Prolonged and Extrasynaptic Excitatory Action of Dopamine Mediated by D1 Receptors in the Rat Striatum In Vivo

The spatiotemporal characteristics of the dopaminergic transmission mediated by D1 receptors were investigated in vivo. For this purpose dopamine (DA) release was evoked in the striatum of anesthetized rats by train electrical stimulations of the medial forebrain bundle (one to four pulses at 15 Hz), which mimicked the spontaneous activity of dopaminergic neurons. The resulting dopamine overflow was electrochemically monitored in real time in the extracellular space. This evoked DA release induced a delayed increase in discharge activity in a subpopulation of single striatal neurons. This excitation was attributable to stimulation of D1 receptors by released DA because it was abolished by acute 6-hydroxydopamine lesion and strongly reduced by the D1 antagonist SCH 23390. Striatal neurons exhibiting this delayed response were also strongly excited by intravenous administration of the D1 agonist SKF 82958. Whereas the DA overflow was closely time-correlated with stimulation, the excitatory response mediated by DA started 200 msec after release and lasted for up to 1 sec. Moreover, functional evidence presented here combined with previous morphological data show that D1 receptors are stimulated by DA diffusing up to 12 μm away from release sites in the extrasynaptic extracellular space. In conclusion, DA released by bursts of action potentials exerts, via D1 receptors, a delayed and prolonged excitatory influence on target neurons. This phasic transmission occurs outside synaptic clefts but still exhibits a high degree of spatial specificity.

[1]  D. Purpura,et al.  Electrophysiological analysis of reciprocal caudato-nigral relations. , 1967, Brain research.

[2]  A. Grace,et al.  The control of firing pattern in nigral dopamine neurons: burst firing , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  R. Nicoll,et al.  Characterization of a slow cholinergic post‐synaptic potential recorded in vitro from rat hippocampal pyramidal cells. , 1984, The Journal of physiology.

[4]  François Gonon,et al.  In vivo electrochemical monitoring of apomorphine penetration into the rat brain , 1985, Neuroscience Letters.

[5]  Charles Nicholson,et al.  Diffusion from an injected volume of a substance in brain tissue with arbitrary volume fraction and tortuosity , 1985, Brain Research.

[6]  L. Descarries,et al.  Quantification of the dopamine innervation in adult rat neostriatum , 1986, Neuroscience.

[7]  B. Bunney,et al.  Activity of A9 and A10 dopaminergic neurons in unrestrained rats: further characterization and effects of apomorphine and cholecystokinin , 1987, Brain Research.

[8]  Akinori Akaike,et al.  Excitatory and inhibitory effects of dopamine on neuronal activity of the caudate nucleus neurons in vitro , 1987, Brain Research.

[9]  P. Calabresi,et al.  Intracellular studies on the dopamine-induced firing inhibition of neostriatal neurons in vitro: Evidence for D1 receptor involvement , 1987, Neuroscience.

[10]  J. Williams,et al.  Inhibitory synaptic potentials recorded from mammalian neurones prolonged by blockade of noradrenaline uptake. , 1987, The Journal of physiology.

[11]  S. Nahorski,et al.  Endogenous Dopamine Functionally Activates D‐1 and D‐2 Receptors in Striatum , 1987, Journal of neurochemistry.

[12]  X.-T. Hu,et al.  Comparison of effects of D-1 and D-2 dopamine receptor agonists on neurons in the rat caudate putamen: an electrophysiological study , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  J. Millar,et al.  Differential Actions of Endogenous and Iontophoretic Dopamine in Rat Striatum , 1990, The European journal of neuroscience.

[14]  P. H. Andersen,et al.  Dopamine receptor agonists: selectivity and dopamine D1 receptor efficacy. , 1990, European journal of pharmacology.

[15]  M. Iadarola,et al.  Cocaine induces striatal c-fos-immunoreactive proteins via dopaminergic D1 receptors. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[16]  F. Gonon,et al.  Presynaptic autoinhibition of the electrically evoked dopamine release studied in the rat olfactory tubercle byin vivo electrochemistry , 1991, Neuroscience.

[17]  K. Chergui,et al.  Relationship between dopamine release in the rat nucleus accumbens and the discharge activity of dopaminergic neurons during local in vivo application of amino acids in the ventral tegmental area , 1992, Neuroscience.

[18]  Bertil Hille,et al.  G protein-coupled mechanisms and nervous signaling , 1992, Neuron.

[19]  George V. Rebec,et al.  Striatal single-unit responses to amphetamine and neuroleptics in freely moving rats , 1993, Neuroscience & Biobehavioral Reviews.

[20]  D L Price,et al.  Localization of D1 and D2 dopamine receptors in brain with subtype-specific antibodies. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[21]  R. Nicoll,et al.  Local and diffuse synaptic actions of GABA in the hippocampus , 1993, Neuron.

[22]  S. Young,et al.  5-hydroxydopamine-labeled dopaminergic axns: Three-dimensional reconstructions of axons, synapses and postsynaptic targets in rat neostriatum , 1994, Neuroscience.

[23]  P. Garris,et al.  Heterogeneity of evoked dopamine overflow wihin the striatal and striatoamygdaloid regions , 1994, Neuroscience.

[24]  K. Chergui,et al.  Nonlinear relationship between impulse flow, dopamine release and dopamine elimination in the rat brainin vivo , 1994, Neuroscience.

[25]  F. Gonon,et al.  Continuousin vivo monitoring of evoked dopamine release in the rat nucleus accumbens by amperometry , 1994, Neuroscience.

[26]  J. Garthwaite,et al.  Synaptic activation of metabotropic glutamate receptors in the parallel Fibre-Purkinje cell pathway in rat cerebellar slices , 1994, Neuroscience.

[27]  S. Tonegawa,et al.  Elimination of cocaine-induced hyperactivity and dopamine-mediated neurophysiological effects in dopamine D1 receptor mutant mice , 1994, Cell.

[28]  P. Garris,et al.  Efflux of dopamine from the synaptic cleft in the nucleus accumbens of the rat brain , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  P. Greengard,et al.  Modulation of calcium currents by a D1 dopaminergic protein kinase/phosphatase cascade in rat neostriatal neurons , 1995, Neuron.

[30]  J. Bolam,et al.  Electron microscopic analysis of D1 and D2 dopamine receptor proteins in the dorsal striatum and their synaptic relationships with motor corticostriatal afferents , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  K. Chergui,et al.  Uptake of Dopamine Released by Impulse Flow in the Rat Mesolimbic and Striatal Systems In Vivo , 1995, Journal of neurochemistry.

[32]  G. Rebec,et al.  Iontophoresis in the neostriatum of awake, unrestrained rats: Differential effects of dopamine, glutamate and ascorbate on motor- and nonmotor-related neurons , 1995, Neuroscience.

[33]  C. Nicholson.  Interaction between diffusion and Michaelis-Menten uptake of dopamine after iontophoresis in striatum. , 1995, Biophysical journal.

[34]  H. C. Cromwell,et al.  Neuromodulatory actions of dopamine on synaptically‐evoked neostriatal responses in slices , 1996 .

[35]  W. Schultz,et al.  Preferential activation of midbrain dopamine neurons by appetitive rather than aversive stimuli , 1996, Nature.

[36]  F. Gonon,et al.  Excitatory effects of dopamine released by impulse flow in the rat nucleus accumbens in vivo , 1996, Neuroscience.

[37]  J. Wickens,et al.  Dopamine reverses the depression of rat corticostriatal synapses which normally follows high-frequency stimulation of cortex In vitro , 1996, Neuroscience.

[38]  B. Bloch,et al.  Ultrastructural localization of D1 dopamine receptor immunoreactivity in rat striatonigral neurons and its relation with dopaminergic innervation , 1996, Brain Research.

[39]  M. Kuhar,et al.  The dopamine transporter is localized to dendritic and axonal plasma membranes of nigrostriatal dopaminergic neurons , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  A M Graybiel,et al.  Cellular responses to psychomotor stimulant and neuroleptic drugs are abnormal in mice lacking the D1 dopamine receptor. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[41]  R. Malenka,et al.  Psychostimulants depress excitatory synaptic transmission in the nucleus accumbens via presynaptic D1-like dopamine receptors , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  K. Chergui,et al.  Burst stimulation of the medial forebrain bundle selectively increases Fos-like immunoreactivity in the limbic forebrain of the rat , 1996, Neuroscience.

[43]  H. C. Cromwell,et al.  Modulatory Actions of Dopamine on NMDA Receptor-Mediated Responses Are Reduced in D1A-Deficient Mutant Mice , 1996, The Journal of Neuroscience.

[44]  A. Gratton,et al.  Behavior-Relevant Changes in Nucleus Accumbens Dopamine Transmission Elicited by Food Reinforcement: An Electrochemical Study in Rat , 1996, The Journal of Neuroscience.