the role of DA in behaviour in detail.


  • 1 Alexander GE, Crutcher MD. Functional architecture of basal ganglia circuits: neural substrates of parallel processing.  Trends Neurosci. 1990;  13 266-271
  • 2 Arbuthnott GW, Wickens J. Space, time and dopamine.  Trends Neurosci. 2007;  30 62-69
  • 3 Arnsten AFT. Catecholamine modulation of prefrontal cortical cognitive function.  Trends Cogn Sci. 1998;  2
  • 4 Baker DA, Xi ZX, Shen H. et al . The origin and neuronal function of in vivo nonsynaptic glutamate.  J Neurosci. 2002;  22 9134-9141
  • 5 Bassareo V, Di Chiara G. Differential responsiveness of dopamine transmission to food-stimuli in nucleus accumbens shell/core compartments.  J Neurosci. 1999;  89 637-641
  • 6 Bassareo V, Di Chiara G. Differential influence of associative and nonassociative learning mechanisms on the responsiveness of prefrontal and accumbal dopamine transmission to food stimuli in rats fed ad libitum.  J Neurosci. 1997;  17 851-861
  • 7 Bassareo V, Di Chiara G. Modulation of feeding-induced activation of mesolimbic dopamine transmission by appetitive stimuli and its relation to motivational state.  Eur J Neurosci. 1999;  11 4389-4397
  • 8 Belin D, Everitt BJ. Cocaine seeking habits depend upon dopamine-dependent serial connectivity linking the ventral with the dorsal striatum.  Neuron. 2008;  57 432-441
  • 9 Belin D, Jonkman S, Dickinson A. et al . Parallel and interactive learning processes within the basal ganglia: relevance for the understanding of addiction.  Behav Brain Res. 2009;  199 89-102
  • 10 Bentivoglio M, Morelli M. The organization and circuits of mesencephalic dopaminergic neurons and the distribution of dopamine receptors in the brain.. In: Dunnett SD, Bentivoglio M, Björklund A, Hökfelt T, eds. Handbook of Chemical Neuroanatomy. Vol 21: Dopamine. Amsterdam: Elsevier; 2005
  • 11 Berridge KC. The debate over dopamine's role in reward: the case for incentive salience.  Psychopharmacology (Berl). 2007;  191 391-431
  • 12 Berridge KC. et al . Espresso reward learning, hold the dopamine: theoretical comment on Robinson.  Behav Neurosci. 2005;  119 336-341
  • 13 Bjorklund A, Dunnett SB. Dopamine neuron systems in the brain: an update.  Trends Neurosci. 2007;  30 194-202
  • 14 Björklund A, Lindvall O. Dopamine-containing systems in the CNS: Elsevier Science Publishers B.V.; 1984;  55
  • 15 Blaha CD, Yang CR, Floresco SB. et al . Stimulation of the ventral subiculum of the hippocampus evokes glutamate receptor-mediated changes in dopamine efflux in the rat nucleus accumbens.  Eur J Neurosci. 1997;  9 902-911
  • 16 Calaminus C, Hauber W. Guidance of instrumental behavior under reversal conditions requires dopamine D1 and D2 receptor activation in the orbitofrontal cortex.  Neuroscience. 2008;  154 1195-1204
  • 17 Carboni E, Silvagni A, Vacca C. et al . Cumulative effect of norepinephrine and dopamine carrier blockade on extracellular dopamine increase in the nucleus accumbens shell, bed nucleus of stria terminalis and prefrontal cortex.  J Neurohem. 2006;  96 473-481
  • 18 Cardinal RN, Parkinson JA, Hall J. et al . Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex.  Neurosci Biobehav Rev. 2002;  26 321-352
  • 19 Chalon S, Garreau L, Emond P. et al . Pharmacological characterization of (E)-N-(3-iodoprop-2-enyl)-2beta-carbomethoxy-3beta-(4'-methylphenyl)n ortropane as a selective and potent inhibitor of the neuronal dopamine transporter.  J Pharmacol Exp Ther. 1999;  291 648-654
  • 20 Cheng J, Feenstra MG. Individual differences in dopamine efflux in nucleus accumbens shell and core during instrumental learning.  Learn Mem. 2006;  13 168-177
  • 21 Cheng JJ, de Bruin JP, Feenstra MG. Dopamine efflux in nucleus accumbens shell and core in response to appetitive classical conditioning.  Eur J Neurosci. 2003;  18 1306-1314
  • 22 Chergui K, Charlety PJ, Akaoka H. et al . Tonic activation of NMDA receptors causes spontaneous burst discharge of rat midbrain dopamine neurons in vivo.  Eur J Neurosci. 1993;  5 137-144
  • 23 Chergui K, Suaud-Chagny MF, Gonon F. Nonlinear relationship between impulse flow, dopamine release and dopamine elimination in the rat brain in vivo.  Neuroscience. 1994;  62 641-645
  • 24 Conrad LC, Pfaff DW. Autoradiographic tracing of nucleus accumbens efferents in the rat.  Brain Res. 1976;  113 589-596
  • 25 Cools R, Frank MJ, Gibbs SE. et al . Striatal dopamine predicts outcome-specific reversal learning and its sensitivity to dopaminergic drug administration.  J Neurosci. 2009;  29 1538-1543
  • 26 Cools R, Gibbs SE, Miyakawa A. et al . Working memory capacity predicts dopamine synthesis capacity in the human striatum.  J Neurosci. 2008;  28 1208-1212
  • 27 Cornwall J, Cooper JD, Phillipson OT. Afferent and efferent connections of the laterodorsal tegmental nucleus in the rat.  Brain Res Bull. 1990;  25 271-284
  • 28 Costa A, Peppe A, Dell'Agnello G. et al . Dopamine and cognitive functioning in de novo subjects with Parkinson's disease: effects of pramipexole and pergolide on working memory.  Neuropsychologia. 2009;  47 1374-1381
  • 29 Cousins MS, Trevitt J, Atherton A. et al . Different behavioral functions of dopamine in the nucleus accumbens and ventrolateral striatum: a microdialysis and behavioral investigation.  J Neurosci. 1999;  91 925-934
  • 30 Cragg SJ, Greenfield SA. Differential autoreceptor control of somatodendritic and axon terminal dopamine release in substantia nigra, ventral tegmental area, and striatum.  J Neurosci. 1997;  17 5738-5746
  • 31 Cragg SJ, Rice ME. Dancing past the DAT at a DA synapse.  Trends Neurosci. 2004;  27 270-277
  • 32 Dahlström A, Fuxe K. Evidence for the existence of monoamine-containing neurons in the central nervous system. I. Demonstration of monoamines in the cell bodies of brain stem neurons.  Acta Physiol Scand Suppl. 1964;  232 1-55
  • 33 Damsma G, Pfaus JG, Wenkstern D. et al . Sexual behavior increases dopamine transmission in the nucleus accumbens and striatum of male rats: comparison with novelty and locomotion.  Behav Neurosci. 1992;  106 181-191
  • 34 Descarries L, Berube-Carriere N, Riad M. et al . Glutamate in dopamine neurons: synaptic versus diffuse transmission.  Brain Res Rev. 2008;  58 290-302
  • 35 Everitt BJ, Robbins TW. Neural systems of reinforcement for drug addiction: from actions to habits to compulsion.  Nat Neurosci. 2005;  8 1481-1489
  • 36 Fadel J, Deutch AY. Anatomical substrates of orexin-dopamine interactions: lateral hypothalamic projections to the ventral tegmental area.  Neuroscience. 2002;  111 379-387
  • 37 Feenstra MG, Botterblom MH. Rapid sampling of extracellular dopamine in the rat prefrontal cortex during food consumption, handling and exposure to novelty.  Brain Res. 1996;  742 17-24
  • 38 Feenstra MG, Botterblom MH, Mastenbroek S. Dopamine and noradrenaline efflux in the prefrontal cortex in the light and dark period: effects of novelty and handling and comparison to the nucleus accumbens.  Neuroscience. 2000;  100 741-748
  • 39 Fields HL, Hjelmstad GO, Margolis EB. et al . Ventral tegmental area neurons in learned appetitive behavior and positive reinforcement.  Annu Rev Neurosci. 2007;  30 289-316
  • 40 Fiorillo CD, Tobler PN, Schultz W. Discrete coding of reward probability and uncertainty by dopamine neurons.  Science. 2003;  299 1898-1902
  • 41 Floresco SB, Magyar O, Ghods-Sharifi S. et al . Multiple dopamine receptor subtypes in the medial prefrontal cortex of the rat regulate set-shifting.  Neuropsychopharmacology. 2006;  31 297-309
  • 42 Floresco SB, Phillips AG. Delay-dependent modulation of memory retrieval by infusion of a dopamine D1 agonist into the rat medial prefrontal cortex.  Behav Neurosci. 2001;  115 934-939
  • 43 Floresco SB, Todd CL, Grace AA. Glutamatergic afferents from the hippocampus to the nucleus accumbens regulate activity of ventral tegmental area dopamine neurons.  J Neurosci. 2001;  21 4915-4922
  • 44 Floresco SB, West AR, Ash B. et al . Afferent modulation of dopamine neuron firing differentially regulates tonic and phasic dopamine transmission.  Nat Neurosci. 2003;  6 968-973
  • 45 Fuchs H, Hauber W. Dopaminergic innervation of the rat globus pallidus characterized by microdialysis and immunohistochemistry.  Eep Brain Res. 2004;  154 66-75
  • 46 Garris PA, Ciolkowski EL, Pastore P. et al . Efflux of dopamine from the synaptic cleft in the nucleus accumbens of the rat brain.  J Neurosci. 1994;  14 6084-6093
  • 47 Gauthier J, Parent M, Levesque M. et al . The axonal arborization of single nigrostriatal neurons in rats.  Brain Res. 1999;  834 228-232
  • 48 Geisler S, Zahm DS. Afferents of the ventral tegmental area in the rat-anatomical substratum for integrative functions.  J Comp Neurol. 2005;  490 270-294
  • 49 Gonon FG. Nonlinear relationship between impulse flow and dopamine released by rat midbrain dopaminergic neurons as studied by in vivo electrochemistry.  Neuroscience. 1988;  24 19-28
  • 50 Goto Y, Otani S, Grace AA. The Yin and Yang of dopamine release: a new perspective.  Neuropharmacology. 2007;  53 583-587
  • 51 Grace AA. Phasic versus tonic dopamine release and the modulation of dopamine system responsivity: a hypothesis for the etiology of schizophrenia.  Neuroscience. 1991;  41 1-24
  • 52 Grace AA, Bunney BS. The control of firing pattern in nigral dopamine neurons: burst firing.  J Neurosci. 1984;  4 2877-2890
  • 53 Grace AA, Bunney BS. The control of firing pattern in nigral dopamine neurons: single spike firing.  J Neurosci. 1984;  4 2866-2876
  • 54 Grace AA, Floresco SB, Goto Y. et al . Regulation of firing of dopaminergic neurons and control of goal-directed behaviors.  Trends Neurosci. 2007;  30 220-227
  • 55 Granon S, Passetti F, Thomas KL. et al . Enhanced and impaired attentional performance after infusion of D1 dopaminergic receptor agents into rat prefrontal cortex.  J Neurosci. 2000;  20 1208-1215
  • 56 Haber SN, Fudge JL, McFarland NR. Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum.  J Neurosci. 2000;  20 2369-2382
  • 57 Hassani OK, Francois C, Yelnik J. et al . Evidence for a dopaminergic innervation of the subthalamic nucleus in the rat.  Brain Res. 1997;  749 88-94
  • 58 Hauber W. Blockade of subthalamic dopamine D1 receptors elicits akinesia in rats.  Neuroreport. 1998;  9 4115-4118
  • 59 Hauber W. Impairments of movement initiation and execution induced by a blockade of dopamine D1 or D2 receptors are reversed by a blockade of N-methyl-D-aspartate receptors.  Neuroscience. 1996;  73 121-130
  • 60 Hauber W, Fuchs H. Dopamine release in the rat globus pallidus characterised by in vivo microdialysis.  Behav Brain Res. 2000;  111 39-44
  • 61 Hauber W, Lutz S. Dopamine D1 or D2 receptor blockade in the globus pallidus produces akinesia in the rat.  Behav Brain Res. 1999;  106 143-150
  • 62 Hauber W, Neuscheler P, Nagel J. et al . Catalepsy induced by a blockade of dopamine D1 or D2 receptors was reversed by a concomitant blockade of adenosine A2A receptors in the caudate-putamen of rats.  Eur J Neurosci. 2001;  14 1287-1293
  • 63 Horvitz JC. Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events.  Neuroscience. 2000;  96 651-656
  • 64 Howland JG, Taepavarapruk P, Phillips AG. Glutamate receptor-dependent modulation of dopamine efflux in the nucleus accumbens by basolateral, but not central, nucleus of the amygdala in rats.  J Neurosci. 2002;  22 1137-1145
  • 65 Hu G, Duffy P, Swanson C. et al . The regulation of dopamine transmission by metabotropic glutamate receptors.  J Pharmacol Exp Ther. 1999;  289 412-416
  • 66 Ikemoto S. Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex.  Brain Res Rev. 2007;  56 27-78
  • 67 Imperato A, Di Chiara G. Trans-striatal dialysis coupled to reverse phase high performance liquid chromatography with electrochemical detection: a new method for the study of the in vivo release of endogenous dopamine and metabolites.  J J Neurosci. 1984;  4 966-977
  • 68 Ito R, Dalley JW, Robbins TW. et al . Dopamine Release in the Dorsal Striatum during Cocaine-Seeking Behavior under the Control of a Drug-Associated Cue.  J Neurosci. 2002;  22 6247-6253
  • 69 Johnson SW, Seutin V, North RA. Burst firing in dopamine neurons induced by N-methyl-D-aspartate: Role of the electrogenic sodium pump.  Science. 1992;  258 665
  • 70 Karreman M, Westerink BH, Moghaddam B. Excitatory amino acid receptors in the ventral tegmental area regulate dopamine release in the ventral striatum.  J Neurochem. 1996;  67 601-607
  • 71 Kawagoe KT, Garris PA, Wiedemann DJ. et al . Regulation of transient dopamine concentration gradients in the microenvironment surrounding nerve terminals in the rat striatum.  Neuroscience. 1992;  51 55-64
  • 72 Keefe KA, Sved AF, Zigmond MJ. et al . Stress-induced dopamine release in the neostriatum – evaluation of the role of action potentials in nigrostriatal dopamine neurons or local initiation by endogenous excitatory amino acids.  J Neurochem. 1993;  61 1943
  • 73 Keefe KA, Zigmond MJ, Abercrombie ED. Invivo regulation of extracellular dopamine in the neostriatum – influence of impulse activity and local excitatory amino acids.  J Neural Tranm-Gen Sect. 1993;  91 223
  • 74 Krebs MO, Desce JM, Kemel ML. et al . Glutamatergic control of dopamine release in the rat striatum: Evidence for presynaptic NMDA receptors on dopaminergic nerve terminals.  J Neurochem. 1991;  56 81
  • 75 Kretschmer BD. Modulation of the mesolimbic dopamine system by glutamate: role of NMDA receptors.  Journal of Neurochemistry. 1999;  73 839-848
  • 76 Lammel S, Hetzel A, Hackel O. et al . Unique properties of mesoprefrontal neurons within a dual mesocorticolimbic dopamine system.  Neuron. 2008;  57 760-773
  • 77 Lapish CC, Kroener S, Durstewitz D. et al . The ability of the mesocortical dopamine system to operate in distinct temporal modes.  Psychopharmacology (Berl). 2007;  191 609-625
  • 78 Leentjens AF, Koester J, Fruh B. et al . The effect of pramipexole on mood and motivational symptoms in Parkinson's disease: a meta-analysis of placebo-controlled studies.  Clinical therapeutics. 2009;  31 89-98
  • 79 Letchworth SR, Smith HR, Porrino LJ. et al . Characterization of a tropane radioligand, [(3)H]2beta-propanoyl-3beta-(4-tolyl) tropane ([(3)H]PTT), for dopamine transport sites in rat brain.  J Pharmacol Exp Ther. 2000;  293 686-696
  • 80 Lex A, Hauber W. Dopamine D1 and D2 receptors in the nucleus accumbens core and shell mediate Pavlovian-instrumental transfer.  Learn Mem. 2008;  15 483-491
  • 81 Lex B, Hauber W. The Role of Dopamine in the Prelimbic Cortex and the Dorsomedial Striatum in Instrumental Conditioning.  Cereb Cortex. 2009; 
  • 82 Lindvall O, Bjorklund A. Dopaminergic innervation of the globus pallidus by collaterals from the nigrostriatal pathway.  Brain Res. 1979;  172 169-173
  • 83 Liss B, Roeper J. Individual dopamine midbrain neurons: functional diversity and flexibility in health and disease.  Brain Res Rev. 2008;  58 314-321
  • 84 Gauthier J, Parent M, Lévesque. et al . The axonal arborizations of single nigrostriatal neurons in rats.  Brain Res. 1999;  834 228-232
  • 85 McCullough LD, Salamone JD. Involvement of nucleus accumbens dopamine in the motor activity induced by periodic food presentation: a microdialysis and behavioral study.  Brain Res. 1992;  592 29-36
  • 86 Mehta MA, Riedel WJ. Dopaminergic enhancement of cognitive function.  Curr Pharm Des. 2006;  12 2487-2500
  • 87 Murschall A, Hauber W. Inactivation of the ventral tegmental area abolished the general excitatory influence of Pavlovian cues on instrumental performance.  Learn Mem. 2006;  13 123-126
  • 88 Niv Y. Cost, benefit, tonic, phasic: what do response rates tell us about dopamine and motivation?.  Ann N Y Acad Sci. 2007;  1104 357-376
  • 89 Oakman SA, Faris PL, Kerr PE. et al . Distribution of pontomesencephalic cholinergic neurons projecting to substantia nigra differs significantly from those projecting to ventral tegmental area.  J Neurosci. 1995;  15 5859-5869
  • 90 Oorschot DE. Total number of neurons in the neostriatal, pallidal, subthalamic, and substantia nigral nuclei of the rat basal ganglia: a stereological study using the cavalieri and optical disector methods.  J Comp Neurol. 1996;  366 580-599
  • 91 Parent A, Sato F, Wu Y. et al . Organization of the basal ganglia: the importance of axonal collateralization.  Trends Neurosci. 2000;  23 S20-S27
  • 92 Paulson PE, Robinson TE. Relationship between circadian changes in spontaneous motor activity and dorsal versus ventral striatal dopamine neurotransmission assessed with on-line microdialysis.  Behav Neurosci. 1994;  108 624-635
  • 93 Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. San Diego, New York: Academic Press; 1997
  • 94 Pfaus JG, Damsma G, Nomikos GG. et al . Sexual behavior enhances central dopamine transmission in the male rat.  Brain Res. 1990;  530 345-348
  • 95 Phillips AG, Ahn S, Floresco SB. Magnitude of dopamine release in medial prefrontal cortex predicts accuracy of memory on a delayed response task.  J Neurosci. 2004;  24 547-553
  • 96 Pickel V, Sesack S. Electron microscopy of central dopamine systems.. In: Bloom FE, Kupfer DJ, eds. Psychopharmacology: the fourth generation of progress. New York: Raven Press Ltd; 1995: 257-268
  • 97 Piercey MF, Hoffmann WE, Smith MW. et al . Inhibition of dopamine neuron firing by pramipexole, a dopamine D3 receptor-preferring agonist: comparison to other dopamine receptor agonists.  Eur J Pharmacol. 1996;  312 35-44
  • 98 Rice ME, Cragg SJ. Dopamine spillover after quantal release: rethinking dopamine transmission in the nigrostriatal pathway.  Brain Res Rev. 2008;  58 303-313
  • 99 Robinson S, Sandstrom SM, Denenberg VH. et al . Distinguishing whether dopamine regulates liking, wanting, and/or learning about rewards.  Behav Neurosci. 2005;  119 5-15
  • 100 Roitman MF, Stuber GD, Phillips PE. et al . Dopamine operates as a subsecond modulator of food seeking.  J Neurosci. 2004;  24 1265-1271
  • 101 Salamone JD, Correa M, Farrar A. et al . Effort-related functions of nucleus accumbens dopamine and associated forebrain circuits.  Psychopharmacology (Berl). 2007;  191 461-482
  • 102 Sandstrom MI, Rebec GV. Extracellular ascorbate modulates glutamate dynamics: role of behavioral activation.  BMC neuroscience. 2007;  8 32
  • 103 Saulskaya N, Marsden CA. Extracellular glutamate in the nucleus accumbens during a conditioned emotional response in the rat.  Brain Res. 1995;  698 114-120
  • 104 Schott BH, Minuzzi L, Krebs RM. et al . Mesolimbic functional magnetic resonance imaging activations during reward anticipation correlate with reward-related ventral striatal dopamine release.  J Neurosci. 2008;  28 14311-14319
  • 105 Schultz W. Behavioral dopamine signals.  Trends Neurosci. 2007;  30 203-210
  • 106 Schultz W. Dopamine neurons and their role in reward mechanisms.  Curr Opin Neurobiol. 1997;  7 191-197
  • 107 Schultz W. Multiple dopamine functions at different time courses.  Annu Rev Neurosci. 2007;  30 259-288
  • 108 Schultz W. Predictive reward signal of dopamine neurons.  J Neurophysiol. 1998;  80 1-27
  • 109 Schweimer J, Hauber W. Dopamine D1 receptors in the anterior cingulate cortex regulate effort-based decision making.  Learn Mem. 2006;  13 777-782
  • 110 Seamans JK, Floresco SB, Phillips AG. D1 receptor modulation of hippocampal-prefrontal cortical circuits integrating spatial memory with executive functions in the rat.  J Neurosci. 1998;  18 1613-1621
  • 111 Semba K, Fibiger HC. Afferent connections of the laterodorsal and the pedunculopontine tegmental nuclei in the rat: a retro- and antero-grade transport and immunohistochemical study.  J Comp Neurol. 1992;  323 387-410
  • 112 Sesack SR, Aoki C, Pickel VM. Ultrastructural localization of D2 receptor-like immunoreactivity in midbrain dopamine neurons and their striatal targets.  J Neurosci. 1994;  14 88-106
  • 113 Sombers LA, Beyene M, Carelli RM. et al . Synaptic overflow of dopamine in the nucleus accumbens arises from neuronal activity in the ventral tegmental area.  J Neurosci J Neurosci. 2009;  29 1735-1742
  • 114 Stefani MR, Moghaddam B. Rule learning and reward contingency are associated with dissociable patterns of dopamine activation in the rat prefrontal cortex, nucleus accumbens, and dorsal striatum.  J Neurosci. 2006;  26 8810-8818
  • 115 Stuber GD, Klanker M, de Ridder B. et al . Reward-predictive cues enhance excitatory synaptic strength onto midbrain dopamine neurons.  Science. 2008;  321 1690-1692
  • 116 Stuber GD, Roitman MF, Phillips PE. et al . Rapid dopamine signaling in the nucleus accumbens during contingent and noncontingent cocaine administration.  Neuropsychopharmacology. 2005;  30 853-863
  • 117 Stuber GD, Wightman RM, Carelli RM. Extinction of cocaine self-administration reveals functionally and temporally distinct dopaminergic signals in the nucleus accumbens.  Neuron. 2005;  46 661-669
  • 118 Taepavarapruk P, Floresco SB, Phillips AG. Hyperlocomotion and increased dopamine efflux in the rat nucleus accumbens evoked by electrical stimulation of the ventral subiculum: role of ionotropic glutamate and dopamine D1 receptors.  Psychopharmacology (Berl). 2000;  151 242-251
  • 119 Tsai HC, Zhang F, Adamantidis A. et al . Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning.  Science. 2009;  324 1080-1084
  • 120 Wanat MJ, Willuhn I, Clark JJ. et al . Phasic dopamine release in appetitive behaviors and drug addiction.  Current Drug Abuse Reviews. 2009;  2 195-213
  • 121 Wightman RM, Heien ML, Wassum KM. et al . Dopamine release is heterogeneous within microenvironments of the rat nucleus accumbens.  Eur J Neurosci. 2007;  26 2046-2054
  • 122 Williams GV, Castner SA. Under the curve: critical issues for elucidating D1 receptor function in working memory.  N Neuroscience. 2006;  139 263-276
  • 123 Williams GV, Golman-Rakic PS. Modulation of memory fields by dopamine D1 receptors in prefrontal cortex.  Nature. 1995;  376 572
  • 124 Wilson C, Nomikos GG, Collu M. et al . Dopaminergic correlates of motivated behavior: importance of drive.  J Neurosci. 1995;  15 5169-5178
  • 125 Wilson CJ, Groves PM, Fifkova E. Monoaminergic synapses, including dendro-dendritic synapses in the rat substantia nigra.  Exp Brain Res. 1977;  30 161-174
  • 126 Wise RA. Brain reward circuitry: insights from unsensed incentives.  Neuron. 2002;  36 229-240
  • 127 Wise RA. Dopamine, learning and motivation.  Nat Rev Neurosci. 2004;  5 483-494
  • 128 Wyvell CL, Berridge KC. Intra-accumbens amphetamine increases the conditioned incentive salience of sucrose reward: enhancement of reward “Wanting” without enhanced “Liking” or response reinforcement.  J Neurosci. 2000;  20 8122-8130
  • 129 Young AM. Increased extracellular dopamine in nucleus accumbens in response to unconditioned and conditioned aversive stimuli: studies using 1 min microdialysis in rats.  J Neurosci Methods. 2004;  138 57-63
  • 130 Zahrt J, Taylor JR, Mathew RG. et al . Supranormal stimulation of D1 dopamine receptors in the rodent prefrontal cortex impairs spatial working memory performance.  J Neurosci. 1997;  17 8528-8535
  • 131 Zoli M, Jansson A, Sykova E. et al . Volume transmission in the CNS and its relevance for neuropsychopharmacology.  Trends Pharmacol. 1999;  20 142-150
  • 132 Zweifel LS, Argilli E, Bonci A. et al . Role of NMDA receptors in dopamine neurons for plasticity and addictive behaviors.  Neuron. 2008;  59 486-496
  • 133 Zweifel LS, Parker JG, Lobb CJ. et al . Disruption of NMDAR-dependent burst firing by dopamine neurons provides selective assessment of phasic dopamine-dependent behavior.  Proc Natl Acad Sci USA. 2009;  106 7281-7288


Prof. Dr. Wolfgang Hauber

Institute of Biology Department of Animal Physiology

University of Stuttgart

Pfaffenwaldring 57

D-70550 Stuttgart


Phone: +49-711-685 65003

Fax: +49-711-685 55003