Skip to main content
Log in

Inhibitory action of dopamine involves a subthreshold Cs+-sensitive conductance in neostriatal neurons

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Intracellular recordings in in vitro slice preparations of rat brain were used to compare the actions of dopamine and dopamine receptor agonists on the subthreshold membrane properties of neostriatal neurons. A reproducible response for dopaminergic agonists was evoked after firing produced by current ramp injections that induced a subthreshold voltage displacement. Dopamine (10–100 μM) decreased both firing rate and membrane slope input resistance in virtually all cells tested. Input resistance change appeared as an increase in inward rectification. Approximate reversal potential was around -87 mV. The D1 receptor agonists SKF 38393 and C1-APB (1–10 μM) mimicked both dopamine effects with a reversal potential around -89 mV. The effects were blocked by the presence of 5–10 μM caesium (Cs+) but not by 1 μM tetrodotoxin, suggesting that main D1 effects on input resistance are due to subthreshold Cs+ sensitive conductances. cAMP analogues mimicked the actions of D1 receptor agonists. The D2 agonist, quinpirole (1–10 μM), did not produce any input resistance change, nonetheless, it still produced a decrease in firing rate. This suggests that the main D2 effect on firing is due to actions on suprathreshold ion conductances. All effects were blocked by D1 and D2 antagonists, respectively. D1 or D2 effects were found in the majority of cells tested.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Akaike A, Ohno Y, Sasa M, Takaori S (1987) Excitatory and inhibitory effects of dopamine on neuronal activity of the caudate neurons in vitro. Brain Res 418: 262–272

    Google Scholar 

  • Bargas J, Galarraga E, Aceves J (1988) Electrotonic properties of neostriatal neurons are modulated by extracellular potassium. Exp Brain Res 72: 390–398

    Google Scholar 

  • Bargas J, Galarraga E, Aceves J (1989) An early outward conductance modulates the firing latency and frequency of neostriatal neurons of the rat brain. Exp Brain Res 75: 146–156

    Google Scholar 

  • Bargas J, Howe A, Eberwine J, Cao Y, Surmeier DJ (1994) Cellular and molecular characterization of Ca2+ currents in acutely isolated, adult rat neostriatal neurons. J Neurosci 14: 6667–6686

    Google Scholar 

  • Benson JA, Adams WB (1987) The control of rhythmic neuronal firing. In: Kaczmareck LK, Levitan IB (eds) Neuromodulation. Oxford University Press, New York, pp 100–118

    Google Scholar 

  • Calabresi P, Mercuri N, Stanzione P, Stefani A, Bernardi G (1987) Intracellular studies on the dopamine-induced firing inhibition of neostriatal neurons in vitro: evidence for D1 receptor involvement. Neuroscience 20: 757–771

    Article  CAS  PubMed  Google Scholar 

  • Cepeda C, Buchwald NA, Levine MS (1993) Neuromodulatory actions of dopamine in the neostriatum are dependent upon the excitatory amino acid receptor subtypes activated. Proc Natl Acad Sci USA 90: 9576–9580

    CAS  PubMed  Google Scholar 

  • Cepeda C, Chandler SH, Shumate LW, Levine MS (1995) Persistent Na+ conductance in medium-sized neostriatal neurons: characterization using infrared videomicroscopy and wholecell patch-clamp recordings. J Neurophysiol 74: 1343–1348

    CAS  PubMed  Google Scholar 

  • Chao TI, Alzheimer C (1995) Do neurons from rat neostriatum express both a TTX-sensitive and a TTX-insensitive slow Na+ current? J Neurophysiol 74: 934–941

    Google Scholar 

  • Civelli O, Bunzow JR, Grandy DK, Zhou QY, Van Tol HHM (1991) Molecular biology of the dopamine receptor. Eur J Pharmacol 207: 277–286

    Google Scholar 

  • Floran B, Aceves J, Sierra A, Martinez-Fong D (1990) Activation of d1 dopamine receptors stimulates the release of GABA in the basal ganglia of the rat. Neurosci Lett 116: 136–140

    Google Scholar 

  • Flores-Hernández J, Galarraga E, Pineda JC, Bargas J (1994) Patterns of excitatory and inhibitory synaptic transmission in the rat neostriatum as revealed by 4-AP. J Neurophysiol 72: 2246–2256

    Google Scholar 

  • Freedman JE, Weight FF (1988) Single K+ channels activated by D2 dopamine receptors in acutely dissociated neurons from rat corpus striatum. Proc Natl Acad Sci USA 85: 3618–3622

    Google Scholar 

  • Galarraga E, Pacheco-Cano MT, Flores-Hernández J, Bargas J (1994) Subthreshold rectification in neostriatal spiny projection neurons. Exp Brain Res 100: 239–249

    CAS  PubMed  Google Scholar 

  • Garcia-Munoz M, Young SJ, Groves PM (1991) Terminal excitability of the corticostriatal pathway. I. Regulation by dopamine receptor stimulation. Brain Res 551: 195–206

    Google Scholar 

  • Gerfen CR (1992) The neostriatal mosaic: multiple levels of compartmental organization in the basal ganglia. Annu Rev Neurosci 15: 285–320

    Google Scholar 

  • Greif GJ, Lin Y-J, Liu J-C, Freedman E. (1995) Dopamine-Modulated potassium channels on rat striatal neurons: specific activation and cellular expression. J Neurosci 15: 4533–544

    Google Scholar 

  • Hernández-López S, Bargas J, Reyes A, Galarraga E (1996) Dopamine modulates the afterhyperpolarization in neostriatal neurons. Neuroreport 7: 454–456

    Google Scholar 

  • Herrling PL, Hull CD (1980) Iontophoretically applied dopamine depolarizes and hyperpolarizes the membrane of cat caudate neurons. Brain Res 192: 441–462

    Google Scholar 

  • Hsu KS, Yang CH, Huang CC, Gean PW (1995) Carbachol-induced inward currents in neostriatal neurons through M1-like muscarinic receptor. Soc Neurosci Abstr 21: 588

    Google Scholar 

  • Jack JJB, Noble D, Tsien RW (1975) Electric current flow in excitable cells. Oxford University Press, Oxford

    Google Scholar 

  • Kebabian JW, Calne DB (1979) Multiple receptors for dopamine. Nature 277: 93–96

    Google Scholar 

  • Lacey MG (1993) Neurotransmitter receptors and ionic conductances regulating the activity of neurons in substantia nigra pars compacta and ventral tegmental area. Prog Brain Res 99: 251–275

    Google Scholar 

  • McGeer PL, McGeer EG (1993) Neurotransmitters and their receptors in the basal ganglia. Adv Neurol 60: 93–100

    Google Scholar 

  • Nisenbaum ES, Wilson CJ (1995) Potassium currents responsible for inward and outward rectification in rat neostriatal spiny projection neurons. J Neurosci 15: 4449–4463

    Google Scholar 

  • Ogata N, Tatebayashi H (1990) Sodium current kinetics in freshly isolated neostriatal neurones of the adult guinea pig. Pflugers Arch 416: 594–603

    Google Scholar 

  • Pacheco-Cano MT, Tapia D, Bargas J, Galarraga E (1993) Comparison of D1 and D2 agonist actions on neostriatal neurons. Soc Neurosci Abstr 19: 127

    Google Scholar 

  • Pineda JC, Bargas J, Flores-Hernández J, Galarraga E (1995) Muscarinic receptors modulate the afterhyperpolarizing potential in neostriatal neurons. Eur J Pharmacol 281: 271–277

    Google Scholar 

  • Piomelli D, Pilon C, Giros B, Sokoloff P, Martres MP, Schwartz JCH (1991) Dopamine activation of the arachidonic acid cascade as a basis for D1/D2 receptor synergism. Nature 353: 164–167

    Google Scholar 

  • Rutherford A, García-Muñoz M, Arbuthnott GW (1988) An after hyperpolarization recorded in striatal cells “in vitro”: effect of dopamine administration. Exp Brain Res 71: 399–405

    CAS  PubMed  Google Scholar 

  • Sibley DR, Monsma FJ Jr (1992) Molecular biology of dopamine receptors. Trends Pharmacol Sci 13: 61–69

    Google Scholar 

  • Strange PG (1993) Dopamine receptors: structure and function. Prog Brain Res 99: 167–179

    Google Scholar 

  • Surmeier DJ, Kitai ST (1993) D1 and D2 dopamine receptor modulation of sodium and potassium currents in rat neostriatal neurons. Prog Brain Res 99: 309–324

    CAS  PubMed  Google Scholar 

  • Surmeier DJ, Reiner A, Levine MS, Ariano MA (1993) Are neostriatal dopamine receptors co-localized? Trends Neurosci 16: 299–305

    Google Scholar 

  • Surmeier DJ, Bargas J, Hemmings HC, Nairn AC, Greengard P (1995) Modulation of calcium currents by D1 dopaminergic protein kinase/phosphatase cascade in rat neostriatal neurons. Neuron 14: 385–397

    CAS  PubMed  Google Scholar 

  • Uchimura N, Higashi H, Nishi S (1986) Hyperpolarizing and depolarizing actions of dopamine via D1 and D2 receptors on nucleus accumbens neurons. Brain Res 375: 368–372

    Google Scholar 

  • Wilson CJ (1993) The generation of natural firing patterns in neostriatal neurons. Prog Brain Res 99: 277–297

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pacheco-Cano, M.T., Bargas, J., Hernández-López, S. et al. Inhibitory action of dopamine involves a subthreshold Cs+-sensitive conductance in neostriatal neurons. Exp Brain Res 110, 205–211 (1996). https://doi.org/10.1007/BF00228552

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00228552

Key words

Navigation