Skip to main content
Log in

Subthreshold rectification in neostriatal spiny projection neurons

  • Original Paper
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Intracellular recordings from slice preparations were used to assess the subthreshold electrophysiological behavior of rat neostriatal projection neurons. Both current steps and ramp currents were used to estimate the current-voltage relationship (I–V plot). Inward rectification in the subthreshold range was a characteristic of most neurons. The amount of rectification varied greatly, and it was complex: membrane voltage trajectories in response to ramps were made up by almost piecewise changes in the rate of voltage rise, suggesting that multiple conductances contribute to the subthreshold range. Inward current blockers such as tetrodotoxin (TTX) or Cd2+ decreased inward rectification, whereas outward current blockers such as tetraethylammonium (TEA) or 4-aminopyridine (4-AP) increased inward rectification. However, most inward rectification was due to TEA- and Cs+-sensitive conductances and not to TTX- or Cd2+-sensitive conductances. Cs+-sensitive conductances predominated at more negative membrane potentials, whereas 4-AP-sensitive conductances predominated at just ±10 mV below the firing threshold. In spite of a very slow activation, there was evidence for transient outward currents modulating the response, i.e., 4-AP-sensitivity, and voltage-sensitivity for firing frequency and threshold. TEA-sensitive conductances also contributed toward fixing the firing threshold. These results imply the contribution of various ion conductances on the shaping of the characteristic physiological firing recorded in vivo. Modulation of these responses by transmitters or peptides may help to understand neural processing in the neostriatum.

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

  • Akins PT, Surmeier DJ, Kitai ST (1990) Muscarinic modulation of the transient potassium current in rat neostriatal neurons. Nature 344:240–242

    Google Scholar 

  • Baldissera F, Campadelli P, Piccinelli L (1987) The dynamic response of cat gastrocnemius motor units investigated by ramp current injection into their motoneurons. J Physiol (Lond) 387:317–330

    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, Galarraga E, Aceves J (1991a) Dendritic activity on neostriatal neurons as inferred from somatic intracellular recordings. Brain Res 539:159–163

    Google Scholar 

  • Bargas J, Howe A, Eberwine J, Cao Y, Surmeier DJ (1994) Acutely isolated rat neostriatal neurons express four types of high-voltage activated Ca2+ current. J Neurosci (in press)

  • Bargas J, Surmeier DJ, Kitai ST (1991b) High-voltage and low-voltage activated calcium currents are expressed by neurons cultured from embryonic rat striatum. Brain Res 541:70–74

    Google Scholar 

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

    Google Scholar 

  • Chang HT, Wilson CJ, Kitai ST (1982) A Golgi study of rat neostriatal neurons: light microscopic analysis. J Comp Neurol 208:107–126

    Google Scholar 

  • Galarraga E, Bargas J, Sierra A, Aceves J (1989) The role of calcium in the repetitive firing of neostriatal neurons. Exp Brain Res 75:157–168

    CAS  PubMed  Google Scholar 

  • Galarraga E, Bargas J (1991) Responses to injection of ramp currents in neostriatal neurons. Soc Neurosci Abstr 17:849

    Google Scholar 

  • Hille B (1992) Ionic channels of excitable membranes. Sinauer, Sunderland, Mass

    Google Scholar 

  • Horikawa K, Armstrong WE (1988) A versatile means of intracellular labeling: injection of biocytin and its detection with avidin conjugates. J Neurosci Methods 25:11–11

    Google Scholar 

  • Hull CD, Bernardi G, Buchwald NA (1970) Intracellular responses of caudate neurons to brain stem stimulation. Brain Res 22:163–179

    Google Scholar 

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

    Google Scholar 

  • Jahnsen H (1986) Electrophysiological characteristics of neurons in the guinea-pig deep cerebellar nuclei in vitro. J Physiol (Lond) 372:129–147

    Google Scholar 

  • Jahnsen H, Llinás R (1984) Electrophysiological properties of ginea-pig thalamic neurones: an in vitro study. J Physiol (Lond) 349:205–226

    Google Scholar 

  • Jiang ZG, North RA (1991) Membrane properties and synaptic responses of rat striatal neurones in vitro. J Physiol (Lond) 443:533–553

    Google Scholar 

  • Kita H, Kita T, Kitai ST (1985) Active membrane properties of rat neostriatal neurons in an in vitro slice preparation. Exp Brain Res 60:54–62

    Google Scholar 

  • Nisenbaum ES, Xu ZC, Wilson CJ (1994) Contribution of a slowly inactivating potassium current to the transition to firing of neostriatal spiny projection neurons. J Neurophysiol 71:1174–1189

    CAS  PubMed  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 23:127

    Google Scholar 

  • Pineda JC, Galarraga E, Bargas J, Cristancho M, Aceves J (1992) Charybdotoxin and apamin sensitivity of the calcium-dependent repolarization and the afterhyperpolarization in neostriatal neurons. J Neurophysiol 68:287–294

    Google Scholar 

  • Pineda JC, Bargas J, Flores-Hernández J, Galarraga E (1993) M1receptors modulate afterhyperpolarization amplitude (AHP) and excitability in neostriatal neurons. Soc Neurosci Abstr 23:127

    Google Scholar 

  • Stelling JW, Jacob TJC (1992) The inward rectifier potassium current underlies oscillatory membrane potential behavior in bovine pigmented ciliary epithelial cells. J Physiol (Lond) 458:439–456

    Google Scholar 

  • Storm JF (1990) Why is the input conductance of hippocampal neurons impaled with microelectrodes so much higher than when giga-seal patch pippetes are used? Soc Neurosci Abstr 16:506

    Google Scholar 

  • Schultz W, Romo R (1992) Role of primate basal ganglia and frontal cortex in the internal generation of movements I. Preparatory activity in the anterior striatum. Exp Brain Res 91:363–384

    Google Scholar 

  • Surmeier DJ, Bargas J, Howe AR (1993) Dopamine D1 receptor activation reduces Ca2+ currents in acutely dissociated rat neostriatal neurons. Soc Neurosci Abstr 23:978

    Google Scholar 

  • Surmeier DJ, Bargas J, Kitai ST (1988) Voltage-clamp analysis of a transient potassium current in rat neostriatal neurons. Brain Res 473:187–192

    Google Scholar 

  • Surmeier DJ, Eberwine J, Wilson CJ, Cao Y, Stefani A, Kitai ST (1992) Dopamine receptor subtypes colocalize in rat strionigral neurons. Proc Natl Acad Sci USA 89:10178–10182

    CAS  PubMed  Google Scholar 

  • Surmeier DJ, Stefani A, Foehring RC, Kitai ST (1991) Developmental regulation of a slowly-inactivating potassium conductance in rat neostriatal neurons. Neurosci Lett 122:41–46

    Google Scholar 

  • Uchimura N, Cherubini E, North A (1989) Inward rectification in rat nucleus accumbens neurons. J Neurophysiol 62:1280–1286

    CAS  PubMed  Google Scholar 

  • Yarom Y, Llinás R (1987) Long-term modifiability of anomalous and delayed rectification in guinea pig inferior olivary neurons. J Neurosci 7:1166–1177

    Google Scholar 

  • Wilson CJ, Groves PM (1981) Spontaneous firing patterns of identified spiny neurons in the rat neostriatum. Brain Res 220:67–80

    Article  CAS  PubMed  Google Scholar 

  • Wilson CJ (1990) Basal Ganglia. In: Shepherd GM (eds) The synaptic organization of the brain. Oxford University Press, Oxford

    Google Scholar 

  • Wilson CJ (1992) Dendritic morphology, inward rectification and the functional properties of neostriatal neurons. In: Single neuron computation. Academic, Boston, pp 141–171

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Galarraga, E., Pacheco-Cano, M.T., Flores-Hernández, J.V. et al. Subthreshold rectification in neostriatal spiny projection neurons. Exp Brain Res 100, 239–249 (1994). https://doi.org/10.1007/BF00227194

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00227194

Key words

Navigation