Elsevier

Brain Research

Volume 564, Issue 2, 15 November 1991, Pages 296-305
Brain Research

Intracellular study of rat globus pallidus neurons: membrane properties and responses to neostriatal, subthalamic and nigral stimulation

https://doi.org/10.1016/0006-8993(91)91466-EGet rights and content

Abstract

Physiological properties of globus pallidus (GP) neurons were studied intracellularly in anesthetized rats. More than 70% of the neurons exhibited continuous repetitive firing of 2–40 Hz, while others exhibited periodic burst firing or no firing. The repetitively firing neurons exhibited the following properties: spike accommodation; spike frequency adaption; continuous firing with a frequency of about 100 Hz generated by intracellular current injections; fast anomalous rectification; ramp-shaped depolarization upon injection of depolarizing current; and post-active hyperpolarization. The burst firing neurons evoked a large depolarization with multiple spikes in response to depolarizing current, and a similar response was observed after the termination of hyperpolarizing current. The few neurons which did not fire spontaneous spikes exhibited strong spike accommodation when they were stimulated by current injections. The continuously firing neurons were antidromically activated by stimulation of the neostriatum (Str) (23 of 68), the subthalamic nucleus (STh) (55 of 75), and the substantia nigra (SN) (25 of 46). The antidromic latencies of the 3 stimulus sites were very similar (about 1 ms). None of the burst firing neurons were antidromically activated. Three non-firing neurons evoked antidromic responses only after Str stimulation. Only repetitively firing neurons evoked postsynaptic responses following stimulation of the Str and the STh. Stimulatin of the Str evoked initial small EPSPs with latencies of 2–4 ms and strong, short duration IPSPs with latencies of 2–12 ms. Stimulation of the STh evoked short latency EPSPs overlapped with IPSPs. Frequently, these responses induced by Str and STh stimulation were followed by other EPSPs lasting 50–100 ms. These results indicated: (1) that the GP contains at least 3 electrophysiologically different types of neurons; (2) that GP projections to the Str, the STh, and the SN are of short latency pathways; (3) that Str stimulation evokes short latency EPSPs followed by IPSPs and late EPSPs in GP neurons; and (4) that STh stimulation evokes short latency EPSPs overlapped with short latency IPSPs and late EPSPs in GP neurons.

References (47)

  • MesulamM.-M. et al.

    Central cholinergic pathways in the rat: an overview based on an alternativ nomenclature

    Neuroscience

    (1983)
  • NakanishiH. et al.

    Intracellular study of rat substantia nigra pars reticulata neurons in an in vitro slice preparation: electrical membrane properties and response characteristics to subthalamic stimulation

    Brain Research

    (1987)
  • NakanishiH. et al.

    Intracellular study of rat entopeduncular nucleus neurons in an in vitro slice preparation: response to subthalamic stimulation

    Brain Research

    (1991)
  • NautaH.J.W.

    A proposed conceptual reorganization of the basal ganglia and telencephalon

    Neuroscience

    (1979)
  • NodaH. et al.

    Responses of cat pallidal neurons to cortical and subcortical stimuli

    Exp. Neurol.

    (1968)
  • OhyeC. et al.

    Responses of subthalamic and pallidal neurons to striatal stimulation: an extracellular study on awake monkeys

    Brain Research

    (1976)
  • ParkM.R. et al.

    Serotonergic excitation from dorsal raphe stimulation recorded intracellularly from rat caudate-putamen

    Brain Research

    (1982)
  • PennyG.R. et al.

    The glutamate decarboxylase-, leucine enkephalin-methionine enkephalin- and substance P-immunoreactive neurons in the neostriatum of the rat and cat: evidence for spatial overlap

    Neuroscience

    (1986)
  • PerkinsM.N. et al.

    Subthalamic projections to the globus pallidus: an electrophysiological study in the rat

    Exp. Neurol.

    (1980)
  • RobledoP. et al.

    Excitatory influence of rat subthalamic nucleus to substantia nigra pars reticulata and the pallidal complex: electrophysiological data

    Brain Research

    (1990)
  • Rouzaire-DuboisB. et al.

    Microiontophoretic studies on the nature of the neurotransmitter in the subthalamo-entopeduncular pathway of the rat

    Brain Research

    (1983)
  • SchmuedL. et al.

    Collateralization and GAD immunoreactivity of descending pallidal efferents

    Brain Research

    (1989)
  • SmithY. et al.

    Neurons of the substantia nigra reticulata receive a dense GABA-containing input from the globus pallidus in the rat

    Brain Research

    (1989)
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