Elsevier

Brain Research

Volume 212, Issue 2, 18 May 1981, Pages 345-359
Brain Research

The influence of striatal stimulation and putative neurotransmitters on identified neurones in the rat substantia nigra

https://doi.org/10.1016/0006-8993(81)90467-4Get rights and content

Abstract

The response of two populations of neurones in the substantia nigra (nigrostriatal compacta neurones and reticulata neurones) to microelectrophoretically administered putative neurotransmitters and stimulation of the ipsilateral striatum has been investigated in anaesthetized rats.

There were marked differences between compacta and reticulata neurones in respect to their action potential configurations, spontaneous firing rates and their responses to striatal stimulation. However, both compacta and reticulata neurones were excited and/or inhibited by striatal stimulation, although inhibition was usually the predominant response in both neuronal populations.

Compacta neurones were strongly inhibited by noradrenaline (NA) and dopamine (DA) but were unaffected by acetylcholine (ACh) and 5-hydroxytryptamine (5-HT). Reticulata neurones were excited by ACh and showed mixed responses to 5-HT DA and NA. Excitant amino acids overdepolarized compacta neurones preventing them from firing rapidly, but induced large increases in reticulata neurone firing rate; effects that were readily antagonized byd-α-aminoadipate. Compacta neurones were less sensitive than reticulata neurones to GABA and glycine. The action of these inhibitory amino acids were selectively and reversible antagonized by bicuculline methochloride and strychnine, respectively.

The striatal-evoked inhibition of both compacta and reticulata neurones was reversibly reduced by bicuculline methochloride and irreversibly reduced by tetanus toxin, but was unaffected by strychnine.

These results demonstrate that nigrostriatal-compacta neurones and reticulata neurones are physiologically and pharmacologically distinct neuronal populations and both receive inhibitory GABAergic and excitatory striatal inputs.

Reference (47)

  • GulleyR.L. et al.

    Synapses in the rat substantia nigra

    Tiss. Cell

    (1971)
  • GuyenetP.G. et al.

    Antidromic identification of dopaminergic and other output neurones of the rat substantia nigra

    Brain Research

    (1978)
  • JamesT.A. et al.

    Rapid behavioural and biochemical effects of tetanus toxin microinjected into the substantia nigra: a dual role for GABA?

    Neurosci. Lett.

    (1979)
  • JamesT.A. et al.

    Is glycine an inhibitory synaptic transmitter in the substantia nigra?

    Europ. J. Pharmacol.

    (1979)
  • KitaiS.T. et al.

    Nigrocaudate and caudato-nigral relatiohship: an electrophysiological study

    Brain Research

    (1975)
  • MartinG.E. et al.

    Contralateral turning evoked by the intranigral microinjection of muscimol and other GABA agonists

    Brain Research

    (1978)
  • MurrinL.C. et al.

    Autoradiographic localization of neuroleptic and dopamine receptors in the caudate-putamen and substantia nigra: effects of lesions

    Europ. J. Pharmacol.

    (1979)
  • OberlanderC. et al.

    Rotational behaviour after unilateral intranigral injection of muscimol in rats

    Europ. J. Pharmacol.

    (1977)
  • OlpeH.R. et al.

    Rotational behaviour induced in rats by intranigral applications of GABA-related drugs and GABA antagonists

    Europ. J. Pharmacol.

    (1977)
  • PycockC.J.

    Turning behaviour in animals

    Neuroscience

    (1980)
  • QuikM. et al.

    Dissociation between the presynaptic dopamine-sensitive adenylate cyclase and [3H]spiperone binding sites in rat substantia nigra

    Brain Research

    (1979)
  • ReavillC. et al.

    Turning behaviour induced by injection of muscimol or picrotoxin into the substantia nigra demonstrates dual GABA components

    Neurosci. Lett.

    (1979)
  • ReisineT.D. et al.

    Localization of dopamine receptors in rat brain

    Brain Research

    (1979)
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