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Irregular spiking of pyramidal neurons organizes as scale-invariant neuronal avalanches in the awake state.

Bellay T, Klaus A, Seshadri S, Plenz D - Elife (2015)

Bottom Line: As the animal transitions from the anesthetized to awake state, spontaneous single neuron firing increases in irregularity and assembles into scale-invariant avalanches at the group level.In vitro spike avalanches emerged naturally yet required balanced excitation and inhibition.This demonstrates that neuronal avalanches are linked to the global physiological state of wakefulness and that cortical resting activity organizes as avalanches from firing of local PN groups to global population activity.

View Article: PubMed Central - PubMed

Affiliation: Section on Critical Brain Dynamics, National Institute of Mental Health, Bethesda, United States.

ABSTRACT
Spontaneous fluctuations in neuronal activity emerge at many spatial and temporal scales in cortex. Population measures found these fluctuations to organize as scale-invariant neuronal avalanches, suggesting cortical dynamics to be critical. Macroscopic dynamics, though, depend on physiological states and are ambiguous as to their cellular composition, spatiotemporal origin, and contributions from synaptic input or action potential (AP) output. Here, we study spontaneous firing in pyramidal neurons (PNs) from rat superficial cortical layers in vivo and in vitro using 2-photon imaging. As the animal transitions from the anesthetized to awake state, spontaneous single neuron firing increases in irregularity and assembles into scale-invariant avalanches at the group level. In vitro spike avalanches emerged naturally yet required balanced excitation and inhibition. This demonstrates that neuronal avalanches are linked to the global physiological state of wakefulness and that cortical resting activity organizes as avalanches from firing of local PN groups to global population activity.

No MeSH data available.


Related in: MedlinePlus

Avalanche dynamics is robust to changes in λthr.(A–C) Cluster size distributions for Δt = 250, 167, and 88 ms (from left to right). The green distributions correspond to the respective thresholds, λthr = , at which the cluster rate was maximal.DOI:http://dx.doi.org/10.7554/eLife.07224.009
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fig4: Avalanche dynamics is robust to changes in λthr.(A–C) Cluster size distributions for Δt = 250, 167, and 88 ms (from left to right). The green distributions correspond to the respective thresholds, λthr = , at which the cluster rate was maximal.DOI:http://dx.doi.org/10.7554/eLife.07224.009

Mentions: For LFP-based avalanche dynamics, it has consistently been shown that power-law exponent and branching ratio increase systematically with temporal resolution Δt (Beggs and Plenz, 2003; Petermann et al., 2009). Importantly, for critical avalanche dynamics and negligible finite-size effects, the temporal resolution for which the power-law exponent, α, is −1.5 yields a branching ratio, σ, close to 1. As shown in Figure 3E, a similar relationship between α and σ was also found empirically for AP avalanches in vivo. Furthermore, the temporal organization of neuronal avalanches, that is, the avalanche life time, was shown to distribute according to a power law with exponent close to −2 (experimentally: [Beggs and Plenz, 2003]; simulations and theory: [Harris, 1989; Eurich et al., 2002]). Similarly, we found that the cluster lifetime, T, distributed according to a power law with slope close to −2 (Figure 3F; Δt = 250 ms, slope γ = 1.7 ± 0.1; Δt = 167 ms, γ = 1.9 ± 0.2; Δt = 88 ms, γ = 2.2 ± 0.2, LLR = 100.4–344.1; p < 0.001). To study the robustness of the power-law size distributions with respect to threshold, we systematically varied λthr around . In Figure 4, we show that the body of the distributions followed a power law up to the predicted cluster size limit (s = λ/Λ = 1 for the normalized distributions) beyond which a cut-off was observed. This cut-off was more pronounced at lower temporal resolutions and higher thresholds as shown previously for LFP-based avalanches (Yu et al., 2014). The threshold robustness and cut-off are in line with previous reports on avalanche dynamics in vitro (Beggs and Plenz, 2003) and in non-human primates (Petermann et al., 2009) and humans (Shriki et al., 2013).10.7554/eLife.07224.009Figure 4.Avalanche dynamics is robust to changes in λthr.


Irregular spiking of pyramidal neurons organizes as scale-invariant neuronal avalanches in the awake state.

Bellay T, Klaus A, Seshadri S, Plenz D - Elife (2015)

Avalanche dynamics is robust to changes in λthr.(A–C) Cluster size distributions for Δt = 250, 167, and 88 ms (from left to right). The green distributions correspond to the respective thresholds, λthr = , at which the cluster rate was maximal.DOI:http://dx.doi.org/10.7554/eLife.07224.009
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4492006&req=5

fig4: Avalanche dynamics is robust to changes in λthr.(A–C) Cluster size distributions for Δt = 250, 167, and 88 ms (from left to right). The green distributions correspond to the respective thresholds, λthr = , at which the cluster rate was maximal.DOI:http://dx.doi.org/10.7554/eLife.07224.009
Mentions: For LFP-based avalanche dynamics, it has consistently been shown that power-law exponent and branching ratio increase systematically with temporal resolution Δt (Beggs and Plenz, 2003; Petermann et al., 2009). Importantly, for critical avalanche dynamics and negligible finite-size effects, the temporal resolution for which the power-law exponent, α, is −1.5 yields a branching ratio, σ, close to 1. As shown in Figure 3E, a similar relationship between α and σ was also found empirically for AP avalanches in vivo. Furthermore, the temporal organization of neuronal avalanches, that is, the avalanche life time, was shown to distribute according to a power law with exponent close to −2 (experimentally: [Beggs and Plenz, 2003]; simulations and theory: [Harris, 1989; Eurich et al., 2002]). Similarly, we found that the cluster lifetime, T, distributed according to a power law with slope close to −2 (Figure 3F; Δt = 250 ms, slope γ = 1.7 ± 0.1; Δt = 167 ms, γ = 1.9 ± 0.2; Δt = 88 ms, γ = 2.2 ± 0.2, LLR = 100.4–344.1; p < 0.001). To study the robustness of the power-law size distributions with respect to threshold, we systematically varied λthr around . In Figure 4, we show that the body of the distributions followed a power law up to the predicted cluster size limit (s = λ/Λ = 1 for the normalized distributions) beyond which a cut-off was observed. This cut-off was more pronounced at lower temporal resolutions and higher thresholds as shown previously for LFP-based avalanches (Yu et al., 2014). The threshold robustness and cut-off are in line with previous reports on avalanche dynamics in vitro (Beggs and Plenz, 2003) and in non-human primates (Petermann et al., 2009) and humans (Shriki et al., 2013).10.7554/eLife.07224.009Figure 4.Avalanche dynamics is robust to changes in λthr.

Bottom Line: As the animal transitions from the anesthetized to awake state, spontaneous single neuron firing increases in irregularity and assembles into scale-invariant avalanches at the group level.In vitro spike avalanches emerged naturally yet required balanced excitation and inhibition.This demonstrates that neuronal avalanches are linked to the global physiological state of wakefulness and that cortical resting activity organizes as avalanches from firing of local PN groups to global population activity.

View Article: PubMed Central - PubMed

Affiliation: Section on Critical Brain Dynamics, National Institute of Mental Health, Bethesda, United States.

ABSTRACT
Spontaneous fluctuations in neuronal activity emerge at many spatial and temporal scales in cortex. Population measures found these fluctuations to organize as scale-invariant neuronal avalanches, suggesting cortical dynamics to be critical. Macroscopic dynamics, though, depend on physiological states and are ambiguous as to their cellular composition, spatiotemporal origin, and contributions from synaptic input or action potential (AP) output. Here, we study spontaneous firing in pyramidal neurons (PNs) from rat superficial cortical layers in vivo and in vitro using 2-photon imaging. As the animal transitions from the anesthetized to awake state, spontaneous single neuron firing increases in irregularity and assembles into scale-invariant avalanches at the group level. In vitro spike avalanches emerged naturally yet required balanced excitation and inhibition. This demonstrates that neuronal avalanches are linked to the global physiological state of wakefulness and that cortical resting activity organizes as avalanches from firing of local PN groups to global population activity.

No MeSH data available.


Related in: MedlinePlus