Skip to main content
SpringerLink
Log in

The ability of the mesocortical dopamine system to operate in distinct temporal modes

  • Review
  • Published:
Psychopharmacology Aims and scope Submit manuscript

Abstract

Background

This review discusses evidence that cells in the mesocortical dopamine (DA) system influence information processing in target areas across three distinct temporal domains.

Discussions

Phasic bursting of midbrain DA neurons may provide temporally precise information about the mismatch between expected and actual rewards (prediction errors) that has been hypothesized to serve as a learning signal in efferent regions. However, because DA acts as a relatively slow modulator of cortical neurotransmission, it is unclear whether DA can indeed act to precisely transmit prediction errors to prefrontal cortex (PFC). In light of recent physiological and anatomical evidence, we propose that corelease of glutamate from DA and/or non-DA neurons in the VTA could serve to transmit this temporally precise signal. In contrast, DA acts in a protracted manner to provide spatially and temporally diffuse modulation of PFC pyramidal neurons and interneurons. This modulation occurs first via a relatively rapid depolarization of fast-spiking interneurons that acts on the order of seconds. This is followed by a more protracted modulation of a variety of other ionic currents on timescales of minutes to hours, which may bias the manner in which cortical networks process information. However, the prolonged actions of DA may be curtailed by counteracting influences, which likely include opposing actions at D1 and D2-like receptors that have been shown to be time- and concentration-dependent. In this way, the mesocortical DA system optimizes the characteristics of glutamate, GABA, and DA neurotransmission both within the midbrain and cortex to communicate temporally precise information and to modulate network activity patterns on prolonged timescales.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abi-Dargham A, Mawlawi O, Lombardo I, Gil R, Martinez D, Huang Y, Hwang DR, Keilp J, Kochan L, Van Heertum R, Gorman JM, Laruelle M (2002) Prefrontal dopamine D1 receptors and working memory in schizophrenia. J Neurosci 22:3708–3719

    PubMed  CAS  Google Scholar 

  • Au-Young SM, Shen H, Yang CR (1999) Medial prefrontal cortical output neurons to the ventral tegmental area (VTA) and their responses to burst-patterned stimulation of the VTA: neuroanatomical and in vivo electrophysiological analyses. Synapse 34(4):245–255 (Dec 15)

    PubMed  CAS  Google Scholar 

  • Bekkers JM (1998) Neurophysiology: are autapses prodigal synapses? Curr Biol 8:R52–R55

    PubMed  CAS  Google Scholar 

  • Berger B, Gaspar P, Verney C (1991) Dopaminergic innervation of the cerebral cortex: unexpected differences between rodents and primates. Trends Neurosci 14:21–27

    PubMed  CAS  Google Scholar 

  • Bergson C, Mrzljak L, Smiley JF, Pappy M, Levenson R, Goldman-Rakic PS (1995) Regional, cellular, and subcellular variations in the distribution of D1 and D5 dopamine receptors in primate brain. J Neurosci 15:7821–7836

    PubMed  CAS  Google Scholar 

  • Berube-Carriere N, Riad M, Dal Bo G, Trudeau LE, Descarries L (2006) Colocalization of dopamine and glutamate in axon terminals of VTA neurons innervating the nucleus accumbens. Soc Neurosci Abs 722:11

    Google Scholar 

  • Bhalla US, Iyengar R (1999) Emergent properties of networks of biological signaling pathways. Science 283(5400):381–387 (Jan 15)

    PubMed  CAS  Google Scholar 

  • Bi GQ, Poo MM (1998) Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci 18(24):10464–10472 (Dec 15)

    PubMed  CAS  Google Scholar 

  • Bunney BS, Aghajanian GK (1976) Dopamine and norepinephrine innervated cells in the rat prefrontal cortex: pharmacological differentiation using microiontophoretic techniques. Life Sci 19:1783–1789

    PubMed  CAS  Google Scholar 

  • Bymaster FP, Katner JS, Nelson DL, Hemrick-Luecke SK, Threlkeld PG, Heiligenstein JH, Morin SM, Gehlert DR, Perry KW (2002) Atomoxetine increases extracellular levels of norepinephrine and dopamine in prefrontal cortex of rat: a potential mechanism for efficacy in attention deficit/hyperactivity disorder. Neuropsychopharmacology 27:699–711

    PubMed  CAS  Google Scholar 

  • Cagniard B, Balsam PD, Brunner D, Zhuang X (2006) Mice with chronically elevated dopamine exhibit enhanced motivation, but not learning, for a food reward. Neuropsychopharmacology 31(7):1362–1370 (Jul)

    PubMed  CAS  Google Scholar 

  • Caille I, Dumartin B, Bloch B (1996) Ultrastructural localization of D1 dopamine receptor immunoreactivity in rat striatonigral neurons and its relation with dopaminergic innervation. Brain Res 730:17–31

    PubMed  CAS  Google Scholar 

  • Cameron DL, Williams JT (1993) Dopamine D1 receptors facilitate transmitter release. 366(6453):344–347 (Nov 25)

    CAS  Google Scholar 

  • Cannon CM, Palmiter RD (2003) Reward without dopamine. J Neurosci 23:10827–10831

    PubMed  CAS  Google Scholar 

  • Cannon CM, Patel RK (2006) Learning about reward without dopamine: conditioned place preference. Soc Neurosci Abs 485:10

    Google Scholar 

  • Cass WA, Gerhardt GA (1995) In vivo assessment of dopamine uptake in rat medial prefrontal cortex: comparison with dorsal striatum and nucleus accumbens. J Neurochem 65:201–207

    Article  PubMed  CAS  Google Scholar 

  • Ceci A, Brambilla A, Duranti P, Grauert M, Grippa N, Borsini F (1999) Effect of antipsychotic drugs and selective dopaminergic antagonists on dopamine-induced facilitatory activity in prelimbic cortical pyramidal neurons. An in vitro study. Neuroscience 93:107–115

    PubMed  CAS  Google Scholar 

  • Chang HT, Wilson CJ, Kitai ST (1981) Single neostriatal efferent axons in the globus pallidus: a light and electron microscopic study. Science 213:915–918

    PubMed  CAS  Google Scholar 

  • Cheer JF, Heien ML, Garris PA, Carelli RM, Wightman RM (2005) Simultaneous dopamine and single-unit recordings reveal accumbens GABAergic responses: implications for intracranial self-stimulation. Proc Natl Acad Sci USA 102(52):19150–19155 (Dec 27)

    PubMed  CAS  Google Scholar 

  • Chen L, Yang CR (2002) Interaction of dopamine D1 and NMDA receptors mediates acute clozapine potentiation of glutamate EPSPs in rat prefrontal cortex. J Neurophysiol 87(5):2324–2336 (May)

    PubMed  CAS  Google Scholar 

  • Chuhma N, Zhang H, Masson J, Zhuang X, Sulzer D, Hen R, Rayport S (2004) Dopamine neurons mediate a fast excitatory signal via their glutamatergic synapses. J Neurosci 24:972–981

    PubMed  CAS  Google Scholar 

  • Cobb SR, Buhl EH, Halasy K, Paulsen O, Somogyi P (1995) Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378(6552):75–78 (Nov 2)

    PubMed  CAS  Google Scholar 

  • Colbert CM, Johnston D (1996) Axonal action-potential initiation and Na+ channel densities in the soma and axon initial segment of subicular pyramidal neurons. J Neurosci 16:6676–6686

    PubMed  CAS  Google Scholar 

  • Colonnier M (1968) Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study. Brain Res 9:268–287

    PubMed  CAS  Google Scholar 

  • Compte A, Brunel N, Goldman-Rakic PS, Wang XJ (2000) Synaptic mechanisms and network dynamics underlying spatial working memory in a cortical network model. Cereb Cortex 10:910–923

    PubMed  CAS  Google Scholar 

  • Dahlstrom A, Fuxe K (1964) Localization of monoamines in the lower brain stem. Experientia 20:398–399

    PubMed  CAS  Google Scholar 

  • Dal Bo G, St-Gelais F, Danik M, Williams S, Cotton M, Trudeau LE (2004) Dopamine neurons in culture express VGLUT2 explaining their capacity to release glutamate at synapses in addition to dopamine. J Neurochem 88:1398–1405

    Article  CAS  Google Scholar 

  • Dayan P, Kakade S, Montague PR (2000) Learning and selective attention. Nat Neurosci 3 (Suppl):1218–1223 (Nov)

    PubMed  CAS  Google Scholar 

  • Denenberg VH, Kim DS, Palmiter RD (2004) The role of dopamine in learning, memory, and performance of a water escape task. Behav Brain Res 148:73–78

    PubMed  CAS  Google Scholar 

  • Deniau JM, Thierry AM, Feger J (1980) Electrophysiological identification of mesencephalic ventromedial tegmental (VMT) neurons projecting to the frontal cortex, septum and nucleus accumbens. Brain Res 189:315–326

    PubMed  CAS  Google Scholar 

  • Descarries L, Lemay B, Doucet G, Berger B (1987) Regional and laminar density of the dopamine innervation in adult rat cerebral cortex. Neuroscience 21:807–824

    PubMed  CAS  Google Scholar 

  • Devoto P, Flore G, Ibba A, Fratta W, Pani L (2001) Lead intoxication during intrauterine life and lactation but not during adulthood reduces nucleus accumbens dopamine release as studied by brain microdialysis. Toxicol Lett 121:199–206

    PubMed  CAS  Google Scholar 

  • Di Chiara G, Loddo P, Tanda G (1999) Reciprocal changes in prefrontal and limbic dopamine responsiveness to aversive and rewarding stimuli after chronic mild stress: implications for the psychobiology of depression. Biol Psychiatry 46:1624–1633

    PubMed  Google Scholar 

  • Di Ciano P, Cardinal RN, Cowell RA, Little SJ, Everitt BJ (2001) Differential involvement of NMDA, AMPA/kainate, and dopamine receptors in the nucleus accumbens core in the acquisition and performance of pavlovian approach behavior. J Neurosci 21(23):9471–9477 (Dec 1)

    PubMed  Google Scholar 

  • Dong Y, White FJ (2003) Dopamine D1-class receptors selectively modulate a slowly inactivating potassium current in rat medial prefrontal cortex pyramidal neurons. J Neurosci 23:2686–2695

    PubMed  CAS  Google Scholar 

  • Dong Y, Cooper D, Nasif F, Hu XT, White FJ (2004) Dopamine modulates inwardly rectifying potassium currents in medial prefrontal cortex pyramidal neurons. J Neurosci 24:3077–3085

    PubMed  CAS  Google Scholar 

  • Duarte C, Lefebvre C, Chaperon F, Hamon M, Thiebot MH (2003) Effects of a dopamine D3 receptor ligand, BP 897, on acquisition and expression of food-, morphine-, and cocaine-induced conditioned place preference, and food-seeking behavior in rats. Neuropsychopharmacology 28(11):1903–1915 (Nov)

    PubMed  CAS  Google Scholar 

  • Durstewitz D, Seamans JK (2002) The computational role of dopamine D1 receptors in working memory. Neural Netw 15:561–572

    PubMed  Google Scholar 

  • Durstewitz D, Kelc M, Gunturkun O (1999) A neurocomputational theory of the dopaminergic modulation of working memory functions. J Neurosci 19(7):2807–2822 (Apr 1)

    PubMed  CAS  Google Scholar 

  • Durstewitz D, Seamans JK, Sejnowski TJ (2000a) Dopamine-mediated stabilization of delay-period activity in a network model of prefrontal cortex. J Neurophysiol 83:1733–1750

    PubMed  CAS  Google Scholar 

  • Durstewitz D, Seamans JK, Sejnowski TJ (2000b) Neurocomputational models of working memory. Nat Neurosci (Suppl):1184–1191

  • Fallon JH, Loughlin SE (1995) Substantia nigra. In: Paxinos G (ed) The rat nervous system. Academic, San Diego, pp 215–237

    Google Scholar 

  • Feenstra MG, Botterblom MH (1996) Rapid sampling of extracellular dopamine in the rat prefrontal cortex during food consumption, handling and exposure to novelty. Brain Res 742:17–24

    PubMed  CAS  Google Scholar 

  • Ferron A, Thierry AM, Le Douarin C, Glowinski J (1984) Inhibitory influence of the mesocortical dopaminergic system on spontaneous activity or excitatory response induced from the thalamic mediodorsal nucleus in the rat medial prefrontal cortex. Brain Res 302:257–265

    PubMed  CAS  Google Scholar 

  • Fiorillo CD, Tobler PN, Schultz W (2003) Discrete coding of reward probability and uncertainty by dopamine neurons. Science 299(5614):1898–1902

    PubMed  CAS  Google Scholar 

  • Fitch TE, Sahr RN, Eastwood BJ, Zhou FC, Yang CR (2006) Dopamine D1/5 receptor modulation of firing rate and bidirectional theta burst firing in medial septal/vertical limb of diagonal band neurons in vivo. J Neurophysiol 95(5):2808–2820 (May)

    PubMed  CAS  Google Scholar 

  • Floresco SB, Blaha CD, Yang CR, Phillips AG (2001a) Modulation of hippocampal and amygdalar-evoked activity of nucleus accumbens neurons by dopamine: cellular mechanisms of input selection. J Neurosci 21:2851–2860

    PubMed  CAS  Google Scholar 

  • Floresco SB, Blaha CD, Yang CR, Phillips AG (2001b) Dopamine D1 and NMDA receptors mediate potentiation of basolateral amygdala evoked firing of nucleus accumbens neurons. J Neurosci 21:6370–6376

    PubMed  CAS  Google Scholar 

  • Fremeau RT Jr, Burman J, Qureshi T, Tran CH, Proctor J, Johnson J, Zhang H, Sulzer D, Copenhagen DR, Storm-Mathisen J, Reimer RJ, Chaudhry FA, Edwards RH (2002) The identification of vesicular glutamate transporter 3 suggests novel modes of signaling by glutamate. Proc Natl Acad Sci USA 99:14488–14493

    PubMed  CAS  Google Scholar 

  • Fremeau RT Jr, Voglmaier S, Seal RP, Edwards RH (2004) VGLUTs define subsets of excitatory neurons and suggest novel roles for glutamate. Trends Neurosci 27:98–103

    PubMed  CAS  Google Scholar 

  • Fricker D, Miles R (2001) Interneurons, spike timing, and perception. Neuron 32(5):771–774 (Dec 6)

    PubMed  CAS  Google Scholar 

  • Funahashi S, Bruce CJ, Goldman-Rakic PS (1989) Mnemonic coding of visual space in the monkey’s dorsolateral prefrontal cortex. J Neurophysiol 61:331–349

    PubMed  CAS  Google Scholar 

  • Gao WJ, Goldman-Rakic PS (2003) Selective modulation of excitatory and inhibitory microcircuits by dopamine. Proc Natl Acad Sci USA 100:2836–2841

    PubMed  CAS  Google Scholar 

  • Gao WJ, Krimer LS, Goldman-Rakic PS (2001) Presynaptic regulation of recurrent excitation by D1 receptors in prefrontal circuits. Proc Natl Acad Sci USA 98:295–300

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Garris PA, Collins LB, Jones SR, Wightman RM (1993) Evoked extracellular dopamine in vivo in the medial prefrontal cortex. J Neurochem 61:637–647

    Article  PubMed  CAS  Google Scholar 

  • Gauthier J, Parent M, Levesque M, Parent A (1999) The axonal arborization of single nigrostriatal neurons in rats. Brain Res 834:228–232

    PubMed  CAS  Google Scholar 

  • Glowinski J, Tassin JP, Thierry AM (1984) The mesocortico-prefrontal dopaminergic neurons. Trends Neurosci 7:415–418

    Google Scholar 

  • Godbout R, Mantz J, Pirot S, Glowinski J, Thierry AM (1991) Inhibitory influence of the mesocortical dopaminergic neurons on their target cells: electrophysiological and pharmacological characterization. J Pharmacol Exp Ther 258:728–738

    PubMed  CAS  Google Scholar 

  • Gogan P, Gueritaud JP, Tyc-Dumont S (1983) Comparison of antidromic and orthodromic action potentials of identified motor axons in the cat’s brain stem. J Physiol 335:205–220

    PubMed  CAS  Google Scholar 

  • Goldman-Rakic PS (1995) Cellular basis of working memory. Neuron 14:477–485

    PubMed  CAS  Google Scholar 

  • Goldman-Rakic PS, Muly EC 3rd, Williams GV (2000) D(1) receptors in prefrontal cells and circuits. Brain Res Brain Res Rev 31:295–301

    PubMed  CAS  Google Scholar 

  • Gonzalez-Burgos G, Kroener S, Seamans JK, Lewis DA, Barrionuevo G (2005) Dopaminergic modulation of short-term synaptic plasticity in fast-spiking interneurons of primate dorsolateral prefrontal cortex. J Neurophysiol 94:4168–4177

    PubMed  CAS  Google Scholar 

  • Gorelova NA, Yang CR (2000) Dopamine D1/D5 receptor activation modulates a persistent sodium current in rat prefrontal cortical neurons in vitro. J Neurophysiol 84:75–87

    PubMed  CAS  Google Scholar 

  • Gorelova N, Seamans JK, Yang CR (2002) Mechanisms of dopamine activation of fast-spiking interneurons that exert inhibition in rat prefrontal cortex. J Neurophysiol 88:3150–3166

    PubMed  CAS  Google Scholar 

  • Grace AA (1991) Phasic versus tonic dopamine release and the modulation of dopamine system responsivity: a hypothesis for the etiology of schizophrenia. Neuroscience 41:1–24

    PubMed  CAS  Google Scholar 

  • Grace AA (2000) The tonic/phasic model of dopamine system regulation and its implications for understanding alcohol and psychostimulant craving. Addiction 95 (Suppl 2):S119–S128

    PubMed  Google Scholar 

  • Grace AA, Bunney BS (1984a) The control of firing pattern in nigral dopamine neurons: burst firing. J Neurosci 4:2877–2890

    PubMed  CAS  Google Scholar 

  • Grace AA, Bunney BS (1984b) The control of firing pattern in nigral dopamine neurons: single spike firing. J Neurosci 4:2866–2876

    PubMed  CAS  Google Scholar 

  • Gras C, Herzog E, Bellenchi GC, Bernard V, Ravassard P, Pohl M, Gasnier B, Giros B, El Mestikawy S (2002) A third vesicular glutamate transporter expressed by cholinergic and serotoninergic neurons. J Neurosci 22:5442–5451

    PubMed  CAS  Google Scholar 

  • Gray EG (1959) Electron microscopy of synaptic contacts on dendrite spines of the cerebral cortex. Nature 183:1592–1593

    PubMed  CAS  Google Scholar 

  • Greengard P (2001) The neurobiology of dopamine signaling. Biosci Rep 21(3):247–269 Jun

    PubMed  CAS  Google Scholar 

  • Gribkoff VK, Ashe JH (1984) Modulation by dopamine of population responses and cell membrane properties of hippocampal CA1 neurons in vitro. Brain Res 292(2):327–338 (Feb 6)

    PubMed  CAS  Google Scholar 

  • Gulledge AT, Jaffe DB (2001) Multiple effects of dopamine on layer V pyramidal cell excitability in rat prefrontal cortex. J Neurophysiol 86:586–595

    PubMed  CAS  Google Scholar 

  • Guyenet PG, Aghajanian GK (1978) Antidromic identification of dopaminergic and other output neurons of the rat substantia nigra. Brain Res 150:69–84

    PubMed  CAS  Google Scholar 

  • Hara Y, Pickel VM (2005) Overlapping intracellular and differential synaptic distributions of dopamine D1 and glutamate N-methyl-D-aspartate receptors in rat nucleus accumbens. J Comp Neurol 492:442–455

    PubMed  CAS  Google Scholar 

  • Hausser M, Stuart G, Racca C, Sakmann B (1995) Axonal initiation and active dendritic propagation of action potentials in substantia nigra neurons. Neuron 15:637–647

    PubMed  CAS  Google Scholar 

  • Henze DA, Gonzalez-Burgos GR, Urban NN, Lewis DA, Barrionuevo G (2000) Dopamine increases excitability of pyramidal neurons in primate prefrontal cortex. J Neurophysiol 84:2799–2809

    PubMed  CAS  Google Scholar 

  • Hernandez L, Hoebel BG (1995) Chronic clozapine selectively decreases prefrontal cortex dopamine as shown by simultaneous cortical, accumbens, and striatal microdialysis in freely moving rats. Pharmacol Biochem Behav 52:581–589

    PubMed  CAS  Google Scholar 

  • Herzog E, Gilchrist J, Gras C, Muzerelle A, Ravassard P, Giros B, Gaspar P, El Mestikawy S (2004) Localization of VGLUT3, the vesicular glutamate transporter type 3, in the rat brain. Neuroscience 123:983–1002

    PubMed  CAS  Google Scholar 

  • Heusner CL, Hnasko TS, Szczypka MS, Liu Y, During MJ, Palmiter RD (2003) Viral restoration of dopamine to the nucleus accumbens is sufficient to induce a locomotor response to amphetamine. Brain Res 980:266–274

    PubMed  CAS  Google Scholar 

  • Hildebrand BE, Nomikos GG, Hertel P, Schilstrom B, Svensson TH (1998) Reduced dopamine output in the nucleus accumbens but not in the medial prefrontal cortex in rats displaying a mecamylamine-precipitated nicotine withdrawal syndrome. Brain Res 779:214–225

    PubMed  CAS  Google Scholar 

  • Hioki H, Fujiyama F, Nakamura K, Wu SX, Matsuda W, Kaneko T (2004) Chemically specific circuit composed of vesicular glutamate transporter 3- and preprotachykinin B-producing interneurons in the rat neocortex. Cereb Cortex 14:1266–1275

    PubMed  Google Scholar 

  • Hnasko TS, Sotak BN, Palmiter RD (2005) Morphine reward in dopamine-deficient mice. Nature 438:854–857

    PubMed  CAS  Google Scholar 

  • Holroyd CB, Coles MG (2002) The neural basis of human error processing: reinforcement learning, dopamine, and the error-related negativity. Psychol Rev 109:679–709

    PubMed  Google Scholar 

  • Holroyd CB, Nieuwenhuis S, Yeung N, Cohen JD (2003) Errors in reward prediction are reflected in the event-related brain potential. Neuroreport 14:2481–2484

    PubMed  Google Scholar 

  • Huang YY, Kandel ER (1995) D1/D5 receptor agonists induce a protein synthesis-dependent late potentiation in the CA1 region of the hippocampus. Proc Natl Acad Sci USA 92(7):2446–2450 (Mar 28)

    PubMed  CAS  Google Scholar 

  • Hull CD, Bernardi G, Price DD, Buchwald NA (1973) Intracellular responses of caudate neurons to temporally and spatially combined stimuli. Exp Neurol 38:324–336

    PubMed  CAS  Google Scholar 

  • Hur EE, Zaborszky L (2005) Vglut2 afferents to the medial prefrontal and primary somatosensory cortices: a combined retrograde tracing in situ hybridization. J Comp Neurol 483:351–373

    PubMed  Google Scholar 

  • Ihalainen JA, Riekkinen P Jr, Feenstra MG (1999) Comparison of dopamine and noradrenaline release in mouse prefrontal cortex, striatum and hippocampus using microdialysis. Neurosci Lett 277:71–74

    PubMed  CAS  Google Scholar 

  • Izaki Y, Hori K, Nomura M (1998) Dopamine and acetylcholine elevation on lever-press acquisition in rat prefrontal cortex. Neurosci Lett 258:33–36

    PubMed  CAS  Google Scholar 

  • Kaneko T, Fujiyama F (2002) Complementary distribution of vesicular glutamate transporters in the central nervous system. Neurosci Res 42:243–250

    PubMed  CAS  Google Scholar 

  • Kawano M, Kawasaki A, Sakata-Haga H, Fukui Y, Kawano H, Nogami H, Hisano S (2006) Particular subpopulations of midbrain and hypothalamic dopamine neurons express vesicular glutamate transporter 2 in the rat brain. J Comp Neurol 498:581–592

    PubMed  CAS  Google Scholar 

  • Kiyatkin EA, Stein EA (1995) Fluctuations in nucleus accumbens dopamine during cocaine self-administration behavior: an in vivo electrochemical study. Neuroscience 64:599–617

    PubMed  CAS  Google Scholar 

  • Kiyatkin EA, Zhukov VN (1988) Impulse activity of mesencephalic neurons on nociceptive stimulation in awake rats. Neurosci Behav Physiol 18:393–400

    PubMed  CAS  Google Scholar 

  • Kocsis JD, Kitai ST (1977) Dual excitatory inputs to caudate spiny neurons from substantia nigra stimulation. Brain Res 138:271–283

    PubMed  CAS  Google Scholar 

  • Kroener S, Krimer LS, Lewis DA, Barrionuevo G (2006) Dopamine increases inhibition in the monkey dorsolateral prefrontal cortex through cell type-specific modulation of interneurons. Cereb Cortex (in press)

  • Lavin A, Grace AA (2001) Stimulation of D1-type dopamine receptors enhances excitability in prefrontal cortical pyramidal neurons in a state-dependent manner. Neuroscience 104:335–346

    PubMed  CAS  Google Scholar 

  • Lavin A, Nogueira L, Lapish CC, Wightman RM, Phillips PE, Seamans JK (2005) Mesocortical dopamine neurons operate in distinct temporal domains using multimodal signaling. J Neurosci 25:5013–5023

    PubMed  CAS  Google Scholar 

  • Lewis BL, O’Donnell P (2000) Ventral tegmental area afferents to the prefrontal cortex maintain membrane potential ‘up’ states in pyramidal neurons via D(1) dopamine receptors. Cereb Cortex 10:1168–1175

    PubMed  CAS  Google Scholar 

  • Lindvall O, Bjorklund A, Skagerberg G (1984) Selective histochemical demonstration of dopamine terminal systems in rat di- and telencephalon: new evidence for dopaminergic innervation of hypothalamic neurosecretory nuclei. Brain Res 306:19–30

    PubMed  CAS  Google Scholar 

  • Ljungberg T, Apicella P, Schultz W (1992) Responses of monkey dopamine neurons during learning of behavioral reactions. J Neurophysiol 67:145–163

    PubMed  CAS  Google Scholar 

  • Mantz J, Godbout R, Pirot S, Glowinski J, Thierry AM (1992) Inhibitory effects of mesocortical dopaminergic neurons on their target cells: electrophysiological and pharmacological characterization. Neurochem Int 20 (Suppl):251S–254S

    PubMed  CAS  Google Scholar 

  • Margolis EB, Lock H, Chefer VI, Shippenberg TS, Hjelmstad GO, Fields HL (2006) {kappa} opioids selectively control dopaminergic neurons projecting to the prefrontal cortex. Proc Natl Acad Sci USA (Feb 13; in press)

  • Matsuda Y, Marzo A, Otani S (2006) The presence of background dopamine signal converts long-term synaptic depression to potentiation in rat prefrontal cortex. J Neurosci 26(18):4803–4810 (May 3)

    PubMed  CAS  Google Scholar 

  • Meador-Woodruff JH, Mansour A, Bunzow JR, Van Tol HH, Watson SJ Jr, Civelli O (1989) Distribution of D2 dopamine receptor mRNA in rat brain. Proc Natl Acad Sci USA 86:7625–7628

    PubMed  CAS  Google Scholar 

  • Mercuri N, Calabresi P, Stanzione P, Bernardi G (1985) Electrical stimulation of mesencephalic cell groups (A9-A10) produces monosynaptic excitatory potentials in rat frontal cortex. Brain Res 338:192–195

    PubMed  CAS  Google Scholar 

  • Miller EK, Cohen JD (2001) An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24:167–202

    PubMed  CAS  Google Scholar 

  • Montague PR, Dayan P, Sejnowski TJ (1996) A framework for mesencephalic dopamine systems based on predictive Hebbian learning. J Neurosci 16:1936–1947 (Review)

    PubMed  CAS  Google Scholar 

  • Mora F, Sweeney KF, Rolls ET, Sanguinetti AM (1976) Spontaneous firing rate of neurones in the prefrontal cortex of the rat: evidence for a dopaminergic inhibition. Brain Res 116:516–522

    PubMed  CAS  Google Scholar 

  • Moron JA, Brockington A, Wise RA, Rocha BA, Hope BT (2002) Dopamine uptake through the norepinephrine transporter in brain regions with low levels of the dopamine transporter: evidence from knock-out mouse lines. J Neurosci 22:389–395

    PubMed  CAS  Google Scholar 

  • Mundorf ML, Joseph JD, Austin CM, Caron MG, Wightman RM (2001) Catecholamine release and uptake in the mouse prefrontal cortex. J Neurochem 79:130–142

    Google Scholar 

  • Negyessy L, Goldman-Rakic PS (2005) Subcellular localization of the dopamine D2 receptor and coexistence with the calcium-binding protein neuronal calcium sensor-1 in the primate prefrontal cortex. J Comp Neurol 488:464–475

    PubMed  CAS  Google Scholar 

  • Nishi A, Bibb JA, Matsuyama S, Hamada M, Higashi H, Nairn AC, Greengard P (2002) Regulation of DARPP-32 dephosphorylation at PKA- and Cdk5-sites by NMDA and AMPA receptors: distinct roles of calcineurin and protein phosphatase-2A. J Neurochem 81(4):832–841 (May)

    PubMed  CAS  Google Scholar 

  • Nishi A, Watanabe Y, Higashi H, Tanaka M, Nairn AC, Greengard P (2005) Glutamate regulation of DARPP-32 phosphorylation in neostriatal neurons involves activation of multiple signaling cascades. Proc Natl Acad Sci USA 102(4):1199–1204 (Jan 25)

    PubMed  CAS  Google Scholar 

  • Parfitt KD, Gratton A, Bickford-Wimer PC (1990) Electrophysiological effects of selective D1 and D2 dopamine receptor agonists in the medial prefrontal cortex of young and aged Fischer 344 rats. J Pharmacol Exp Ther 254:539–545

    PubMed  CAS  Google Scholar 

  • Penit-Soria J, Audinat E, Crepel F (1987) Excitation of rat prefrontal cortical neurons by dopamine: an in vitro electrophysiological study. Brain Res 425:263–274

    PubMed  CAS  Google Scholar 

  • Phillips PE, Stuber GD, Heien ML, Wightman RM, Carelli RM (2003) Subsecond dopamine release promotes cocaine seeking. Nature 422:614–618

    PubMed  CAS  Google Scholar 

  • Phillips AG, Ahn S, Floresco SB (2004) Magnitude of dopamine release in medial prefrontal cortex predicts accuracy of memory on a delayed response task. J Neurosci 24(2):547–553

    PubMed  CAS  Google Scholar 

  • Pirot S, Godbout R, Mantz J, Tassin JP, Glowinski J, Thierry AM (1992) Inhibitory effects of ventral tegmental area stimulation on the activity of prefrontal cortical neurons: evidence for the involvement of both dopaminergic and GABAergic components. Neuroscience 49:857–865

    PubMed  CAS  Google Scholar 

  • Porrino LJ, Goldman-Rakic PS (1982) Brainstem innervation of prefrontal and anterior cingulate cortex in the rhesus monkey revealed by retrograde transport of HRP. J Comp Neurol 205:63–76

    PubMed  CAS  Google Scholar 

  • Prensa L, Parent A (2001) The nigrostriatal pathway in the rat: A single-axon study of the relationship between dorsal and ventral tier nigral neurons and the striosome/matrix striatal compartments. J Neurosci 21:7247–7260

    PubMed  CAS  Google Scholar 

  • Preston RJ, McCrea RA, Chang HT, Kitai ST (1981) Anatomy and physiology of substantia nigra and retrorubral neurons studied by extra- and intracellular recording and by horseradish peroxidase labeling. Neuroscience 6:331–344

    PubMed  CAS  Google Scholar 

  • Redgrave P, Prescott TJ, Gurney K (1999) Is the short-latency dopamine response too short to signal reward error? Trends Neurosci 22:146–151

    PubMed  CAS  Google Scholar 

  • Robinson S, Sandstrom SM, Denenberg VH, Palmiter RD (2005) Distinguishing whether dopamine regulates liking, wanting, and/or learning about rewards. Behav Neurosci 119(1):5–15 (Feb)

    PubMed  CAS  Google Scholar 

  • Rompre PP, Wise RA (1989) Behavioral evidence for midbrain dopamine depolarization inactivation. Brain Res 477:152–156

    PubMed  CAS  Google Scholar 

  • Salamone JD, Correa M, Mingote SM, Weber SM (2005) Beyond the reward hypothesis: alternative functions of nucleus accumbens dopamine. Curr Opin Pharmacol 5:34–41

    PubMed  CAS  Google Scholar 

  • Schafer MK, Varoqui H, Defamie N, Weihe E, Erickson JD (2002) Molecular cloning and functional identification of mouse vesicular glutamate transporter 3 and its expression in subsets of novel excitatory neurons. J Biol Chem 277:50734–50748

    PubMed  Google Scholar 

  • Schultz W (1998a) The phasic reward signal of primate dopamine neurons. Adv Pharmacol 42:686–690

    PubMed  CAS  Google Scholar 

  • Schultz W (1998b) Predictive reward signal of dopamine neurons. J Neurophysiol 80:1–27

    PubMed  CAS  Google Scholar 

  • Schultz W (2002) Getting formal with dopamine and reward. Neuron 36:241–263

    PubMed  CAS  Google Scholar 

  • Schultz W, Romo R (1990) Dopamine neurons of the monkey midbrain: contingencies of responses to stimuli eliciting immediate behavioral reactions. J Neurophysiol 63:607–624

    PubMed  CAS  Google Scholar 

  • Schultz W, Apicella P, Ljungberg T, Romo R, Scarnati E (1993a) Reward-related activity in the monkey striatum and substantia nigra. Prog Brain Res 99:227–235

    PubMed  CAS  Google Scholar 

  • Schultz W, Apicella P, Ljungberg T (1993b) Responses of monkey dopamine neurons to reward and conditioned stimuli during successive steps of learning a delayed response task. J Neurosci 13:900–913

    PubMed  CAS  Google Scholar 

  • Schultz W, Dayan P, Montague PR (1997) A neural substrate of prediction and reward. Science 275:1593–1599

    PubMed  CAS  Google Scholar 

  • Seamans JK, Yang CR (2004) The principal features and mechanisms of dopamine modulation in the prefrontal cortex. Prog Neurobiol 74:1–58

    PubMed  CAS  Google Scholar 

  • Seamans JK, Durstewitz D, Christie BR, Stevens CF, Sejnowski TJ (2001a) Dopamine D1/D5 receptor modulation of excitatory synaptic inputs to layer V prefrontal cortex neurons. Proc Natl Acad Sci USA 98:301–306

    PubMed  CAS  Google Scholar 

  • Seamans JK, Gorelova N, Durstewitz D, Yang CR (2001b) Bidirectional dopamine modulation of GABAergic inhibition in prefrontal cortical pyramidal neurons. J Neurosci 21:3628–3638

    PubMed  CAS  Google Scholar 

  • Seamans JK, Nogueira L, Lavin A (2003) Synaptic basis of persistent activity in prefrontal cortex in vivo and in organotypic cultures. Cereb Cortex 13:1242–1250

    PubMed  Google Scholar 

  • Seguela P, Watkins KC, Descarries L (1988) Ultrastructural features of dopamine axon terminals in the anteromedial and the suprarhinal cortex of adult rat. Brain Res 442:11–22

    PubMed  CAS  Google Scholar 

  • Sesack SR, Bunney BS (1989) Pharmacological characterization of the receptor mediating electrophysiological responses to dopamine in the rat medial prefrontal cortex: a microiontophoretic study. J Pharmacol Exp Ther 248:1323–1333

    PubMed  CAS  Google Scholar 

  • Sesack SR, Aoki C, Pickel VM (1994) Ultrastructural localization of D2 receptor-like immunoreactivity in midbrain dopamine neurons and their striatal targets. J Neurosci 14:88–106

    PubMed  CAS  Google Scholar 

  • Sesack SR, Hawrylak VA, Guido MA, Levey AI (1998) Cellular and subcellular localization of the dopamine transporter in rat cortex. Adv Pharmacol 42:171–174

    PubMed  CAS  Google Scholar 

  • Shi WX, Zheng P, Liang XF, Bunney BS (1997) Characterization of dopamine-induced depolarization of prefrontal cortical neurons. Synapse 26:415–422

    PubMed  CAS  Google Scholar 

  • Shoblock JR, Sullivan EB, Maisonneuve IM, Glick SD (2003) Neurochemical and behavioral differences between d-methamphetamine and d-amphetamine in rats. Psychopharmacology (Berl) 165:359–369

    CAS  Google Scholar 

  • Siggins GR (1978) Electrophysiological role of dopamine in the striatum: excitatory or inhibitory? In: Lipton MA, DiMascio A, Killam KF (eds) Psychopharmacology: a generation of progress. Raven, New York, pp 143–157

    Google Scholar 

  • Smiley JF, Goldman-Rakic PS (1993) Heterogeneous targets of dopamine synapses in monkey prefrontal cortex demonstrated by serial section electron microscopy: a laminar analysis using the silver-enhanced diaminobenzidine sulfide (SEDS) immunolabeling technique. Cereb Cortex 3:223–238

    PubMed  CAS  Google Scholar 

  • Smiley JF, Levey AI, Ciliax BJ, Goldman-Rakic PS (1994) D1 dopamine receptor immunoreactivity in human and monkey cerebral cortex: predominant and extrasynaptic localization in dendritic spines. Proc Natl Acad Sci USA 91:5720–5724

    PubMed  CAS  Google Scholar 

  • Sotak BN, Hnasko TS, Robinson S, Kremer EJ, Palmiter RD (2005) Dysregulation of dopamine signaling in the dorsal striatum inhibits feeding. Brain Res 1061:88–96

    PubMed  CAS  Google Scholar 

  • Spyraki C, Fibiger HC, Phillips AG (1982) Dopaminergic substrates of amphetamine-induced place preference conditioning. Brain Res 253(1–2):185–193 (Dec 16)

    PubMed  CAS  Google Scholar 

  • Sulzer D, Joyce MP, Lin L, Geldwert D, Haber SN, Hattori T, Rayport S (1998) Dopamine neurons make glutamatergic synapses in vitro. J Neurosci 18:4588–4602

    PubMed  CAS  Google Scholar 

  • Suri RE, Schultz W (1999) A neural network model with dopamine-like reinforcement signal that learns a spatial delayed response task. Neuroscience 91:871–890

    PubMed  CAS  Google Scholar 

  • Swanson LW (1982) The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res Bull 9(1–6):321–353

    Google Scholar 

  • Szabadics J, Varga C, Molnár G, Oláh S, Barzó P, Tamás G (2006) Excitatory effect of GABAergic axo-axonic cells in cortical microcircuits. Science 311:233–235

    PubMed  CAS  Google Scholar 

  • Tamas G, Buhl EH, Lorincz A, Somogyi P (2000) Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons. Nat Neurosci 3:366–371

    PubMed  CAS  Google Scholar 

  • Tepper JM, Sawyer SF, Groves PM (1987) Electrophysiologically identified nigral dopaminergic neurons intracellularly labeled with HRP: light-microscopic analysis. J Neurosci 7:2794–2806

    PubMed  CAS  Google Scholar 

  • Thierry AM, Deniau JM, Herve D, Chevalier G (1980) Electrophysiological evidence for non-dopaminergic mesocortical and mesolimbic neurons in the rat. Brain Res 201:210–214

    PubMed  CAS  Google Scholar 

  • Thierry AM, Pirot S, Gioanni Y, Glowinski J (1998) Dopamine function in the prefrontal cortex. Adv Pharmacol 42:717–720

    Article  PubMed  CAS  Google Scholar 

  • Tobler PN, Fiorillo CD, Schultz W (2005) Adaptive coding of reward value by dopamine neurons. Science 307:1642–1645

    PubMed  CAS  Google Scholar 

  • Trantham-Davidson H, Neely LC, Lavin A, Seamans JK (2004) Mechanisms underlying differential D1 versus D2 dopamine receptor regulation of inhibition in prefrontal cortex. J Neurosci 24:10652–10659

    PubMed  CAS  Google Scholar 

  • Tseng KY, O’Donnell P (2004) Dopamine-glutamate interactions controlling prefrontal cortical pyramidal cell excitability involve multiple signaling mechanisms. J Neurosci 24:5131–5139

    PubMed  CAS  Google Scholar 

  • Tseng KY, Mallet N, Toreson KL, Le Moine C, Gonon F, O’Donnell P (2006) Excitatory response of prefrontal cortical fast-spiking interneurons to ventral tegmental area stimulation in vivo. Synapse 59:412–417

    PubMed  CAS  Google Scholar 

  • Umemiya M, Raymond LA (1997) Dopaminergic modulation of excitatory postsynaptic currents in rat neostriatal neurons. J Neurophysiol 78(3):1248–1255 (Sep)

    PubMed  CAS  Google Scholar 

  • Ungless MA (2004) Dopamine: the salient issue. Trends Neurosci 27(12):702–706

    PubMed  CAS  Google Scholar 

  • Ungless MA, Magill PJ, Bolam JP (2004) Uniform inhibition of dopamine neurons in the ventral tegmental area by aversive stimuli. Science 303:2040–2042

    PubMed  CAS  Google Scholar 

  • Urban NN, Gonzalez-Burgos G, Henze DA, Lewis DA, Barrionuevo G (2002) Selective reduction by dopamine of excitatory synaptic inputs to pyramidal neurons in primate prefrontal cortex. J Physiol 539(Pt 3):707–712 (Mar 15)

    PubMed  CAS  Google Scholar 

  • VanVeen V, Carter CS (2002) The anterior cingulate as a conflict monitor: fMRI and ERP studies. Physiol Behav 77:477–482

    CAS  Google Scholar 

  • Volkow ND, Wang GJ, Fowler JS, Ding YS (2005) Imaging the effects of methylphenidate on brain dopamine: new model on its therapeutic actions for attention-deficit/hyperactivity disorder. Biol Psychiatry 57(11):1410–1415

    PubMed  CAS  Google Scholar 

  • Waelti P, Dickinson A, Schultz W (2001) Dopamine responses comply with basic assumptions of formal learning theory. Nature 412(6842):43–48 (Jul 5)

    PubMed  CAS  Google Scholar 

  • Wang J, O’Donnell P (2001) D(1) dopamine receptors potentiate NMDA-mediated excitability increase in layer V prefrontal cortical pyramidal neurons. Cereb Cortex 11:452–462

    PubMed  CAS  Google Scholar 

  • Wayment HK, Schenk JO, Sorg BA (2001) Characterization of extracellular dopamine clearance in the medial prefrontal cortex: role of monoamine uptake and monoamine oxidase inhibition. J Neurosci 21:35–44

    PubMed  CAS  Google Scholar 

  • Williams GV, Millar J (1990) Concentration-dependent actions of stimulated dopamine release on neuronal activity in rat striatum. Neuroscience 39:1–16

    PubMed  CAS  Google Scholar 

  • Williams GV, Goldman-Rakic PS (1995) Modulation of memory fields by dopamine D1 receptors in prefrontal cortex. Nature 376(6541):572–575 (Aug 17)

    PubMed  CAS  Google Scholar 

  • Williams SM, Goldman-Rakic PS (1998) Widespread origin of the primate mesofrontal dopamine system. Cereb Cortex 8:321–345

    PubMed  CAS  Google Scholar 

  • Winterer G, Weinberger DR (2004) Genes, dopamine and cortical signal-to-noise ratio in schizophrenia. Trends Neurosci 27:683–690

    PubMed  CAS  Google Scholar 

  • Wise RA (2005) Forebrain substrates of reward and motivation. J Comp Neurol 493:115–121

    PubMed  CAS  Google Scholar 

  • Wu J, Hablitz JJ (2005) Cooperative activation of D1 and D2 dopamine receptors enhances a hyperpolarization-activated inward current in layer I interneurons. J Neurosci 25:6322–6328

    PubMed  CAS  Google Scholar 

  • Yang SN (2000) Sustained enhancement of AMPA receptor- and NMDA receptor-mediated currents induced by dopamine D1/D5 receptor activation in the hippocampus: an essential role of postsynaptic Ca2+. Hippocampus 10(1):57–63

    PubMed  CAS  Google Scholar 

  • Yang CR, Chen L (2005) Targeting prefrontal cortical dopamine D1 and N-methyl-D-aspartate receptor interactions in schizophrenia treatment. Neuroscientist 11(5):452–470 (Oct)

    PubMed  CAS  Google Scholar 

  • Yang CR, Seamans JK (1996) Dopamine D1 receptor actions in layers V-VI rat prefrontal cortex neurons in vitro: modulation of dendritic-somatic signal integration. J Neurosci 16:1922–1935

    PubMed  CAS  Google Scholar 

  • Young CE, Yang CR (2005) Dopamine D1-like receptor modulates layer- and frequency-specific short-term synaptic plasticity in rat prefrontal cortical neurons. Eur J Neurosci 21(12):3310–3320 (Jun)

    PubMed  Google Scholar 

  • Zheng P, Zhang XX, Bunney BS, Shi WX (1999) Opposite modulation of cortical N-methyl-D-aspartate receptor-mediated responses by low and high concentrations of dopamine. Neuroscience 91:527–535

    PubMed  CAS  Google Scholar 

  • Zhou FM, Hablitz JJ (1999) Dopamine modulation of membrane and synaptic properties of interneurons in rat cerebral cortex. J Neurophysiol 81:967–976

    PubMed  CAS  Google Scholar 

  • Zoli M, Torri C, Ferrari R, Jansson A, Zini I, Fuxe K, Agnati LF (1998) The emergence of the volume transmission concept. Brain Res Brain Res Rev 26:136–147

    PubMed  CAS  Google Scholar 

Download references

Acknowledgement

This work was supported by the National Institutes of Health (C06 RR015455), from the Extramural Research Facilities Program of the National Center for Research Resources, and NIDA 14698 (AL).

Author information

Authors and Affiliations

  1. Department of Neurosciences, Medical University of South Carolina, Suite 430 BSB 173 Ashley, Charleston, SC, USA

    Christopher C. Lapish, Sven Kroener & Antonieta Lavin

  2. Centre for Theoretical and Computational Neuroscience, University of Plymouth, Plymouth, United Kingdom

    Daniel Durstewitz

  3. Brain Research Centre, University of British Columbia, Vancouver, British Columbia, Canada

    Jeremy K. Seamans

Authors
  1. Christopher C. Lapish
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sven Kroener
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Daniel Durstewitz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Antonieta Lavin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jeremy K. Seamans
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christopher C. Lapish.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lapish, C.C., Kroener, S., Durstewitz, D. et al. The ability of the mesocortical dopamine system to operate in distinct temporal modes. Psychopharmacology 191, 609–625 (2007). https://doi.org/10.1007/s00213-006-0527-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00213-006-0527-8

Keywords

Search

Navigation