Dopamine excites fast-spiking interneurons in the striatum.

The striatum is the main recipient of dopaminergic innervation. Striatal projection neurons are controlled by cholinergic and GABAergic interneurons. The effects of dopamine on projection neurons and cholinergic interneurons have been described. Its action on GABAergic interneurons, however, is still unknown. We studied the effects of dopamine on fast-spiking (FS) GABAergic interneurons in vitro, with intracellular recordings. Bath application of dopamine elicited a depolarization accompanied by an increase in membrane input resistance (an effect that persisted in the presence of tetrodotoxin) and action-potential discharge. These effects were mimicked by the D1-like dopamine receptor agonist SKF38393 but not by the D2-like agonist quinpirole. Evoked corticostriatal glutamatergic synaptic currents were not affected by dopamine. Conversely, GABAergic currents evoked by intrastriatal stimulation were reversibly depressed by dopamine and D2-like, but not D1-like, agonists. Cocaine elicited effects similar to those of dopamine on membrane potential and synaptic currents. These results show that endogenous dopamine exerts a dual excitatory action on FS interneurons, by directly depolarizing them (through D1-like receptors) and by reducing their synaptic inhibition (through presynaptic D2-like receptors).

[1]  Paolo Calabresi,et al.  Electrophysiology of dopamine in normal and denervated striatal neurons , 2000, Trends in Neurosciences.

[2]  J. Tepper,et al.  Inhibitory control of neostriatal projection neurons by GABAergic interneurons , 1999, Nature Neuroscience.

[3]  J. Bolam,et al.  Selective Innervation of Neostriatal Interneurons by a Subclass of Neuron in the Globus Pallidus of the Rat , 1998, The Journal of Neuroscience.

[4]  C. Cepeda,et al.  Dopamine modulation of responses mediated by excitatory amino acids in the neostriatum. , 1998, Advances in pharmacology.

[5]  T Nagatsu,et al.  Synaptic integration mediated by striatal cholinergic interneurons in basal ganglia function. , 2000, Science.

[6]  J. Obeso,et al.  Pathophysiology of the basal ganglia in Parkinson's disease , 2000, Trends in Neurosciences.

[7]  T. W. Berger,et al.  Functionally distinct subpopulations of striatal neurons are differentially regulated by gabaergic and dopaminergic inputs—I. In vivo analysis , 1992, Neuroscience.

[8]  Y. Kawaguchi,et al.  Dopamine D1-Like Receptor Activation Excites Rat Striatal Large Aspiny Neurons In Vitro , 1998, The Journal of Neuroscience.

[9]  P. Greengard,et al.  Dopamine and cAMP-Regulated Phosphoprotein 32 kDa Controls Both Striatal Long-Term Depression and Long-Term Potentiation, Opposing Forms of Synaptic Plasticity , 2000, The Journal of Neuroscience.

[10]  D. Joel,et al.  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 , 2000, Neuroscience.

[11]  Charles J. Wilson,et al.  Surround inhibition among projection neurons is weak or nonexistent in the rat neostriatum. , 1994, Journal of neurophysiology.

[12]  R. Wise,et al.  The neurobiology of addiction , 2019, Annals of the New York Academy of Sciences.

[13]  J. Aceves,et al.  Inhibitory control of the GABAergic transmission in the rat neostriatum by D2 dopamine receptors , 1999, Neuroscience.

[14]  M. Zigmond,et al.  Influence of dopamine on GABA release in striatum: evidence for D1–D2 interactions and non-synaptic influences , 1997, Neuroscience.

[15]  T. Momiyama,et al.  Dopamine D2‐like receptors selectively block N‐type Ca2+ channels to reduce GABA release onto rat striatal cholinergic interneurones , 2001, The Journal of physiology.

[16]  T. W. Berger,et al.  Functionally distinct subpopulations of striatal neurons are differentially regulated by gabaergic and dopaminergic inputs—II. In vitro analysis , 1992, Neuroscience.

[17]  P. Calabresi,et al.  Activation of D2-Like Dopamine Receptors Reduces Synaptic Inputs to Striatal Cholinergic Interneurons , 2000, The Journal of Neuroscience.

[18]  G. Koob.  Neurobiology of Addiction: Toward the Development of New Therapies , 2000, Annals of the New York Academy of Sciences.

[19]  R. Blakely,et al.  Biogenic amine transporters: regulation in flux , 2000, Current Opinion in Neurobiology.

[20]  S. Sealfon,et al.  Dopamine receptors: from structure to behavior , 2000, Trends in Neurosciences.

[21]  R. Malenka,et al.  Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbens. , 2000, Annual review of neuroscience.

[22]  Charles J. Wilson,et al.  Striatal interneurones: chemical, physiological and morphological characterization , 1995, Trends in Neurosciences.

[23]  K. Tang,et al.  Dopamine-dependent synaptic plasticity in striatum during in vivo development. , 2001, Proceedings of the National Academy of Sciences of the United States of America.