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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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The ISO modulates network oscillations in the α (8–13 Hz) frequency band and can underlie cyclic paroxysms.A. Simultaneous LFP and multi-unit recording from the LGN in the presence of 50 µM Cch showing that the ISO in firing (bottom, MUA) is associated with a modulation of faster oscillations in the LFP (top). The sections labelled 1 and 2 are expanded below and reveal that the ∼13 Hz field oscillations are associated with HT bursts (blue arrows in expanded sections) that appear to drive activity in an additional tonic firing cell (red arrows in expanded sections) (see [27]). B. ISO at ∼0.1 Hz recorded intracellularly from an LGN TC neuron where the most depolarized phase of the oscillation is crowned not only by action potentials but also by a combination of spikelets and burstlets (green arrows in the enlarged section below). C. Top traces: LGN TC neuron recorded intracellularly showing continuous tonic firing (see enlarged section below). Bottom traces: application of 20 mM TMA brings about an ISO at ∼0.05 Hz. In this condition the cell also exhibits brief depolarizing events (green arrows) that occur just before and after the transient firing episodes (see enlargements as indicated).
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pone-0004447-g002: The ISO modulates network oscillations in the α (8–13 Hz) frequency band and can underlie cyclic paroxysms.A. Simultaneous LFP and multi-unit recording from the LGN in the presence of 50 µM Cch showing that the ISO in firing (bottom, MUA) is associated with a modulation of faster oscillations in the LFP (top). The sections labelled 1 and 2 are expanded below and reveal that the ∼13 Hz field oscillations are associated with HT bursts (blue arrows in expanded sections) that appear to drive activity in an additional tonic firing cell (red arrows in expanded sections) (see [27]). B. ISO at ∼0.1 Hz recorded intracellularly from an LGN TC neuron where the most depolarized phase of the oscillation is crowned not only by action potentials but also by a combination of spikelets and burstlets (green arrows in the enlarged section below). C. Top traces: LGN TC neuron recorded intracellularly showing continuous tonic firing (see enlarged section below). Bottom traces: application of 20 mM TMA brings about an ISO at ∼0.05 Hz. In this condition the cell also exhibits brief depolarizing events (green arrows) that occur just before and after the transient firing episodes (see enlargements as indicated).

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)

The ISO modulates network oscillations in the α (8–13 Hz) frequency band and can underlie cyclic paroxysms.A. Simultaneous LFP and multi-unit recording from the LGN in the presence of 50 µM Cch showing that the ISO in firing (bottom, MUA) is associated with a modulation of faster oscillations in the LFP (top). The sections labelled 1 and 2 are expanded below and reveal that the ∼13 Hz field oscillations are associated with HT bursts (blue arrows in expanded sections) that appear to drive activity in an additional tonic firing cell (red arrows in expanded sections) (see [27]). B. ISO at ∼0.1 Hz recorded intracellularly from an LGN TC neuron where the most depolarized phase of the oscillation is crowned not only by action potentials but also by a combination of spikelets and burstlets (green arrows in the enlarged section below). C. Top traces: LGN TC neuron recorded intracellularly showing continuous tonic firing (see enlarged section below). Bottom traces: application of 20 mM TMA brings about an ISO at ∼0.05 Hz. In this condition the cell also exhibits brief depolarizing events (green arrows) that occur just before and after the transient firing episodes (see enlargements as indicated).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2637539&req=5

pone-0004447-g002: The ISO modulates network oscillations in the α (8–13 Hz) frequency band and can underlie cyclic paroxysms.A. Simultaneous LFP and multi-unit recording from the LGN in the presence of 50 µM Cch showing that the ISO in firing (bottom, MUA) is associated with a modulation of faster oscillations in the LFP (top). The sections labelled 1 and 2 are expanded below and reveal that the ∼13 Hz field oscillations are associated with HT bursts (blue arrows in expanded sections) that appear to drive activity in an additional tonic firing cell (red arrows in expanded sections) (see [27]). B. ISO at ∼0.1 Hz recorded intracellularly from an LGN TC neuron where the most depolarized phase of the oscillation is crowned not only by action potentials but also by a combination of spikelets and burstlets (green arrows in the enlarged section below). C. Top traces: LGN TC neuron recorded intracellularly showing continuous tonic firing (see enlarged section below). Bottom traces: application of 20 mM TMA brings about an ISO at ∼0.05 Hz. In this condition the cell also exhibits brief depolarizing events (green arrows) that occur just before and after the transient firing episodes (see enlargements as indicated).
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