Synaptic and intrinsic control of membrane excitability of neostriatal neurons. II. An in vitro analysis

Research output: Contribution to journalArticle

Abstract

The effects of intrinsic membrane properties on the spontaneous and synaptically evoked activity of neostriatal neurons were studied in an in vitro slice preparation with the use of intracellular recordings. The recorded neurons did not show spontaneous action potentials at rest; depolarizing current pulses triggered a tonic firing pattern. Subthreshold spontaneous depolarizing potentials (SDPs) were observed in 52% of the recorded neurons. The amplitude of these potentials at rest ranged between 2 and 15 mV, and their duration between 4 and 100 ms. The frequency and the amplitude of the SDPs were functions of the membrane potential: membrane depolarization by constant positive current increased the frequency of the SDPs and reduced their amplitude; hyperpolarization of the membrane decreased their frequency and increased their amplitude. Often, at membrane potentials more negative than -90 mV, SDPs were completely suppressed. SDPs were blocked by low calcium-cobalt containing solutions. In the presence of tetrodotoxin (TTX, 1-3 μM), SDPs were completely abolished in 50% of the tested neurons; in the remaining neurons, small (1-4 mV) TTX-resistant SDPs were observed. In most of the neurons, bicuculline (BIC, 10-100 μM) and low concentrations of tetanus toxin (5-10 μg/ml) did not clearly affect the SDPs. Higher concentrations of tetanus toxin (100 μg/ml) blocked the SDPs as well as the synaptic potentials evoked by intrastriatal stimulation. At resting membrane potential, intrastriatal stimulation produced a fast depolarizing postsynaptic potential (EPSP) that was reduced by BIC (10-100 μM). The relationship between EPSP amplitude and membrane potential was studied either by utilizing K+-chloride electrodes or by the use of cesium-chloride electrodes. In both these cases, the reversal potential for the EPSPs was between 0 and -14 mV. In cesium-loaded neurons, the decrease of the EPSP, usually observed at negative membrane potentials (below -85 mV), was clearly reduced. Internal cesium prolonged the duration of the SDPs and of the EPSPs evoked by intrastriatal stimulation. The relationship between the spontaneous and evoked synaptic activity and membrane potential was studied in the presence of different external potassium blockers. 4-Aminopyridine (4AP, 0.1-1 mM) increased the EPSP amplitude and the frequency of the SDPs, but did not decrease membrane rectification and the shunt of the EPSPs present at negative membrane potentials. On the contrary, rectification of the membrane and the shunt of the EPSPs below -85 mV were clearly reduced by tetraethylammonium (TEA 10-20 mM). Low concentrations of barium (1-5 μM) selectively increased the amplitude of the evoked EPSPs without altering the membrane resistance; higher concentrations of this K+ blocker (0.1-1 mM) produced large SDPs, triggering bursts of spikes, and increased the membrane resistance by reducing the rectification in the hyperpolarizing direction. Most of the barium- and 4AP-induced SDPs persisted in the presence of BIC. The presence of a possible tonic inhibitory control of the nigral dopaminergic projection on the spontaneous and evoked synaptic activity was studied by utilizing slices from dopamine-depleted rats (electrolytic lesion of the homolateral substantia nigra or reserpine pretreatment). These procedures did not alter the intrinsic or synaptic excitability of neostriatal cells. We conclude that intrinsic membrane properties of neostriatal neurons strongly influence the spontaneous and the synaptically evoked excitability of these cells. Potassium channels operating at negative potentials and underlying membrane rectification modulate the amplitude of the synaptically induced membrane depolarizations. This regulatory mechanism exerts a filtering function in the neostriatal neurons, and it may play a major role in the transduction of the signals from the neostriatum to the other structures of the basal ganglia.

Original languageEnglish
Pages (from-to)663-675
Number of pages13
JournalJournal of Neurophysiology
Volume63
Issue number4
Publication statusPublished - 1990

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Excitatory Postsynaptic Potentials
Membrane Potentials
imidazole mustard
Neurons
Membranes
Synaptic Potentials
Tetanus Toxin
Cesium
Substantia Nigra
Barium
Electrodes
Neostriatum
In Vitro Techniques
Synaptic Membranes
4-Aminopyridine
Tetraethylammonium
Bicuculline
Potassium Channels
Reserpine
Tetrodotoxin

ASJC Scopus subject areas

  • Physiology
  • Neuroscience(all)

Cite this

Synaptic and intrinsic control of membrane excitability of neostriatal neurons. II. An in vitro analysis. / Calabresi, P.; Mercuri, N. B.; Bernardi, G.

In: Journal of Neurophysiology, Vol. 63, No. 4, 1990, p. 663-675.

Research output: Contribution to journalArticle

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abstract = "The effects of intrinsic membrane properties on the spontaneous and synaptically evoked activity of neostriatal neurons were studied in an in vitro slice preparation with the use of intracellular recordings. The recorded neurons did not show spontaneous action potentials at rest; depolarizing current pulses triggered a tonic firing pattern. Subthreshold spontaneous depolarizing potentials (SDPs) were observed in 52{\%} of the recorded neurons. The amplitude of these potentials at rest ranged between 2 and 15 mV, and their duration between 4 and 100 ms. The frequency and the amplitude of the SDPs were functions of the membrane potential: membrane depolarization by constant positive current increased the frequency of the SDPs and reduced their amplitude; hyperpolarization of the membrane decreased their frequency and increased their amplitude. Often, at membrane potentials more negative than -90 mV, SDPs were completely suppressed. SDPs were blocked by low calcium-cobalt containing solutions. In the presence of tetrodotoxin (TTX, 1-3 μM), SDPs were completely abolished in 50{\%} of the tested neurons; in the remaining neurons, small (1-4 mV) TTX-resistant SDPs were observed. In most of the neurons, bicuculline (BIC, 10-100 μM) and low concentrations of tetanus toxin (5-10 μg/ml) did not clearly affect the SDPs. Higher concentrations of tetanus toxin (100 μg/ml) blocked the SDPs as well as the synaptic potentials evoked by intrastriatal stimulation. At resting membrane potential, intrastriatal stimulation produced a fast depolarizing postsynaptic potential (EPSP) that was reduced by BIC (10-100 μM). The relationship between EPSP amplitude and membrane potential was studied either by utilizing K+-chloride electrodes or by the use of cesium-chloride electrodes. In both these cases, the reversal potential for the EPSPs was between 0 and -14 mV. In cesium-loaded neurons, the decrease of the EPSP, usually observed at negative membrane potentials (below -85 mV), was clearly reduced. Internal cesium prolonged the duration of the SDPs and of the EPSPs evoked by intrastriatal stimulation. The relationship between the spontaneous and evoked synaptic activity and membrane potential was studied in the presence of different external potassium blockers. 4-Aminopyridine (4AP, 0.1-1 mM) increased the EPSP amplitude and the frequency of the SDPs, but did not decrease membrane rectification and the shunt of the EPSPs present at negative membrane potentials. On the contrary, rectification of the membrane and the shunt of the EPSPs below -85 mV were clearly reduced by tetraethylammonium (TEA 10-20 mM). Low concentrations of barium (1-5 μM) selectively increased the amplitude of the evoked EPSPs without altering the membrane resistance; higher concentrations of this K+ blocker (0.1-1 mM) produced large SDPs, triggering bursts of spikes, and increased the membrane resistance by reducing the rectification in the hyperpolarizing direction. Most of the barium- and 4AP-induced SDPs persisted in the presence of BIC. The presence of a possible tonic inhibitory control of the nigral dopaminergic projection on the spontaneous and evoked synaptic activity was studied by utilizing slices from dopamine-depleted rats (electrolytic lesion of the homolateral substantia nigra or reserpine pretreatment). These procedures did not alter the intrinsic or synaptic excitability of neostriatal cells. We conclude that intrinsic membrane properties of neostriatal neurons strongly influence the spontaneous and the synaptically evoked excitability of these cells. Potassium channels operating at negative potentials and underlying membrane rectification modulate the amplitude of the synaptically induced membrane depolarizations. This regulatory mechanism exerts a filtering function in the neostriatal neurons, and it may play a major role in the transduction of the signals from the neostriatum to the other structures of the basal ganglia.",
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T1 - Synaptic and intrinsic control of membrane excitability of neostriatal neurons. II. An in vitro analysis

AU - Calabresi, P.

AU - Mercuri, N. B.

AU - Bernardi, G.

PY - 1990

Y1 - 1990

N2 - The effects of intrinsic membrane properties on the spontaneous and synaptically evoked activity of neostriatal neurons were studied in an in vitro slice preparation with the use of intracellular recordings. The recorded neurons did not show spontaneous action potentials at rest; depolarizing current pulses triggered a tonic firing pattern. Subthreshold spontaneous depolarizing potentials (SDPs) were observed in 52% of the recorded neurons. The amplitude of these potentials at rest ranged between 2 and 15 mV, and their duration between 4 and 100 ms. The frequency and the amplitude of the SDPs were functions of the membrane potential: membrane depolarization by constant positive current increased the frequency of the SDPs and reduced their amplitude; hyperpolarization of the membrane decreased their frequency and increased their amplitude. Often, at membrane potentials more negative than -90 mV, SDPs were completely suppressed. SDPs were blocked by low calcium-cobalt containing solutions. In the presence of tetrodotoxin (TTX, 1-3 μM), SDPs were completely abolished in 50% of the tested neurons; in the remaining neurons, small (1-4 mV) TTX-resistant SDPs were observed. In most of the neurons, bicuculline (BIC, 10-100 μM) and low concentrations of tetanus toxin (5-10 μg/ml) did not clearly affect the SDPs. Higher concentrations of tetanus toxin (100 μg/ml) blocked the SDPs as well as the synaptic potentials evoked by intrastriatal stimulation. At resting membrane potential, intrastriatal stimulation produced a fast depolarizing postsynaptic potential (EPSP) that was reduced by BIC (10-100 μM). The relationship between EPSP amplitude and membrane potential was studied either by utilizing K+-chloride electrodes or by the use of cesium-chloride electrodes. In both these cases, the reversal potential for the EPSPs was between 0 and -14 mV. In cesium-loaded neurons, the decrease of the EPSP, usually observed at negative membrane potentials (below -85 mV), was clearly reduced. Internal cesium prolonged the duration of the SDPs and of the EPSPs evoked by intrastriatal stimulation. The relationship between the spontaneous and evoked synaptic activity and membrane potential was studied in the presence of different external potassium blockers. 4-Aminopyridine (4AP, 0.1-1 mM) increased the EPSP amplitude and the frequency of the SDPs, but did not decrease membrane rectification and the shunt of the EPSPs present at negative membrane potentials. On the contrary, rectification of the membrane and the shunt of the EPSPs below -85 mV were clearly reduced by tetraethylammonium (TEA 10-20 mM). Low concentrations of barium (1-5 μM) selectively increased the amplitude of the evoked EPSPs without altering the membrane resistance; higher concentrations of this K+ blocker (0.1-1 mM) produced large SDPs, triggering bursts of spikes, and increased the membrane resistance by reducing the rectification in the hyperpolarizing direction. Most of the barium- and 4AP-induced SDPs persisted in the presence of BIC. The presence of a possible tonic inhibitory control of the nigral dopaminergic projection on the spontaneous and evoked synaptic activity was studied by utilizing slices from dopamine-depleted rats (electrolytic lesion of the homolateral substantia nigra or reserpine pretreatment). These procedures did not alter the intrinsic or synaptic excitability of neostriatal cells. We conclude that intrinsic membrane properties of neostriatal neurons strongly influence the spontaneous and the synaptically evoked excitability of these cells. Potassium channels operating at negative potentials and underlying membrane rectification modulate the amplitude of the synaptically induced membrane depolarizations. This regulatory mechanism exerts a filtering function in the neostriatal neurons, and it may play a major role in the transduction of the signals from the neostriatum to the other structures of the basal ganglia.

AB - The effects of intrinsic membrane properties on the spontaneous and synaptically evoked activity of neostriatal neurons were studied in an in vitro slice preparation with the use of intracellular recordings. The recorded neurons did not show spontaneous action potentials at rest; depolarizing current pulses triggered a tonic firing pattern. Subthreshold spontaneous depolarizing potentials (SDPs) were observed in 52% of the recorded neurons. The amplitude of these potentials at rest ranged between 2 and 15 mV, and their duration between 4 and 100 ms. The frequency and the amplitude of the SDPs were functions of the membrane potential: membrane depolarization by constant positive current increased the frequency of the SDPs and reduced their amplitude; hyperpolarization of the membrane decreased their frequency and increased their amplitude. Often, at membrane potentials more negative than -90 mV, SDPs were completely suppressed. SDPs were blocked by low calcium-cobalt containing solutions. In the presence of tetrodotoxin (TTX, 1-3 μM), SDPs were completely abolished in 50% of the tested neurons; in the remaining neurons, small (1-4 mV) TTX-resistant SDPs were observed. In most of the neurons, bicuculline (BIC, 10-100 μM) and low concentrations of tetanus toxin (5-10 μg/ml) did not clearly affect the SDPs. Higher concentrations of tetanus toxin (100 μg/ml) blocked the SDPs as well as the synaptic potentials evoked by intrastriatal stimulation. At resting membrane potential, intrastriatal stimulation produced a fast depolarizing postsynaptic potential (EPSP) that was reduced by BIC (10-100 μM). The relationship between EPSP amplitude and membrane potential was studied either by utilizing K+-chloride electrodes or by the use of cesium-chloride electrodes. In both these cases, the reversal potential for the EPSPs was between 0 and -14 mV. In cesium-loaded neurons, the decrease of the EPSP, usually observed at negative membrane potentials (below -85 mV), was clearly reduced. Internal cesium prolonged the duration of the SDPs and of the EPSPs evoked by intrastriatal stimulation. The relationship between the spontaneous and evoked synaptic activity and membrane potential was studied in the presence of different external potassium blockers. 4-Aminopyridine (4AP, 0.1-1 mM) increased the EPSP amplitude and the frequency of the SDPs, but did not decrease membrane rectification and the shunt of the EPSPs present at negative membrane potentials. On the contrary, rectification of the membrane and the shunt of the EPSPs below -85 mV were clearly reduced by tetraethylammonium (TEA 10-20 mM). Low concentrations of barium (1-5 μM) selectively increased the amplitude of the evoked EPSPs without altering the membrane resistance; higher concentrations of this K+ blocker (0.1-1 mM) produced large SDPs, triggering bursts of spikes, and increased the membrane resistance by reducing the rectification in the hyperpolarizing direction. Most of the barium- and 4AP-induced SDPs persisted in the presence of BIC. The presence of a possible tonic inhibitory control of the nigral dopaminergic projection on the spontaneous and evoked synaptic activity was studied by utilizing slices from dopamine-depleted rats (electrolytic lesion of the homolateral substantia nigra or reserpine pretreatment). These procedures did not alter the intrinsic or synaptic excitability of neostriatal cells. We conclude that intrinsic membrane properties of neostriatal neurons strongly influence the spontaneous and the synaptically evoked excitability of these cells. Potassium channels operating at negative potentials and underlying membrane rectification modulate the amplitude of the synaptically induced membrane depolarizations. This regulatory mechanism exerts a filtering function in the neostriatal neurons, and it may play a major role in the transduction of the signals from the neostriatum to the other structures of the basal ganglia.

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