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ATP-dependent infra-slow (<0.1 Hz) oscillations in thalamic networks.

Lörincz ML, Geall F, Bao Y, Crunelli V, Hughes SW - PLoS ONE (2009)

Bottom Line: This ISO is a neuronal population phenomenon which modulates faster gap junction (GJ)-dependent network oscillations, and can underlie epileptic activity when AchRs or mGluRs are stimulated excessively.In individual thalamocortical neurons the ISO is primarily shaped by rhythmic, long-lasting hyperpolarizing potentials which reflect the activation of A1 receptors, by ATP-derived adenosine, and subsequent opening of Ba(2+)-sensitive K(+) channels.We argue that this ISO has a likely non-neuronal origin and may contribute to shaping ISOs in the intact brain.

View Article: PubMed Central - PubMed

Affiliation: School of Biosciences, Cardiff University, Cardiff, UK.

ABSTRACT
An increasing number of EEG and resting state fMRI studies in both humans and animals indicate that spontaneous low frequency fluctuations in cerebral activity at <0.1 Hz (infra-slow oscillations, ISOs) represent a fundamental component of brain functioning, being known to correlate with faster neuronal ensemble oscillations, regulate behavioural performance and influence seizure susceptibility. Although these oscillations have been commonly indicated to involve the thalamus their basic cellular mechanisms remain poorly understood. Here we show that various nuclei in the dorsal thalamus in vitro can express a robust ISO at approximately 0.005-0.1 Hz that is greatly facilitated by activating metabotropic glutamate receptors (mGluRs) and/or Ach receptors (AchRs). This ISO is a neuronal population phenomenon which modulates faster gap junction (GJ)-dependent network oscillations, and can underlie epileptic activity when AchRs or mGluRs are stimulated excessively. In individual thalamocortical neurons the ISO is primarily shaped by rhythmic, long-lasting hyperpolarizing potentials which reflect the activation of A1 receptors, by ATP-derived adenosine, and subsequent opening of Ba(2+)-sensitive K(+) channels. We argue that this ISO has a likely non-neuronal origin and may contribute to shaping ISOs in the intact brain.

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Response of the ISO to changes in membrane polarization and the presence of the ISO in LFP recordings.A. Intracellular recording of an ISO in a TC neuron in the LGN at different levels of steady current. Note that although ISO is mainly sculpted by long-lasting rhythmic hyperpolarizing potentials (green arrows in 3) it also involves depolarizing events (blue arrows in 3) (See also Figs. S5B and S5C). B. Plots showing that the amplitude (top) of the long-lasting hyperpolarizing potentials exhibited by the neuron in A is reduced as the cell is hyperpolarized but that the frequency (bottom) of the ISO is unaltered at ∼0.05 Hz. The traces to the right show enlarged examples of the long-lasting hyperpolarizing potentials in A (aligned at their start by the green dotted line at different levels of membrane polarization, red dotted line indicates the baseline membrane potential; numbers correspond to the traces in A). Note again the presence of additional depolarizing events (blue arrows). C. Simultaneous LFP and intracellular TC neuron recording of an ISO at ∼0.06 Hz (dark red trace) in the MGN (black trace) at different levels of steady injected current as indicated. The corresponding firing rate histogram is shown immediately below. Shown further below is an enlarged section of the recording (as indicated, action potentials truncated) illustrating that the negative peaks of the LFP (blue vertical lines) are coincident with a hyperpolarization and an accompanying suppression in firing in the TC neuron. B. Additional simultaneous LFP and intracellular TC neuron recording of an ISO at ∼0.083 Hz (red trace) obtained in the LGN. The traces to the right show the LFP negative peak-triggered averages for the LFP and membrane potential. (10 µM SR95531 and 10 µM CGP54626 were present for the recording shown in C).
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pone-0004447-g005: Response of the ISO to changes in membrane polarization and the presence of the ISO in LFP recordings.A. Intracellular recording of an ISO in a TC neuron in the LGN at different levels of steady current. Note that although ISO is mainly sculpted by long-lasting rhythmic hyperpolarizing potentials (green arrows in 3) it also involves depolarizing events (blue arrows in 3) (See also Figs. S5B and S5C). B. Plots showing that the amplitude (top) of the long-lasting hyperpolarizing potentials exhibited by the neuron in A is reduced as the cell is hyperpolarized but that the frequency (bottom) of the ISO is unaltered at ∼0.05 Hz. The traces to the right show enlarged examples of the long-lasting hyperpolarizing potentials in A (aligned at their start by the green dotted line at different levels of membrane polarization, red dotted line indicates the baseline membrane potential; numbers correspond to the traces in A). Note again the presence of additional depolarizing events (blue arrows). C. Simultaneous LFP and intracellular TC neuron recording of an ISO at ∼0.06 Hz (dark red trace) in the MGN (black trace) at different levels of steady injected current as indicated. The corresponding firing rate histogram is shown immediately below. Shown further below is an enlarged section of the recording (as indicated, action potentials truncated) illustrating that the negative peaks of the LFP (blue vertical lines) are coincident with a hyperpolarization and an accompanying suppression in firing in the TC neuron. B. Additional simultaneous LFP and intracellular TC neuron recording of an ISO at ∼0.083 Hz (red trace) obtained in the LGN. The traces to the right show the LFP negative peak-triggered averages for the LFP and membrane potential. (10 µM SR95531 and 10 µM CGP54626 were present for the recording shown in C).

Mentions: In order to better understand the cellular events underlying the ISO, we closely examined the temporal development of this phenomenon from a state of quiescence following moderate trans-ACPD and/or Cch application. In all cases, the emergence of the ISO was associated with a progressive increase in the occurrence and rhythmicity of a long-lasting hyperpolarizing potentials (amplitude at −60 mV: 6.9±1.0 mV; duration: 15.8±1.3 s; n = 16) until a stable ISO was established (Fig. 4A and B). In most cells, these potentials were highly conserved from cycle to cycle, often displayed a prominent biphasic waveform (time between the onset of the two phases: 4.1±0.09 s; n = 5) (Fig. 4B, see arrows; see also Fig. S4B) and were similar to those we have shown previously to occur in a small number (∼3%) of TC neurons in control conditions [30]. We also often observed additional relatively faster depolarizing events (amplitude: 4.3±0.4 mV; duration: 0.9±0.1 s; n = 20 events) that mainly occurred either just prior to the onset of the long-lasting hyperpolarizing potentials (Figs. 5A and B and Fig. S5B) or during their repolarizing phase (Fig. 2C and Fig. S5C). Thus, the ISO in individual TC neurons is fundamentally shaped by long-lasting rhythmic hyperpolarizing potentials but also involves relatively faster depolarizing events.


ATP-dependent infra-slow (<0.1 Hz) oscillations in thalamic networks.

Lörincz ML, Geall F, Bao Y, Crunelli V, Hughes SW - PLoS ONE (2009)

Response of the ISO to changes in membrane polarization and the presence of the ISO in LFP recordings.A. Intracellular recording of an ISO in a TC neuron in the LGN at different levels of steady current. Note that although ISO is mainly sculpted by long-lasting rhythmic hyperpolarizing potentials (green arrows in 3) it also involves depolarizing events (blue arrows in 3) (See also Figs. S5B and S5C). B. Plots showing that the amplitude (top) of the long-lasting hyperpolarizing potentials exhibited by the neuron in A is reduced as the cell is hyperpolarized but that the frequency (bottom) of the ISO is unaltered at ∼0.05 Hz. The traces to the right show enlarged examples of the long-lasting hyperpolarizing potentials in A (aligned at their start by the green dotted line at different levels of membrane polarization, red dotted line indicates the baseline membrane potential; numbers correspond to the traces in A). Note again the presence of additional depolarizing events (blue arrows). C. Simultaneous LFP and intracellular TC neuron recording of an ISO at ∼0.06 Hz (dark red trace) in the MGN (black trace) at different levels of steady injected current as indicated. The corresponding firing rate histogram is shown immediately below. Shown further below is an enlarged section of the recording (as indicated, action potentials truncated) illustrating that the negative peaks of the LFP (blue vertical lines) are coincident with a hyperpolarization and an accompanying suppression in firing in the TC neuron. B. Additional simultaneous LFP and intracellular TC neuron recording of an ISO at ∼0.083 Hz (red trace) obtained in the LGN. The traces to the right show the LFP negative peak-triggered averages for the LFP and membrane potential. (10 µM SR95531 and 10 µM CGP54626 were present for the recording shown in C).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2637539&req=5

pone-0004447-g005: Response of the ISO to changes in membrane polarization and the presence of the ISO in LFP recordings.A. Intracellular recording of an ISO in a TC neuron in the LGN at different levels of steady current. Note that although ISO is mainly sculpted by long-lasting rhythmic hyperpolarizing potentials (green arrows in 3) it also involves depolarizing events (blue arrows in 3) (See also Figs. S5B and S5C). B. Plots showing that the amplitude (top) of the long-lasting hyperpolarizing potentials exhibited by the neuron in A is reduced as the cell is hyperpolarized but that the frequency (bottom) of the ISO is unaltered at ∼0.05 Hz. The traces to the right show enlarged examples of the long-lasting hyperpolarizing potentials in A (aligned at their start by the green dotted line at different levels of membrane polarization, red dotted line indicates the baseline membrane potential; numbers correspond to the traces in A). Note again the presence of additional depolarizing events (blue arrows). C. Simultaneous LFP and intracellular TC neuron recording of an ISO at ∼0.06 Hz (dark red trace) in the MGN (black trace) at different levels of steady injected current as indicated. The corresponding firing rate histogram is shown immediately below. Shown further below is an enlarged section of the recording (as indicated, action potentials truncated) illustrating that the negative peaks of the LFP (blue vertical lines) are coincident with a hyperpolarization and an accompanying suppression in firing in the TC neuron. B. Additional simultaneous LFP and intracellular TC neuron recording of an ISO at ∼0.083 Hz (red trace) obtained in the LGN. The traces to the right show the LFP negative peak-triggered averages for the LFP and membrane potential. (10 µM SR95531 and 10 µM CGP54626 were present for the recording shown in C).
Mentions: In order to better understand the cellular events underlying the ISO, we closely examined the temporal development of this phenomenon from a state of quiescence following moderate trans-ACPD and/or Cch application. In all cases, the emergence of the ISO was associated with a progressive increase in the occurrence and rhythmicity of a long-lasting hyperpolarizing potentials (amplitude at −60 mV: 6.9±1.0 mV; duration: 15.8±1.3 s; n = 16) until a stable ISO was established (Fig. 4A and B). In most cells, these potentials were highly conserved from cycle to cycle, often displayed a prominent biphasic waveform (time between the onset of the two phases: 4.1±0.09 s; n = 5) (Fig. 4B, see arrows; see also Fig. S4B) and were similar to those we have shown previously to occur in a small number (∼3%) of TC neurons in control conditions [30]. We also often observed additional relatively faster depolarizing events (amplitude: 4.3±0.4 mV; duration: 0.9±0.1 s; n = 20 events) that mainly occurred either just prior to the onset of the long-lasting hyperpolarizing potentials (Figs. 5A and B and Fig. S5B) or during their repolarizing phase (Fig. 2C and Fig. S5C). Thus, the ISO in individual TC neurons is fundamentally shaped by long-lasting rhythmic hyperpolarizing potentials but also involves relatively faster depolarizing events.

Bottom Line: This ISO is a neuronal population phenomenon which modulates faster gap junction (GJ)-dependent network oscillations, and can underlie epileptic activity when AchRs or mGluRs are stimulated excessively.In individual thalamocortical neurons the ISO is primarily shaped by rhythmic, long-lasting hyperpolarizing potentials which reflect the activation of A1 receptors, by ATP-derived adenosine, and subsequent opening of Ba(2+)-sensitive K(+) channels.We argue that this ISO has a likely non-neuronal origin and may contribute to shaping ISOs in the intact brain.

View Article: PubMed Central - PubMed

Affiliation: School of Biosciences, Cardiff University, Cardiff, UK.

ABSTRACT
An increasing number of EEG and resting state fMRI studies in both humans and animals indicate that spontaneous low frequency fluctuations in cerebral activity at <0.1 Hz (infra-slow oscillations, ISOs) represent a fundamental component of brain functioning, being known to correlate with faster neuronal ensemble oscillations, regulate behavioural performance and influence seizure susceptibility. Although these oscillations have been commonly indicated to involve the thalamus their basic cellular mechanisms remain poorly understood. Here we show that various nuclei in the dorsal thalamus in vitro can express a robust ISO at approximately 0.005-0.1 Hz that is greatly facilitated by activating metabotropic glutamate receptors (mGluRs) and/or Ach receptors (AchRs). This ISO is a neuronal population phenomenon which modulates faster gap junction (GJ)-dependent network oscillations, and can underlie epileptic activity when AchRs or mGluRs are stimulated excessively. In individual thalamocortical neurons the ISO is primarily shaped by rhythmic, long-lasting hyperpolarizing potentials which reflect the activation of A1 receptors, by ATP-derived adenosine, and subsequent opening of Ba(2+)-sensitive K(+) channels. We argue that this ISO has a likely non-neuronal origin and may contribute to shaping ISOs in the intact brain.

Show MeSH
Related in: MedlinePlus