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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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Following intense activation of AchRs or mGluRs the ISO can be associated with cyclic paroxysms.A. Simultaneous LFP and unit recording from the VB in the presence of 100 µM Cch showing an ISO at ∼0.03 Hz. The underlined section is enlarged below. Additional enlargements of the sections marked 1 and 2 are shown further below, as indicated, and reveal that LFP activity consists of a mixture of fast runs at ∼10 Hz corresponding to periods of tonic firing (1), and rhythmic SW/PSW complexes at ∼4 Hz (2) which are related to unusually powerful HT burst activity. In 1 and 2, the underlined sections are expanded to the immediate right. B. Simultaneous LFP and unit recording from the LGN in the presence of 200 µM trans-ACPD showing an ISO at ∼0.004 Hz. The underlined section is enlarged below. Additional enlargements of the sections marked 1 and 2 are shown further below, as indicated, and reveal that field activity consists of rhythmic SW/PSW complexes at ∼3 Hz which are closely related to HT burst activity in the simultaneously recorded TC neuron.
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pone-0004447-g003: Following intense activation of AchRs or mGluRs the ISO can be associated with cyclic paroxysms.A. Simultaneous LFP and unit recording from the VB in the presence of 100 µM Cch showing an ISO at ∼0.03 Hz. The underlined section is enlarged below. Additional enlargements of the sections marked 1 and 2 are shown further below, as indicated, and reveal that LFP activity consists of a mixture of fast runs at ∼10 Hz corresponding to periods of tonic firing (1), and rhythmic SW/PSW complexes at ∼4 Hz (2) which are related to unusually powerful HT burst activity. In 1 and 2, the underlined sections are expanded to the immediate right. B. Simultaneous LFP and unit recording from the LGN in the presence of 200 µM trans-ACPD showing an ISO at ∼0.004 Hz. The underlined section is enlarged below. Additional enlargements of the sections marked 1 and 2 are shown further below, as indicated, and reveal that field activity consists of rhythmic SW/PSW complexes at ∼3 Hz which are closely related to HT burst activity in the simultaneously recorded TC neuron.

Mentions: When applied individually, increasing the concentration of either trans-ACPD or Cch (to 200 µM and 100 µM, respectively) led to a slight increase in the percentage of cells showing ISOs (19%, n = 19 of 98; 200 µM trans-ACPD: 17%, n = 10 of 56; 100 µM Cch: 21%, n = 9 of 42) (Fig. 1D and Fig. S2). However, the mean frequency of these oscillations was significantly lower (0.015±0.003 Hz; range 0.004–0.04 Hz, n = 16; p<0.01) than during moderate application (Fig. 1D). Furthermore, following this more intense mGluR or AchR activation, recurrent episodes of firing were of a higher mean frequency (peak firing rate: 39.8.7±3.8 Hz; p<0.01; n = 12) and more commonly involved HT bursting (79%, n = 15 of 19) (Fig. 1D). Moreover, in this condition, these HT bursts were considerably more powerful (mean spikes per burst: 3.7±0.3 vs 2.2±0.1; p<0.01; n = 40 events) (Fig. 3A) and rather than being correlated with normal α rhythms, could be associated with cyclic paroxysmal activity [22], [23] in the LFP comprising recurring sequences of rhythmic spike wave (SW) and poly-spike wave (PSW) complexes at ∼2–4 Hz (mean frequency: 2.9±0.3 Hz; peak-to-peak amplitude: 268.2±85.0 µV; n = 5) that were sometimes intermingled with fast runs at ∼10–20 Hz (mean frequency: 14.1±3.8 Hz; peak-to-peak amplitude: 114.0±58.2 µV; n = 3) (Fig. 3A and B).


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

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

Following intense activation of AchRs or mGluRs the ISO can be associated with cyclic paroxysms.A. Simultaneous LFP and unit recording from the VB in the presence of 100 µM Cch showing an ISO at ∼0.03 Hz. The underlined section is enlarged below. Additional enlargements of the sections marked 1 and 2 are shown further below, as indicated, and reveal that LFP activity consists of a mixture of fast runs at ∼10 Hz corresponding to periods of tonic firing (1), and rhythmic SW/PSW complexes at ∼4 Hz (2) which are related to unusually powerful HT burst activity. In 1 and 2, the underlined sections are expanded to the immediate right. B. Simultaneous LFP and unit recording from the LGN in the presence of 200 µM trans-ACPD showing an ISO at ∼0.004 Hz. The underlined section is enlarged below. Additional enlargements of the sections marked 1 and 2 are shown further below, as indicated, and reveal that field activity consists of rhythmic SW/PSW complexes at ∼3 Hz which are closely related to HT burst activity in the simultaneously recorded TC neuron.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2637539&req=5

pone-0004447-g003: Following intense activation of AchRs or mGluRs the ISO can be associated with cyclic paroxysms.A. Simultaneous LFP and unit recording from the VB in the presence of 100 µM Cch showing an ISO at ∼0.03 Hz. The underlined section is enlarged below. Additional enlargements of the sections marked 1 and 2 are shown further below, as indicated, and reveal that LFP activity consists of a mixture of fast runs at ∼10 Hz corresponding to periods of tonic firing (1), and rhythmic SW/PSW complexes at ∼4 Hz (2) which are related to unusually powerful HT burst activity. In 1 and 2, the underlined sections are expanded to the immediate right. B. Simultaneous LFP and unit recording from the LGN in the presence of 200 µM trans-ACPD showing an ISO at ∼0.004 Hz. The underlined section is enlarged below. Additional enlargements of the sections marked 1 and 2 are shown further below, as indicated, and reveal that field activity consists of rhythmic SW/PSW complexes at ∼3 Hz which are closely related to HT burst activity in the simultaneously recorded TC neuron.
Mentions: When applied individually, increasing the concentration of either trans-ACPD or Cch (to 200 µM and 100 µM, respectively) led to a slight increase in the percentage of cells showing ISOs (19%, n = 19 of 98; 200 µM trans-ACPD: 17%, n = 10 of 56; 100 µM Cch: 21%, n = 9 of 42) (Fig. 1D and Fig. S2). However, the mean frequency of these oscillations was significantly lower (0.015±0.003 Hz; range 0.004–0.04 Hz, n = 16; p<0.01) than during moderate application (Fig. 1D). Furthermore, following this more intense mGluR or AchR activation, recurrent episodes of firing were of a higher mean frequency (peak firing rate: 39.8.7±3.8 Hz; p<0.01; n = 12) and more commonly involved HT bursting (79%, n = 15 of 19) (Fig. 1D). Moreover, in this condition, these HT bursts were considerably more powerful (mean spikes per burst: 3.7±0.3 vs 2.2±0.1; p<0.01; n = 40 events) (Fig. 3A) and rather than being correlated with normal α rhythms, could be associated with cyclic paroxysmal activity [22], [23] in the LFP comprising recurring sequences of rhythmic spike wave (SW) and poly-spike wave (PSW) complexes at ∼2–4 Hz (mean frequency: 2.9±0.3 Hz; peak-to-peak amplitude: 268.2±85.0 µV; n = 5) that were sometimes intermingled with fast runs at ∼10–20 Hz (mean frequency: 14.1±3.8 Hz; peak-to-peak amplitude: 114.0±58.2 µV; n = 3) (Fig. 3A and B).

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