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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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Appearance of a population ISO in TC neurons following moderate activation of AchRs and/or mGluRs.A. Application of of 50 µM Cch induces spontaneous firing in a TC neuron that is modulated by an ISO at ∼0.03 Hz (second trace from top). The corresponding auto-correlogram and firing rate histogram are shown to the right and immediately below, respectively. Shown further below are enlarged sections from one of the firing episodes, as indicated, which reveal a mixture of tonic firing and HT bursts (blue bars). B. Firing rate histograms from three distinct, simultaneously recorded VB TC neurons (respective spike waveforms are shown to the far right) showing an ISO at ∼0.05 Hz in the presence of 100 µM trans-ACPD (See also Fig. S1). Note how the firing of neuron 3 (bottom plot, blue bars) generally peaks before that of neuron 1 (top plot, red bars) but that neuron 2 (middle plot, grey bars) seems to be directly linked by both cells (light red and light blue bars). The plots below show the respective cross-correlograms for the 3 possible neuron-neuron combinations as indicated. C. Intracellular recording of an LGN TC neuron which exhibits an ISO at ∼0.075 Hz following 50 µM Cch application. The corresponding auto-correlogram and firing rate histogram are shown to the right and immediately below, respectively, and enlarged sections are shown further below, as indicated (HT bursts indicated by blue bars). D. Histograms summarizing the effect of moderate (100 µM trans-ACPD or 50 µM Cch), combined (100 µM trans-ACPD and 50 µM Cch) and intense (200 µM trans-ACPD or 100 µM Cch) agonist application on ISO prevalence (left), percentage of ISOs involving HT bursting (middle) and ISO frequency (right).
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pone-0004447-g001: Appearance of a population ISO in TC neurons following moderate activation of AchRs and/or mGluRs.A. Application of of 50 µM Cch induces spontaneous firing in a TC neuron that is modulated by an ISO at ∼0.03 Hz (second trace from top). The corresponding auto-correlogram and firing rate histogram are shown to the right and immediately below, respectively. Shown further below are enlarged sections from one of the firing episodes, as indicated, which reveal a mixture of tonic firing and HT bursts (blue bars). B. Firing rate histograms from three distinct, simultaneously recorded VB TC neurons (respective spike waveforms are shown to the far right) showing an ISO at ∼0.05 Hz in the presence of 100 µM trans-ACPD (See also Fig. S1). Note how the firing of neuron 3 (bottom plot, blue bars) generally peaks before that of neuron 1 (top plot, red bars) but that neuron 2 (middle plot, grey bars) seems to be directly linked by both cells (light red and light blue bars). The plots below show the respective cross-correlograms for the 3 possible neuron-neuron combinations as indicated. C. Intracellular recording of an LGN TC neuron which exhibits an ISO at ∼0.075 Hz following 50 µM Cch application. The corresponding auto-correlogram and firing rate histogram are shown to the right and immediately below, respectively, and enlarged sections are shown further below, as indicated (HT bursts indicated by blue bars). D. Histograms summarizing the effect of moderate (100 µM trans-ACPD or 50 µM Cch), combined (100 µM trans-ACPD and 50 µM Cch) and intense (200 µM trans-ACPD or 100 µM Cch) agonist application on ISO prevalence (left), percentage of ISOs involving HT bursting (middle) and ISO frequency (right).

Mentions: Following the individual or combined application of moderate concentrations of the Group I/II mGluR agonist, trans-ACPD (100 µM) [25], [29] and/or the non-specific AchR agonist, carbachol (Cch) (50 µM) [27] we found that a subset of TC neurons (individual drug application: 14%, n = 27 of 192; combined drug application: 37%, n = 40 of 109) from the cat LGN, MGN and VB maintained in vitro exhibited spontaneous firing that was modulated by a prominent infra-slow (<0.1 Hz) oscillation (ISO) (individual drug application: 0.034±0.01 Hz; n = 11; combined drug application: 0.046±0.004 Hz; n = 20) (Fig. 1 and Figs. S1 and S2). This ISO was evident in both extracellular single unit and intracellular recordings and consisted of prolonged periods of waxing and waning action potential output (peak firing rate: 27.8±5.9 Hz; n = 11) that were usually separated by periods of quiescence (Fig. 1 and Figs. S1 and S2). This action potential output could comprise either episodes of tonic firing only (individual drug application: 41%, n = 11 of 27; combined drug application: 45%, n = 18 of 40) (Fig. S1A), episodes of intermingled tonic firing and high-threshold (HT) bursts (individual drug application: 48%, n = 13 of 27; combined drug application: 48%, n = 19 of 40) (Figs. 1A, 1C and Fig. S1C) or periods of HT bursts only (individual drug application: 11%, n = 3 of 27; combined drug application: 7%, n = 3 of 40) (Fig. S1B). In most instances, ISOs were highly rhythmic (e.g. Fig. 2B and 2C), but could occasionally exhibit a more irregular appearance (e.g. Fig. 2A). Once established ISOs were extremely robust and could last for several hours.


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

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

Appearance of a population ISO in TC neurons following moderate activation of AchRs and/or mGluRs.A. Application of of 50 µM Cch induces spontaneous firing in a TC neuron that is modulated by an ISO at ∼0.03 Hz (second trace from top). The corresponding auto-correlogram and firing rate histogram are shown to the right and immediately below, respectively. Shown further below are enlarged sections from one of the firing episodes, as indicated, which reveal a mixture of tonic firing and HT bursts (blue bars). B. Firing rate histograms from three distinct, simultaneously recorded VB TC neurons (respective spike waveforms are shown to the far right) showing an ISO at ∼0.05 Hz in the presence of 100 µM trans-ACPD (See also Fig. S1). Note how the firing of neuron 3 (bottom plot, blue bars) generally peaks before that of neuron 1 (top plot, red bars) but that neuron 2 (middle plot, grey bars) seems to be directly linked by both cells (light red and light blue bars). The plots below show the respective cross-correlograms for the 3 possible neuron-neuron combinations as indicated. C. Intracellular recording of an LGN TC neuron which exhibits an ISO at ∼0.075 Hz following 50 µM Cch application. The corresponding auto-correlogram and firing rate histogram are shown to the right and immediately below, respectively, and enlarged sections are shown further below, as indicated (HT bursts indicated by blue bars). D. Histograms summarizing the effect of moderate (100 µM trans-ACPD or 50 µM Cch), combined (100 µM trans-ACPD and 50 µM Cch) and intense (200 µM trans-ACPD or 100 µM Cch) agonist application on ISO prevalence (left), percentage of ISOs involving HT bursting (middle) and ISO frequency (right).
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Related In: Results  -  Collection

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pone-0004447-g001: Appearance of a population ISO in TC neurons following moderate activation of AchRs and/or mGluRs.A. Application of of 50 µM Cch induces spontaneous firing in a TC neuron that is modulated by an ISO at ∼0.03 Hz (second trace from top). The corresponding auto-correlogram and firing rate histogram are shown to the right and immediately below, respectively. Shown further below are enlarged sections from one of the firing episodes, as indicated, which reveal a mixture of tonic firing and HT bursts (blue bars). B. Firing rate histograms from three distinct, simultaneously recorded VB TC neurons (respective spike waveforms are shown to the far right) showing an ISO at ∼0.05 Hz in the presence of 100 µM trans-ACPD (See also Fig. S1). Note how the firing of neuron 3 (bottom plot, blue bars) generally peaks before that of neuron 1 (top plot, red bars) but that neuron 2 (middle plot, grey bars) seems to be directly linked by both cells (light red and light blue bars). The plots below show the respective cross-correlograms for the 3 possible neuron-neuron combinations as indicated. C. Intracellular recording of an LGN TC neuron which exhibits an ISO at ∼0.075 Hz following 50 µM Cch application. The corresponding auto-correlogram and firing rate histogram are shown to the right and immediately below, respectively, and enlarged sections are shown further below, as indicated (HT bursts indicated by blue bars). D. Histograms summarizing the effect of moderate (100 µM trans-ACPD or 50 µM Cch), combined (100 µM trans-ACPD and 50 µM Cch) and intense (200 µM trans-ACPD or 100 µM Cch) agonist application on ISO prevalence (left), percentage of ISOs involving HT bursting (middle) and ISO frequency (right).
Mentions: Following the individual or combined application of moderate concentrations of the Group I/II mGluR agonist, trans-ACPD (100 µM) [25], [29] and/or the non-specific AchR agonist, carbachol (Cch) (50 µM) [27] we found that a subset of TC neurons (individual drug application: 14%, n = 27 of 192; combined drug application: 37%, n = 40 of 109) from the cat LGN, MGN and VB maintained in vitro exhibited spontaneous firing that was modulated by a prominent infra-slow (<0.1 Hz) oscillation (ISO) (individual drug application: 0.034±0.01 Hz; n = 11; combined drug application: 0.046±0.004 Hz; n = 20) (Fig. 1 and Figs. S1 and S2). This ISO was evident in both extracellular single unit and intracellular recordings and consisted of prolonged periods of waxing and waning action potential output (peak firing rate: 27.8±5.9 Hz; n = 11) that were usually separated by periods of quiescence (Fig. 1 and Figs. S1 and S2). This action potential output could comprise either episodes of tonic firing only (individual drug application: 41%, n = 11 of 27; combined drug application: 45%, n = 18 of 40) (Fig. S1A), episodes of intermingled tonic firing and high-threshold (HT) bursts (individual drug application: 48%, n = 13 of 27; combined drug application: 48%, n = 19 of 40) (Figs. 1A, 1C and Fig. S1C) or periods of HT bursts only (individual drug application: 11%, n = 3 of 27; combined drug application: 7%, n = 3 of 40) (Fig. S1B). In most instances, ISOs were highly rhythmic (e.g. Fig. 2B and 2C), but could occasionally exhibit a more irregular appearance (e.g. Fig. 2A). Once established ISOs were extremely robust and could last for several hours.

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