Elsevier

Brain Research

Volume 138, Issue 2, 16 December 1977, Pages 271-283
Brain Research

Dual excitatory inputs to caudate spiny neurons from substantia nigra stimulation

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Summary

In the present set of experiments a two component excitatory postsynaptic potential (EPSP) (fast and slow) was recorded from caudate (Cd) neurons after substantia nigra (SN) stimulation in the α-chloralose anesthetized cat. Several unique properties of the fast response are demonstrated and used to determine certain functional properties of Cd neurons. The following conclusions have been drawn from these experiments. (1) A dual excitatory innervation pattern (fast and slow) exists to the Cd from SN stimulation. (2) The fast system is independent of the Cd efferent system. (3) Neurons receiving this dual input are spine laden neurons. (4) Dendritic inhibition is operating on these neurons and often has little or no direct influence on the observed soma membrane potential. The dendritic inhibition reduced test EPSP amplitude for several hundred milliseconds for all Cd afferents except for the fast SN input. Such a decoupling of the fast input from the inhibition may play an important role in Cd signal processing.

References (41)

  • KitaiS.T. et al.

    Electrophysiological and horseradish peroxidase studies of precerebellar afferents to the nucleus interpositus anterior: I. Climbing fiber system

    Brain Research

    (1977)
  • KitaiS.T. et al.

    Nigro-caudate and caudato-nigral relationship: an electrophysiological study

    Brain Research

    (1975)
  • KocsisJ.D. et al.

    Convergence of excitatory synaptic inputs to caudate spiny neurons

    Brain Research

    (1977)
  • KuypersH.G.J.M. et al.

    Retrograde axonal transport of horseradish peroxidase in rat forebrain

    Brain Research

    (1974)
  • MillerJ.J. et al.

    Anatomical and electrophysiological identification of a projection from the mesencephalic raphi to the caudato-putamen in the rat

    Brain Research

    (1975)
  • MooreR.Y. et al.

    Anatomical and chemical studies of a nigro-neostriatal projection in the cat

    Brain Research

    (1971)
  • NautaH.J.W. et al.

    Afferents to the rat caudato putamen studied with horseradish peroxidase. An evaluation of retrograde neuroanatomical research method

    Brain Research

    (1974)
  • RobertsonR.T. et al.

    Brainstem projections to the striatum: Experimental morphological studies in the rat

    Exp. Neurol.

    (1975)
  • Ande´nN.E. et al.

    Ascending monoamine neurons to the telencephalon

    Acta Physiol. scand.

    (1966)
  • BloomF.E. et al.

    Anesthesia and the responsiveness of individual neurones of the caudate nucleus of the cat to acetylcholine, norephinephrine and dopamine administered by microelectrophoresis

    J. Pharmacol exp. Ther.

    (1965)
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