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Experimental Brain Research

, Volume 86, Issue 1, pp 141–150 | Cite as

Repetitive firing properties of putative dopamine-containing neurons in vitro: regulation by an apamin-sensitive Ca2+-activated K+ conductance

  • P. D. Shepard
  • B. S. Bunney
Article

Summary

Intracellular recording techniques were used to study the effects of apamin (APA), a selective inhibitor of one type of Ca2+-activated K+ channel, on the electroresponsive properties of dopamine (DA)-containing neurons within the zona compacta of the substantia nigra (SNc) in rat. Bath application of APA (1 μM) blocked the slow component of a complex post-spike afterhyperpolarization (AHPs) without affecting other characteristics of the action potential. Blockade of AHPs was accompanied by an increase in the number and frequency of action potentials evoked by depolarizing current pulses. However, APA failed to affect the cellular mechanisms underlying spike frequency adaptation or poststimulus inhibitory period. These data indicate that AHPs can exert a strong influence on the interspike interval but is probably not involved in regulating slower adaptive neuronal responses.

Key words

Substantia nigra Apamin Ca2+-activated K++ channel Afterhyperpolarization Intracellular recording Rat 

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References

  1. Aghajanian GK, Rasmussen K (1989) Intracellular studies in the facial nucleus illustrating a simple new method for obtaining viable motoneurons in adult rat brain slices. Synapse 3:331–338Google Scholar
  2. Andrade R, Aghajanian GK (1984) Locus coeruleus activity in vitro: intrinsic regulation by a calcium-dependent potassium conductance but not alpha-2-adrenoceptors. J Neurosci 4:161–170Google Scholar
  3. Barrett EF, Barrett JN (1976) Separation of two voltage-sensitive potassium currents and demonstration of a tetrodotoxin-resistant calcium current in frog motoneurons. J Physiol 255:737–774Google Scholar
  4. Benson JA, Cooke IM (1984) Driver potentials and the organization of rhythmic bursting in crustacean ganglia. TINS 7:85–91Google Scholar
  5. Blatz AL, Magleby KL (1986) Single apamin-blocked Ca-activated K+ channels of small conductance in cultured rat skeletal muscle. Nature 323:718–720Google Scholar
  6. Blatz AL, Magleby KL (1987) Calcium-activated potassium channels. TINS 10:463–467Google Scholar
  7. Bourque CW, Brown DA (1987) Apamin and d-tubocurarine block the hyperpolarization of rat supraoptic neurosecretory neurons. Neurosci Lett 82:185–190Google Scholar
  8. Bourque CW, Randle CR, Renaud LP (1985) Calcium-dependent potassium conductance in rat supraoptic nucleus neurosecretory neurons. J Neurophysiol 54:1375–1382Google Scholar
  9. Finlayson PG, Marshall KC (1988) Synchronous bursting of locus coeruleus neurons in tissue culture. Neuroscience 24:217–225Google Scholar
  10. Fujimura K, Matsuda Y (1988) Responses to ramp current stimulation of the neurons in the substantia nigra pars compacta in vitro. Brain Res 475:177–181Google Scholar
  11. Galarraga E, Bargas J, Sierra A, Aceves J (1989) The role of calcium in the repetitive firing of neostriatal neurons. Exp Brain Res 75:157–168PubMedGoogle Scholar
  12. Grace AA (1987) The regulation of dopamine neuron activity as determined by in vivo and in vitro intracellular recordings. In: Chiodo LA, Freeman AS (eds) Neurophysiology of dopaminergic systems: current status and clinical perspectives. Lakeshore Press, Grosse Pointe, pp 1–66Google Scholar
  13. Grace AA, Bunney BS (1983a) Intracellular and extracellular electrophysiology of nigral dopaminergic neurons: I. Identification and characterization. Neuroscience 10:301–315Google Scholar
  14. Grace AA, Bunney BS (1983b) Intracellular and extracellular electrophysiology of nigral dopaminergic neurons: II. Action potential generating mechanisms and morphological correlates. Neuroscience 10:317–331Google Scholar
  15. Grace AA, Bunney BS (1984a) The control of firing pattern in nigral dopamine neurons: single spike firing. J Neurosci 4:2866–2876Google Scholar
  16. Grace AA, Bunney BS (1984b) The control of firing pattern in nigral dopamine neurons: burst firing. J Neurosci 4:2877–2890Google Scholar
  17. Grace AA, Onn SP (1989) Morphology and electrophysiological properties of immunocytochemically identified rat dopamine neurons recorded in vitro. J Neurosci 9:3463–3481Google Scholar
  18. Halliwell JV, Adams PR (1982) Voltage-clamp analysis of muscarinic excitation in hippocampal neurons. Brain Res 250:71–92Google Scholar
  19. Harris NC, Webb C, Greenfield SA (1989) A possible pacemaker mechanism in pars compacta neurons of the guinea-pig substantia nigra revealed by various ion channel blocking agents. Neuroscience 31:355–362Google Scholar
  20. Harris-Warrick RM, Flamm RE (1987) Multiple mechanisms of bursting in a conditional bursting neuron. J Neuroscience 7:2113–2128Google Scholar
  21. Harris-Warrick RM, Johnson BR (1987) Potassium channel blockade induces rhythmic activity in a conditional burster neuron. Brain Res 416:381–386Google Scholar
  22. Hugues M, Romey G, Duval D, Vincent JP, Lazdunski M (1982) Apamin as a selective blocker of the calcium-dependent potassium channel in neuroblastoma cells: Voltage clamp and biochemical characterization of the toxin receptor. Proc Natl Acad Sci 79:1308–1312Google Scholar
  23. Kawai T, Watanabe M (1986) Blockade of Ca2+-activated K+ conductance by apamin in rat sympathetic neurones. Br J Pharmacol 87:225–232Google Scholar
  24. Kelso SR, Nelson DO, Silva NL, Boulant JA (1983) A slice chamber for intracellular and extracellular recording during continuous perfusion. Brain Res Bull 10:853–857Google Scholar
  25. Kita T, Kita H, Kitai ST (1986) Electrical membrane properties of rat substantia nigra compacta neurons in an in vitro slice preparation. Brain Res 372:21–30Google Scholar
  26. Lacey MG, North (1987) Timer-dependent inward rectification in rat substantia nigra compacta neurons: Voltage clamp analysis. Soc Neurosci Abstr 13:533Google Scholar
  27. Lacey MG, Mercuri NB, North RA (1987) Dopamine acts on D2 receptors to increase potassium conductance in neurons of the rat substantia nigra zona compacta. J Physiol 392:397–416Google Scholar
  28. Lancaster B, Nicoll RA (1987) Properties of two calcium-activated hyperpolarizations in rat hippocampal neurons. J Physiol 389:187–203Google Scholar
  29. Lazdunski M, Fosset M, Hugues M, Mourre C, Romey G, Schmidt-Antomarchi H (1985) The apamin-sensitive Ca2+dependent K+ channel: molecular properties, differentiation and endogenous ligands in mammalian brain. Biochem Soc Symp 50:31–42Google Scholar
  30. Llinas R, Greenfield SA, Jahnsen H (1984) Electrophysiological properties of pars compacta cells in the in vitro substantia nigra: a possible mechanism for dendritic release. Brain Res 294:127–132Google Scholar
  31. Marty A (1988) The physiological role of calcium-dependent channels. TINS 12:420–424Google Scholar
  32. Madison DV, Nicoll RA (1984) Control of the repetitive discharge of rat CA1 pyramidal neurones in vitro. J Physiol 354:319–331Google Scholar
  33. Matsuda Y, Fujimura K, Yoshida S (1987) Two types of neurons in the substantia nigra pars compacta studied in a slice preparation. Neuroscience Res 5:172–179Google Scholar
  34. Meech RW (1978) Calcium-dependent potassium activation in nervous tissues. Ann Rev Biophy Bioeng 7:1–18Google Scholar
  35. Mourre C, Hugues M, Lazdunski M (1986) Quantitative autoradiographic mapping in rat brain of the receptor of apamin, a polypeptide toxin specific for one class of Ca2+-activated K+ channels. Brain Res 382:239–249Google Scholar
  36. Osmanovic SS, Shefner SA, Brodie MS (1990) Functional significance of the apamin-sensitive conductance in rat locus coeruleus neurons. Brain Res 530:283–289Google Scholar
  37. Pennefather P, Lancaster B, Adams PR, Nicoll RA (1985) Two distinct Ca2+-dependent K+ currents in bullfrog sympathetic ganglion cells. Proc Natl Acad Sci 82:3040–3044Google Scholar
  38. Ritchie AK (1987) Two distinct calcium-activated potassium currents in a rat anterior pituitary cell line. J Physiol 385:591–609Google Scholar
  39. Sanghera MK, Trulson ME, German DC (1984) Electrophysiological properties of mouse dopamine neurons: in vivo and in vitro studies. Neuroscience 12:793–801Google Scholar
  40. Schmid-Antomarchi H, Hugues M, Lazdunski M (1986) Properties of the apamin-sensitive Ca2+-activated K+ channel in PC12 pheochromocytoma cells which hyperproduce the apamin receptor. J Biol Chem 261:8633–8637Google Scholar
  41. Schwindt PC, Spain WJ, Foehring RC, Stafstrom MC, Chubb MC, Crill WE (1988) Multiple potassium conductances and their functions in neurons from cat sensorimotor cortex in vitro. J Physiol 59:424–449Google Scholar
  42. Shepard PD, Bunney BS (1988a) Effects of apamin on the discharge properties of putative dopamine-containing neurons in vitro. Brain Res 463:380–384Google Scholar
  43. Shepard PD, Bunney BS (1988b) Effects of apamin on the membrane properties of putative dopamine-containing neurons in vitro. Soc Neurosci Abstr 14:932Google Scholar
  44. Shepard PD, German DC (1988) Electrophysiological and pharmacological evidence for the existence of distinct subpopulations of nigrostriatal dopaminergic neurons in the rat. Neuroscience 27:537–546Google Scholar
  45. Silva NL, Bunney BS (1988) Intracellular studies of dopamine neurons in vitro: pacemakers modulated by dopamine. Eur J Pharmacol 149:307–315Google Scholar
  46. Silva NL, Pechura CM, Barker JL (1990) Postnatal rat nigrostriatal dopaminergic neurons exhibit five types of potassium conductances. J Neurophysiol 64:262–272Google Scholar
  47. Spain WJ, Schwindt PC, Crill WE (1987) Anomalous rectification in neurons from cat sensorimotor cortex in vitro. J Neurophysiol 57:1555–1576Google Scholar
  48. Stanzione P, Stefani A, Bernardi G (1988) Morphine induces a spontaneous and evoked bursting activity in rat cortical neurons by adding a postsynaptic active mechanism to the synaptic input: an intracellular study in vivo. Neuroscience 26:45–53Google Scholar
  49. Steriade M, Deschenes M, Domich L, Mulle C (1985) Abolition of spindle oscillation in thalamic neurons disconnected from nucleus reticularis thalami. J Neurophysiol 54:1473–1497Google Scholar
  50. Szente MB, Baranyi A, Woody CD (1988) Intracellular injection of apamin reduces a slow potassium current mediating hyperpolarizations and IPSPs in neocortical neurons of cats. Brain Res 461:64–74Google Scholar
  51. Tanaka K, Minota S, Kuba K, Koyano K, Abe T (1986) Differential effects of apamin on Ca2+ — dependent K+ currents in bullfrog sympathetic ganglion cells. Neurosci Lett 69:233–238Google Scholar
  52. Williams JT, North RA, Shefner SA, Nishi S, Egan TM (1984) Membrane properties of rat locus coeruleus neurons. Neuroscience 13:137–156Google Scholar
  53. Yarom Y, Llinas R (1987) Long-term modifiability of anomalous and delayed rectification in guinea pig inferior olivary neurons. J Neurosci 7:1166–1177Google Scholar
  54. Zhang L, Krnjevic K (1987) Apamin depresses selectively the afterhyperpolarization of cat spinal motoneurons. Neurosci Lett 74:58–62Google Scholar

Copyright information

© Springer-Verlag 1991

Authors and Affiliations

  • P. D. Shepard
    • 1
  • B. S. Bunney
    • 1
  1. 1.Departments of Psychiatry and PharmacologyYale University School of MedicineNew HavenUSA

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