Synaptic and intrinsic control of membrane excitability of neostriatal neurons. I. An in vivo analysis

P. Calabresi, N. B. Mercuri, A. Stefani, G. Bernardi

Research output: Contribution to journalArticle

94 Citations (Scopus)

Abstract

The relationship between membrane properties of neostriatal neurons and spontaneous and evoked synaptic potentials was studied with the use of intracellular recordings from anesthetized rats. Most of these neurons showed regular or irregular spontaneous depolarizing potentials that only in a few cases triggered action potentials at resting level. The stimulation of the ipsilateral substantia nigra or of the sensorimotor cortex produced a relatively fast depolarizing postsynaptic potential (EPSP). In some cells this potential was followed by an inhibitory period that appeared as an hyperpolarization when the cell was depolarized from the resting level (inhibitory postsynaptic potential, IPSP). A late and long-lasting depolarization (LD) followed the EPSP or the EPSP-IPSP sequence. Repetitive discharge with little adaptation was observed during direct depolarization. Most of the neurons tested for current-voltage (I-V) relationship showed nonlinearity of the input resistance in the hyperpolarizing direction. Spontaneous and evoked EPSPs were decreased in their amplitude and duration when the membrane potential was held at levels more hyperpolarized than -85 mV because of the strong rectification at these levels of hyperpolarization. Local microiontophoretic application of bicuculline (BIC) or systemic administration of BIC and pentylenetetrazole (PTZ) produced a reduction of the IPSPs. The reduction of the inhibitory transmission caused a strong increase of the LD. The current-evoked firing pattern was not greatly altered. The intracellular application of cesium increased the amplitude and the duration of the spontaneous depolarizations that triggered bursts of action potentials under this condition. Spikes were broadened and the rectification in the hyperpolarization direction was reduced. Iontophoretically applied cadmium strongly depressed the amplitude of the spontaneous and evoked postsynaptic potentials. During cadmium application, nigral stimulation produced constant latency, all-or-none spikes in the absence of any synaptic potential. Repetitive stimulation of the ipsilateral substantia nigra by electrical shocks (5 Hz, 25 s) produced a progressive and reversible decrease of the spontaneous depolarizing potentials (SDPs) and a decrease of the firing rate. In the same cells, when the train of stimulation was delivered in the ipsilateral cortex, a membrane depolarization coupled with an increase of the firing rate was observed. We conclude that although synaptic circuits mediate a phasic inhibition in neostriatum, the low level of spontaneous firing of most neostriatal neurons is mainly because of the effects that membrane properties exert on the spontaneous and the evoked synaptic depolarizations in the striatum. The single stimulations of the substantia nigra and of the cerebral cortex produce a sequence of fast synaptic events (EPSP-IPSP-LD), whereas the repetitive activation of nigral and cortical afferents results, respectively, in long-lasting inhibition and excitation of neostriatal neurons.

Original languageEnglish
Pages (from-to)651-662
Number of pages12
JournalJournal of Neurophysiology
Volume63
Issue number4
Publication statusPublished - 1990

Fingerprint

Excitatory Postsynaptic Potentials
Substantia Nigra
Inhibitory Postsynaptic Potentials
Synaptic Potentials
Neurons
Membranes
Bicuculline
Cadmium
Evoked Potentials
Action Potentials
Miniature Postsynaptic Potentials
Neostriatum
Cesium
Pentylenetetrazole
Cerebral Cortex
Membrane Potentials
Shock
Direction compound

ASJC Scopus subject areas

  • Physiology
  • Neuroscience(all)

Cite this

Synaptic and intrinsic control of membrane excitability of neostriatal neurons. I. An in vivo analysis. / Calabresi, P.; Mercuri, N. B.; Stefani, A.; Bernardi, G.

In: Journal of Neurophysiology, Vol. 63, No. 4, 1990, p. 651-662.

Research output: Contribution to journalArticle

@article{b6894942e08841e2bec30449640aac0f,
title = "Synaptic and intrinsic control of membrane excitability of neostriatal neurons. I. An in vivo analysis",
abstract = "The relationship between membrane properties of neostriatal neurons and spontaneous and evoked synaptic potentials was studied with the use of intracellular recordings from anesthetized rats. Most of these neurons showed regular or irregular spontaneous depolarizing potentials that only in a few cases triggered action potentials at resting level. The stimulation of the ipsilateral substantia nigra or of the sensorimotor cortex produced a relatively fast depolarizing postsynaptic potential (EPSP). In some cells this potential was followed by an inhibitory period that appeared as an hyperpolarization when the cell was depolarized from the resting level (inhibitory postsynaptic potential, IPSP). A late and long-lasting depolarization (LD) followed the EPSP or the EPSP-IPSP sequence. Repetitive discharge with little adaptation was observed during direct depolarization. Most of the neurons tested for current-voltage (I-V) relationship showed nonlinearity of the input resistance in the hyperpolarizing direction. Spontaneous and evoked EPSPs were decreased in their amplitude and duration when the membrane potential was held at levels more hyperpolarized than -85 mV because of the strong rectification at these levels of hyperpolarization. Local microiontophoretic application of bicuculline (BIC) or systemic administration of BIC and pentylenetetrazole (PTZ) produced a reduction of the IPSPs. The reduction of the inhibitory transmission caused a strong increase of the LD. The current-evoked firing pattern was not greatly altered. The intracellular application of cesium increased the amplitude and the duration of the spontaneous depolarizations that triggered bursts of action potentials under this condition. Spikes were broadened and the rectification in the hyperpolarization direction was reduced. Iontophoretically applied cadmium strongly depressed the amplitude of the spontaneous and evoked postsynaptic potentials. During cadmium application, nigral stimulation produced constant latency, all-or-none spikes in the absence of any synaptic potential. Repetitive stimulation of the ipsilateral substantia nigra by electrical shocks (5 Hz, 25 s) produced a progressive and reversible decrease of the spontaneous depolarizing potentials (SDPs) and a decrease of the firing rate. In the same cells, when the train of stimulation was delivered in the ipsilateral cortex, a membrane depolarization coupled with an increase of the firing rate was observed. We conclude that although synaptic circuits mediate a phasic inhibition in neostriatum, the low level of spontaneous firing of most neostriatal neurons is mainly because of the effects that membrane properties exert on the spontaneous and the evoked synaptic depolarizations in the striatum. The single stimulations of the substantia nigra and of the cerebral cortex produce a sequence of fast synaptic events (EPSP-IPSP-LD), whereas the repetitive activation of nigral and cortical afferents results, respectively, in long-lasting inhibition and excitation of neostriatal neurons.",
author = "P. Calabresi and Mercuri, {N. B.} and A. Stefani and G. Bernardi",
year = "1990",
language = "English",
volume = "63",
pages = "651--662",
journal = "Journal of Neurophysiology",
issn = "0022-3077",
publisher = "American Physiological Society",
number = "4",

}

TY - JOUR

T1 - Synaptic and intrinsic control of membrane excitability of neostriatal neurons. I. An in vivo analysis

AU - Calabresi, P.

AU - Mercuri, N. B.

AU - Stefani, A.

AU - Bernardi, G.

PY - 1990

Y1 - 1990

N2 - The relationship between membrane properties of neostriatal neurons and spontaneous and evoked synaptic potentials was studied with the use of intracellular recordings from anesthetized rats. Most of these neurons showed regular or irregular spontaneous depolarizing potentials that only in a few cases triggered action potentials at resting level. The stimulation of the ipsilateral substantia nigra or of the sensorimotor cortex produced a relatively fast depolarizing postsynaptic potential (EPSP). In some cells this potential was followed by an inhibitory period that appeared as an hyperpolarization when the cell was depolarized from the resting level (inhibitory postsynaptic potential, IPSP). A late and long-lasting depolarization (LD) followed the EPSP or the EPSP-IPSP sequence. Repetitive discharge with little adaptation was observed during direct depolarization. Most of the neurons tested for current-voltage (I-V) relationship showed nonlinearity of the input resistance in the hyperpolarizing direction. Spontaneous and evoked EPSPs were decreased in their amplitude and duration when the membrane potential was held at levels more hyperpolarized than -85 mV because of the strong rectification at these levels of hyperpolarization. Local microiontophoretic application of bicuculline (BIC) or systemic administration of BIC and pentylenetetrazole (PTZ) produced a reduction of the IPSPs. The reduction of the inhibitory transmission caused a strong increase of the LD. The current-evoked firing pattern was not greatly altered. The intracellular application of cesium increased the amplitude and the duration of the spontaneous depolarizations that triggered bursts of action potentials under this condition. Spikes were broadened and the rectification in the hyperpolarization direction was reduced. Iontophoretically applied cadmium strongly depressed the amplitude of the spontaneous and evoked postsynaptic potentials. During cadmium application, nigral stimulation produced constant latency, all-or-none spikes in the absence of any synaptic potential. Repetitive stimulation of the ipsilateral substantia nigra by electrical shocks (5 Hz, 25 s) produced a progressive and reversible decrease of the spontaneous depolarizing potentials (SDPs) and a decrease of the firing rate. In the same cells, when the train of stimulation was delivered in the ipsilateral cortex, a membrane depolarization coupled with an increase of the firing rate was observed. We conclude that although synaptic circuits mediate a phasic inhibition in neostriatum, the low level of spontaneous firing of most neostriatal neurons is mainly because of the effects that membrane properties exert on the spontaneous and the evoked synaptic depolarizations in the striatum. The single stimulations of the substantia nigra and of the cerebral cortex produce a sequence of fast synaptic events (EPSP-IPSP-LD), whereas the repetitive activation of nigral and cortical afferents results, respectively, in long-lasting inhibition and excitation of neostriatal neurons.

AB - The relationship between membrane properties of neostriatal neurons and spontaneous and evoked synaptic potentials was studied with the use of intracellular recordings from anesthetized rats. Most of these neurons showed regular or irregular spontaneous depolarizing potentials that only in a few cases triggered action potentials at resting level. The stimulation of the ipsilateral substantia nigra or of the sensorimotor cortex produced a relatively fast depolarizing postsynaptic potential (EPSP). In some cells this potential was followed by an inhibitory period that appeared as an hyperpolarization when the cell was depolarized from the resting level (inhibitory postsynaptic potential, IPSP). A late and long-lasting depolarization (LD) followed the EPSP or the EPSP-IPSP sequence. Repetitive discharge with little adaptation was observed during direct depolarization. Most of the neurons tested for current-voltage (I-V) relationship showed nonlinearity of the input resistance in the hyperpolarizing direction. Spontaneous and evoked EPSPs were decreased in their amplitude and duration when the membrane potential was held at levels more hyperpolarized than -85 mV because of the strong rectification at these levels of hyperpolarization. Local microiontophoretic application of bicuculline (BIC) or systemic administration of BIC and pentylenetetrazole (PTZ) produced a reduction of the IPSPs. The reduction of the inhibitory transmission caused a strong increase of the LD. The current-evoked firing pattern was not greatly altered. The intracellular application of cesium increased the amplitude and the duration of the spontaneous depolarizations that triggered bursts of action potentials under this condition. Spikes were broadened and the rectification in the hyperpolarization direction was reduced. Iontophoretically applied cadmium strongly depressed the amplitude of the spontaneous and evoked postsynaptic potentials. During cadmium application, nigral stimulation produced constant latency, all-or-none spikes in the absence of any synaptic potential. Repetitive stimulation of the ipsilateral substantia nigra by electrical shocks (5 Hz, 25 s) produced a progressive and reversible decrease of the spontaneous depolarizing potentials (SDPs) and a decrease of the firing rate. In the same cells, when the train of stimulation was delivered in the ipsilateral cortex, a membrane depolarization coupled with an increase of the firing rate was observed. We conclude that although synaptic circuits mediate a phasic inhibition in neostriatum, the low level of spontaneous firing of most neostriatal neurons is mainly because of the effects that membrane properties exert on the spontaneous and the evoked synaptic depolarizations in the striatum. The single stimulations of the substantia nigra and of the cerebral cortex produce a sequence of fast synaptic events (EPSP-IPSP-LD), whereas the repetitive activation of nigral and cortical afferents results, respectively, in long-lasting inhibition and excitation of neostriatal neurons.

UR - http://www.scopus.com/inward/record.url?scp=0025274408&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0025274408&partnerID=8YFLogxK

M3 - Article

C2 - 2341866

AN - SCOPUS:0025274408

VL - 63

SP - 651

EP - 662

JO - Journal of Neurophysiology

JF - Journal of Neurophysiology

SN - 0022-3077

IS - 4

ER -