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The M-current contributes to high threshold membrane potential oscillations in a cell type-specific way in the pedunculopontine nucleus of mice.

Bordas C, Kovacs A, Pal B - Front Cell Neurosci (2015)

Bottom Line: Blockade of the M-current abolished the oscillatory activity at 20 Hz, and largely diminished it at other frequencies.Taken together, the M-current seems to be characteristic for PPN cholinergic neurons.It provides a possibility for modulating gamma band activity of these cells, thus contributing to neuromodulatory regulation of the reticular activating system.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Medicine, Department of Physiology, University of Debrecen Debrecen, Hungary.

ABSTRACT
The pedunculopontine nucleus is known as a cholinergic nucleus of the reticular activating system, participating in regulation of sleep and wakefulness. Besides cholinergic neurons, it consists of GABAergic and glutamatergic neurons as well. According to classical and recent studies, more subgroups of neurons were defined. Groups based on the neurotransmitter released by a neuron are not homogenous, but can be further subdivided. The PPN neurons do not only provide cholinergic and non-cholinergic inputs to several subcortical brain areas but they are also targets of cholinergic and other different neuromodulatory actions. Although cholinergic neuromodulation has been already investigated in the nucleus, one of its characteristic targets, the M-type potassium current has not been described yet. Using slice electrophysiology, we provide evidence in the present work that cholinergic neurons possess M-current, whereas GABAergic neurons lack it. The M-current contributes to certain functional differences of cholinergic and GABAergic neurons, as spike frequency adaptation, action potential firing frequency or the amplitude difference of medium afterhyperpolarizations (AHPs). Furthermore, we showed that high threshold membrane potential oscillation with high power, around 20 Hz frequency is a functional property of almost all cholinergic cells, whereas GABAergic neurons have only low amplitude oscillations. Blockade of the M-current abolished the oscillatory activity at 20 Hz, and largely diminished it at other frequencies. Taken together, the M-current seems to be characteristic for PPN cholinergic neurons. It provides a possibility for modulating gamma band activity of these cells, thus contributing to neuromodulatory regulation of the reticular activating system.

No MeSH data available.


Related in: MedlinePlus

The presence or absence of the M-current contributes to the electrophysiological differences between cholinergic and GABAergic neurons. (A) Train of action potentials recorded from a cholinergic neuron, elicited by 100 pA current injection (black). (B) Train of action potentials from a GABAergic neuron, elicited by the same stimulus (green). (C–E) Statistical comparison of electrophysiological parameters of cholinergic (black) and GABAergic (green) neurons. (C) Current injections elicit higher frequency of action potential firing from GABAergic neurons. (D) Cell type dependence of the first interspike interval (hollow circles: individual data; black squares: average ± SEM). (E) Cell type-dependent changes of the adaptation index (see text; hollow circles: individual data; black squares: average ± SEM). (F,G) Cell type dependence of the amplitudes of afterhyperpolarizations (AHPs). (F) Voltage traces from a cholinergic (black) and a GABAergic (green) neuron. Dashed lines indicate the points where the fast, medium and slow AHPs were determined. (G) Statistical comparison of fast (fAHP), medium (mAHP) and slow AHPs (sAHP). Black: cholinergic; green: GABAergic. (H) Train of action potentials recorded from another cholinergic neuron, recorded under control conditions (black). (I) Train of action potentials recorded from another cholinergic neuron, recorded in the presence of 20 μM XE991 (red). (J–L) Statistical comparison of electrophysiological parameters of cholinergic neurons under control conditions (black) and with 20 μM XE991 (red). (J) Current injections elicit higher frequency of action potential firing in the presence of XE991. (K) Changes of the first interspike interval by application of XE991 (hollow circles: individual data; black squares: average ± SEM). (L) changes of the adaptation index with application of XE991 (see text; hollow circles: individual data; black squares: average ± SEM). (M,N) Effect of XE991 on the amplitudes of AHPs. (M) Voltage traces from a cholinergic neuron under control conditions (black) and in the presence of XE991 (red). Dashed lines indicate the points where the fast, medium and slow AHPs were determined. (N) Statistical comparison of fast (fAHP), medium (mAHP) and slow AHPs (sAHP). Black: control; red: XE991.
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Figure 2: The presence or absence of the M-current contributes to the electrophysiological differences between cholinergic and GABAergic neurons. (A) Train of action potentials recorded from a cholinergic neuron, elicited by 100 pA current injection (black). (B) Train of action potentials from a GABAergic neuron, elicited by the same stimulus (green). (C–E) Statistical comparison of electrophysiological parameters of cholinergic (black) and GABAergic (green) neurons. (C) Current injections elicit higher frequency of action potential firing from GABAergic neurons. (D) Cell type dependence of the first interspike interval (hollow circles: individual data; black squares: average ± SEM). (E) Cell type-dependent changes of the adaptation index (see text; hollow circles: individual data; black squares: average ± SEM). (F,G) Cell type dependence of the amplitudes of afterhyperpolarizations (AHPs). (F) Voltage traces from a cholinergic (black) and a GABAergic (green) neuron. Dashed lines indicate the points where the fast, medium and slow AHPs were determined. (G) Statistical comparison of fast (fAHP), medium (mAHP) and slow AHPs (sAHP). Black: cholinergic; green: GABAergic. (H) Train of action potentials recorded from another cholinergic neuron, recorded under control conditions (black). (I) Train of action potentials recorded from another cholinergic neuron, recorded in the presence of 20 μM XE991 (red). (J–L) Statistical comparison of electrophysiological parameters of cholinergic neurons under control conditions (black) and with 20 μM XE991 (red). (J) Current injections elicit higher frequency of action potential firing in the presence of XE991. (K) Changes of the first interspike interval by application of XE991 (hollow circles: individual data; black squares: average ± SEM). (L) changes of the adaptation index with application of XE991 (see text; hollow circles: individual data; black squares: average ± SEM). (M,N) Effect of XE991 on the amplitudes of AHPs. (M) Voltage traces from a cholinergic neuron under control conditions (black) and in the presence of XE991 (red). Dashed lines indicate the points where the fast, medium and slow AHPs were determined. (N) Statistical comparison of fast (fAHP), medium (mAHP) and slow AHPs (sAHP). Black: control; red: XE991.

Mentions: In order to achieve this, 28 cholinergic and 17 GABAergic neurons were patched. Parameters likely depending on M-current were investigated, as firing frequency, first interspike interval and adaptation index of an action potential train or amplitudes of fast, medium and slow AHPs. Using current-clamp mode of the whole-cell technique, 1-s-long square pulse current injections were applied with an amplitude of 50 and 100 pA, while the resting membrane potential was set to −60 mV (Figures 2A,B).


The M-current contributes to high threshold membrane potential oscillations in a cell type-specific way in the pedunculopontine nucleus of mice.

Bordas C, Kovacs A, Pal B - Front Cell Neurosci (2015)

The presence or absence of the M-current contributes to the electrophysiological differences between cholinergic and GABAergic neurons. (A) Train of action potentials recorded from a cholinergic neuron, elicited by 100 pA current injection (black). (B) Train of action potentials from a GABAergic neuron, elicited by the same stimulus (green). (C–E) Statistical comparison of electrophysiological parameters of cholinergic (black) and GABAergic (green) neurons. (C) Current injections elicit higher frequency of action potential firing from GABAergic neurons. (D) Cell type dependence of the first interspike interval (hollow circles: individual data; black squares: average ± SEM). (E) Cell type-dependent changes of the adaptation index (see text; hollow circles: individual data; black squares: average ± SEM). (F,G) Cell type dependence of the amplitudes of afterhyperpolarizations (AHPs). (F) Voltage traces from a cholinergic (black) and a GABAergic (green) neuron. Dashed lines indicate the points where the fast, medium and slow AHPs were determined. (G) Statistical comparison of fast (fAHP), medium (mAHP) and slow AHPs (sAHP). Black: cholinergic; green: GABAergic. (H) Train of action potentials recorded from another cholinergic neuron, recorded under control conditions (black). (I) Train of action potentials recorded from another cholinergic neuron, recorded in the presence of 20 μM XE991 (red). (J–L) Statistical comparison of electrophysiological parameters of cholinergic neurons under control conditions (black) and with 20 μM XE991 (red). (J) Current injections elicit higher frequency of action potential firing in the presence of XE991. (K) Changes of the first interspike interval by application of XE991 (hollow circles: individual data; black squares: average ± SEM). (L) changes of the adaptation index with application of XE991 (see text; hollow circles: individual data; black squares: average ± SEM). (M,N) Effect of XE991 on the amplitudes of AHPs. (M) Voltage traces from a cholinergic neuron under control conditions (black) and in the presence of XE991 (red). Dashed lines indicate the points where the fast, medium and slow AHPs were determined. (N) Statistical comparison of fast (fAHP), medium (mAHP) and slow AHPs (sAHP). Black: control; red: XE991.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
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Figure 2: The presence or absence of the M-current contributes to the electrophysiological differences between cholinergic and GABAergic neurons. (A) Train of action potentials recorded from a cholinergic neuron, elicited by 100 pA current injection (black). (B) Train of action potentials from a GABAergic neuron, elicited by the same stimulus (green). (C–E) Statistical comparison of electrophysiological parameters of cholinergic (black) and GABAergic (green) neurons. (C) Current injections elicit higher frequency of action potential firing from GABAergic neurons. (D) Cell type dependence of the first interspike interval (hollow circles: individual data; black squares: average ± SEM). (E) Cell type-dependent changes of the adaptation index (see text; hollow circles: individual data; black squares: average ± SEM). (F,G) Cell type dependence of the amplitudes of afterhyperpolarizations (AHPs). (F) Voltage traces from a cholinergic (black) and a GABAergic (green) neuron. Dashed lines indicate the points where the fast, medium and slow AHPs were determined. (G) Statistical comparison of fast (fAHP), medium (mAHP) and slow AHPs (sAHP). Black: cholinergic; green: GABAergic. (H) Train of action potentials recorded from another cholinergic neuron, recorded under control conditions (black). (I) Train of action potentials recorded from another cholinergic neuron, recorded in the presence of 20 μM XE991 (red). (J–L) Statistical comparison of electrophysiological parameters of cholinergic neurons under control conditions (black) and with 20 μM XE991 (red). (J) Current injections elicit higher frequency of action potential firing in the presence of XE991. (K) Changes of the first interspike interval by application of XE991 (hollow circles: individual data; black squares: average ± SEM). (L) changes of the adaptation index with application of XE991 (see text; hollow circles: individual data; black squares: average ± SEM). (M,N) Effect of XE991 on the amplitudes of AHPs. (M) Voltage traces from a cholinergic neuron under control conditions (black) and in the presence of XE991 (red). Dashed lines indicate the points where the fast, medium and slow AHPs were determined. (N) Statistical comparison of fast (fAHP), medium (mAHP) and slow AHPs (sAHP). Black: control; red: XE991.
Mentions: In order to achieve this, 28 cholinergic and 17 GABAergic neurons were patched. Parameters likely depending on M-current were investigated, as firing frequency, first interspike interval and adaptation index of an action potential train or amplitudes of fast, medium and slow AHPs. Using current-clamp mode of the whole-cell technique, 1-s-long square pulse current injections were applied with an amplitude of 50 and 100 pA, while the resting membrane potential was set to −60 mV (Figures 2A,B).

Bottom Line: Blockade of the M-current abolished the oscillatory activity at 20 Hz, and largely diminished it at other frequencies.Taken together, the M-current seems to be characteristic for PPN cholinergic neurons.It provides a possibility for modulating gamma band activity of these cells, thus contributing to neuromodulatory regulation of the reticular activating system.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Medicine, Department of Physiology, University of Debrecen Debrecen, Hungary.

ABSTRACT
The pedunculopontine nucleus is known as a cholinergic nucleus of the reticular activating system, participating in regulation of sleep and wakefulness. Besides cholinergic neurons, it consists of GABAergic and glutamatergic neurons as well. According to classical and recent studies, more subgroups of neurons were defined. Groups based on the neurotransmitter released by a neuron are not homogenous, but can be further subdivided. The PPN neurons do not only provide cholinergic and non-cholinergic inputs to several subcortical brain areas but they are also targets of cholinergic and other different neuromodulatory actions. Although cholinergic neuromodulation has been already investigated in the nucleus, one of its characteristic targets, the M-type potassium current has not been described yet. Using slice electrophysiology, we provide evidence in the present work that cholinergic neurons possess M-current, whereas GABAergic neurons lack it. The M-current contributes to certain functional differences of cholinergic and GABAergic neurons, as spike frequency adaptation, action potential firing frequency or the amplitude difference of medium afterhyperpolarizations (AHPs). Furthermore, we showed that high threshold membrane potential oscillation with high power, around 20 Hz frequency is a functional property of almost all cholinergic cells, whereas GABAergic neurons have only low amplitude oscillations. Blockade of the M-current abolished the oscillatory activity at 20 Hz, and largely diminished it at other frequencies. Taken together, the M-current seems to be characteristic for PPN cholinergic neurons. It provides a possibility for modulating gamma band activity of these cells, thus contributing to neuromodulatory regulation of the reticular activating system.

No MeSH data available.


Related in: MedlinePlus