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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

High threshold membrane potential oscillations are affected by the M-current. (A) Representative voltage trace from a cholinergic cell elicited by a ramp of depolarizing current injection under control conditions. (B) Voltage trace from the same neuron in the presence of TTX. (C) High threshold oscillation recorded from a cholinergic neuron in the presence of TTX. (D) High threshold oscillation recorded from a GABAergic neuron in the presence of TTX. (E) Power spectrum of the oscillatory activity of the cholinergic neuron shown on panel (C). (F) Power spectrum of the oscillatory activity of the GABAergic neuron shown on panel (D). (G) Statistical summary of the power spectra of all recorded neurons (average ± SEM). Black: cholinergic, green: GABAergic. The black line indicates the frequency range where significant difference was found between datasets obtained from cholinergic and GABAergic neurons. (H) Power peaks plotted against the frequencies at the power maximum (black: cholinergic; green: GABAergic neurons). (I) High threshold oscillation recorded from another cholinergic neuron in the presence of TTX. (J) Records from the same neuron in the presence of 20 μM XE991. (K) Power spectrum of the oscillatory activity of the cholinergic neuron shown on panel (I). (L) Power spectrum of the oscillatory activity with XE991, shown on panel (J). (M) Statistical summary of the power spectra of all cholinergic neurons under control conditions (black) and with XE991 (red; average ± SEM). (N) Comparison of power spectra of cholinergic neurons in the presence of XE991 (red) and GABAergic neurons (green; average ± SEM). Black lines of panels (M,N) indicate the frequency ranges where statistical differences were found between the two examined populations of data. Dashed lines of panels (A–D) and (I,J) indicate 0 mV.
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Figure 3: High threshold membrane potential oscillations are affected by the M-current. (A) Representative voltage trace from a cholinergic cell elicited by a ramp of depolarizing current injection under control conditions. (B) Voltage trace from the same neuron in the presence of TTX. (C) High threshold oscillation recorded from a cholinergic neuron in the presence of TTX. (D) High threshold oscillation recorded from a GABAergic neuron in the presence of TTX. (E) Power spectrum of the oscillatory activity of the cholinergic neuron shown on panel (C). (F) Power spectrum of the oscillatory activity of the GABAergic neuron shown on panel (D). (G) Statistical summary of the power spectra of all recorded neurons (average ± SEM). Black: cholinergic, green: GABAergic. The black line indicates the frequency range where significant difference was found between datasets obtained from cholinergic and GABAergic neurons. (H) Power peaks plotted against the frequencies at the power maximum (black: cholinergic; green: GABAergic neurons). (I) High threshold oscillation recorded from another cholinergic neuron in the presence of TTX. (J) Records from the same neuron in the presence of 20 μM XE991. (K) Power spectrum of the oscillatory activity of the cholinergic neuron shown on panel (I). (L) Power spectrum of the oscillatory activity with XE991, shown on panel (J). (M) Statistical summary of the power spectra of all cholinergic neurons under control conditions (black) and with XE991 (red; average ± SEM). (N) Comparison of power spectra of cholinergic neurons in the presence of XE991 (red) and GABAergic neurons (green; average ± SEM). Black lines of panels (M,N) indicate the frequency ranges where statistical differences were found between the two examined populations of data. Dashed lines of panels (A–D) and (I,J) indicate 0 mV.

Mentions: In order to elicit these oscillations, 1 s long current ramp injections were used with a maximal amplitude of 800 pA (Figure 3A). Adding 1 μM TTX, action potentials were blocked and only high threshold oscillations were recorded (Figure 3B). Oscillations fell in a frequency range of 10–45 Hz.


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)

High threshold membrane potential oscillations are affected by the M-current. (A) Representative voltage trace from a cholinergic cell elicited by a ramp of depolarizing current injection under control conditions. (B) Voltage trace from the same neuron in the presence of TTX. (C) High threshold oscillation recorded from a cholinergic neuron in the presence of TTX. (D) High threshold oscillation recorded from a GABAergic neuron in the presence of TTX. (E) Power spectrum of the oscillatory activity of the cholinergic neuron shown on panel (C). (F) Power spectrum of the oscillatory activity of the GABAergic neuron shown on panel (D). (G) Statistical summary of the power spectra of all recorded neurons (average ± SEM). Black: cholinergic, green: GABAergic. The black line indicates the frequency range where significant difference was found between datasets obtained from cholinergic and GABAergic neurons. (H) Power peaks plotted against the frequencies at the power maximum (black: cholinergic; green: GABAergic neurons). (I) High threshold oscillation recorded from another cholinergic neuron in the presence of TTX. (J) Records from the same neuron in the presence of 20 μM XE991. (K) Power spectrum of the oscillatory activity of the cholinergic neuron shown on panel (I). (L) Power spectrum of the oscillatory activity with XE991, shown on panel (J). (M) Statistical summary of the power spectra of all cholinergic neurons under control conditions (black) and with XE991 (red; average ± SEM). (N) Comparison of power spectra of cholinergic neurons in the presence of XE991 (red) and GABAergic neurons (green; average ± SEM). Black lines of panels (M,N) indicate the frequency ranges where statistical differences were found between the two examined populations of data. Dashed lines of panels (A–D) and (I,J) indicate 0 mV.
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Related In: Results  -  Collection

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Figure 3: High threshold membrane potential oscillations are affected by the M-current. (A) Representative voltage trace from a cholinergic cell elicited by a ramp of depolarizing current injection under control conditions. (B) Voltage trace from the same neuron in the presence of TTX. (C) High threshold oscillation recorded from a cholinergic neuron in the presence of TTX. (D) High threshold oscillation recorded from a GABAergic neuron in the presence of TTX. (E) Power spectrum of the oscillatory activity of the cholinergic neuron shown on panel (C). (F) Power spectrum of the oscillatory activity of the GABAergic neuron shown on panel (D). (G) Statistical summary of the power spectra of all recorded neurons (average ± SEM). Black: cholinergic, green: GABAergic. The black line indicates the frequency range where significant difference was found between datasets obtained from cholinergic and GABAergic neurons. (H) Power peaks plotted against the frequencies at the power maximum (black: cholinergic; green: GABAergic neurons). (I) High threshold oscillation recorded from another cholinergic neuron in the presence of TTX. (J) Records from the same neuron in the presence of 20 μM XE991. (K) Power spectrum of the oscillatory activity of the cholinergic neuron shown on panel (I). (L) Power spectrum of the oscillatory activity with XE991, shown on panel (J). (M) Statistical summary of the power spectra of all cholinergic neurons under control conditions (black) and with XE991 (red; average ± SEM). (N) Comparison of power spectra of cholinergic neurons in the presence of XE991 (red) and GABAergic neurons (green; average ± SEM). Black lines of panels (M,N) indicate the frequency ranges where statistical differences were found between the two examined populations of data. Dashed lines of panels (A–D) and (I,J) indicate 0 mV.
Mentions: In order to elicit these oscillations, 1 s long current ramp injections were used with a maximal amplitude of 800 pA (Figure 3A). Adding 1 μM TTX, action potentials were blocked and only high threshold oscillations were recorded (Figure 3B). Oscillations fell in a frequency range of 10–45 Hz.

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