Elsevier

Neuroscience

Volume 10, Issue 2, October 1983, Pages 333-335, 337-348
Neuroscience

Intracellular and extracellular electrophysiology of nigral dopaminergic neurons—3. Evidence for electrotonic coupling

https://doi.org/10.1016/0306-4522(83)90137-9Get rights and content

Abstract

Using three independentin vivo methods, we have obtained evidence for electrotonic coupling between sets of rat zona compacta dopaminergic neurons: (1) Lucifer yellow injection into single dopamine neurons resulted in labeling of two to five dopamine neurons in 18 out of 33 injections. Similar injections into reticular formation or nigral reticulata cells did not demonstrate multiple labeling. (2) Intracellular recording revealed spontaneously occurring small (3–15 mV) fast potentials that often triggered action potentials in dopamine neurons when the membrane potential was close to firing threshold. These fast potentials had a firing rate and pattern similar to that reported previously for extracellularly recorded dopamine neurons. Fast potentials were activated antidromically from the caudate nucleus at a latency similar to that reported for dopamine neurons, followed high frequency antidromic stimulation at a constant latency, and collided with spontaneously occurring fast potentials. However, directly elicited action potentials would not collide reliably with antidromically activated fast potentials. Intracellular injection of depolarizing or hyperpolarizing current increased and decreased, respectively, the rate of occurrence of these potentials. The firing rate of fast potentials could be increased and decreased by the intravenous administration of dopamine antagonists and agonists, respectively. (3) Simultaneous extracellular recording from pairs of DA neurons revealed numerous instances of synchronized action potentials. This was observed more frequently following intravenous haloperidol administration. Sets of burst firing dopamine neurons recorded simultaneously consistently demonstrated a decrease in the interspike interval as the burst progressed; a phenomenon commonly reported in other electrically coupled systems.

Electrical coupling has been suggested to be present in sets of identified nigrostriatal dopamine neurons. Electrical communication between these neurons could be involved in modulating burst firing and in synchronizing dopamine release.

Reference (77)

  • MerickelM.B. et al.

    Analysis of a network of electrically coupled neurons producing rhythmic activity in the snail,Helisoma trivolvis

    IEEE Trans. Biomed. Engn.

    (1977)
  • PellioniszA. et al.

    Brain modeling by tensor network theory and computer simulation. The cerebellum: distributed processor for predictive coordinaton

    Neuroscience

    (1979)
  • PinchingA.J. et al.

    The neuropil of the glomeruli of the olfactory bulb

    J. Cell Sci.

    (1971)
  • SchwynR.C. et al.

    The primate substantia nigra: a Golgi and electron microscopic study

    J. Hirnforsch.

    (1974)
  • SegundoJ.P. et al.

    Sensitivity of neurones inAplysia to temporal pattern of arriving impulses

    J. exp. Biol.

    (1963)
  • SocolarS.J. et al.

    Methods for studying transmission through permeable cell-to-cell junctions

  • TennysonV.M. et al.

    The developing neostriatum of the rabbit: correlation of fluorescence histochemistry, electron microscopy, endogenous dopamine levels, and (3H) dopamine uptake

    Brain Res.

    (1972)
  • WaxmanS.G. et al.

    Coordinated micropinocytotic activity of adjacent neuronal membranes in mammalian central nervous system

    Neurosci. Letts

    (1980)
  • WilsonC.J. et al.

    Monoaminergic synapses, including dnedro-dendritic synapses in the rat substantia nigra

    Expl Brain Res.

    (1977)
  • AndénN.-E.

    Effect of reserpine and other drugs on the monoamine metabolism with special reference to the CNS

    Annls Med. Exp. Biol. Fenn.

    (1968)
  • AndénN.-E. et al.

    Evidence for dopamine receptor stimulation by apomorphine

    J. Pharm. Pharmac.

    (1967)
  • AndrewR.D. et al.

    Dye transfer through gap junctions between neuroendocrine cells of rat hypothalamus

    Science, N.Y.

    (1981)
  • BakerR. et al.

    Electrotonic coupling between neurones in the rat mesencephalic nucleus

    J. Physiol., Lond

    (1971)
  • BennettM.V.L.

    Physiology of electrotonic junctions

    Ann. N.Y. Acad. Sci.

    (1966)
  • BennettM.V.L.

    Function of electrotonic junctions in embryonic and adult tissues

  • BennettM.V.L.

    Electrical transmission: a functional analysis and comparison to chemical transmission

  • BennettM.V.L. et al.

    Gap junctions, electrotonic coupling, and intercellular communication

    Neurosci. Res. Prog. Bull.

    (1978)
  • BennettM.V.L. et al.

    Physiology and ultrastructure of electrotonic junctions—I. Supramedullary neurons

    J. Neurophysiol.

    (1967)
  • BennettM.V.L. et al.

    Physiology and ultrastructure of electrotonic junctions—III. Giant electromotor neurons ofMalapterus electricus

    J. Neurophysiol.

    (1967)
  • BennettM.V.L. et al.

    Physiology and ultrastructure of electrotonic junctions—II. Spinal and medullary electromotor nuclei in mormyrid fish

    J. Neurophysiol.

    (1967)
  • BerryM.S.

    A system of electrically coupled small cells in the buccal ganglia of the pond snailPlanorbis corneus

    J. exp. Biol.

    (1972)
  • BerryM.S.

    Electrotonic coupling between identified large cells in the buccal ganglia ofPlanorbis corneus

    J. exp. Biol.

    (1972)
  • BunneyB.S. et al.

    Dopaminergic neurons: effect of antipsychotic drugs and amphetamine on single cell activity

    J. Pharmac. exp. Thér.

    (1973)
  • CarpenterM.B.

    An anatomical organization of the corpus striatum and related nuclei

  • CoombsJ.S. et al.

    Excitatory synaptic action in motoneurones

    J. Physiol., Lond.

    (1955)
  • CurtisD.R. et al.

    The time courses of excitatory and inhibitory synaptic actions

    J. Physiol., London

    (1959)
  • DahlströmA. et al.

    Evidence for the existence of monoamine-containing neurons in the central nervous system

    Acta physiol. scand.

    (1964)
  • de la TorreJ.C. et al.

    A methodological approach to rapid and sensitive monoamine histofluorescence using a modified glyoxylic acid technique: the SPG method

    Histochemistry

    (1976)
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