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

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      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.

      DOI: http://dx.doi.org/10.7554/eLife.07224.001

      eLife digest

      Even when we are not engaged in any specific task, the brain shows coordinated patterns of spontaneous activity that can be monitored using electrodes placed on the scalp. This resting activity shapes the way that the brain responds to subsequent stimuli. Changes in resting activity patterns are seen in various neurological and psychiatric disorders, as well as in healthy individuals following sleep deprivation.

      The brain's outer layer is known as the cortex. On a large scale, when monitoring many thousands of neurons, resting activity in the cortex demonstrates propagation in the brain in an organized manner. Specifically, resting activity was found to organize as so-called neuronal avalanches, in which large bursts of neuronal activity are grouped with medium-sized and smaller bursts in a very characteristic order. In fact, the sizes of these bursts—that is, the number of neurons that fire—are found to be scale-invariant, that is, the ratio of large bursts to medium-sized bursts is the same as that of medium-sized to small bursts. Such scale-invariance suggests that neuronal bursts are not independent of one another. However, it is largely unclear how neuronal avalanches arise from individual neurons, which fire simply in a noisy, irregular manner.

      Bellay, Klaus et al. have now provided insights into this process by examining patterns of firing of a particular type of neuron—known as a pyramidal cell—in the cortex of rats as they recover from anesthesia. As the animals awaken, the firing of individual pyramidal cells in the cortex becomes even more irregular than under anesthesia. However, by considering the activity of a group of these neurons, Bellay, Klaus et al. realized that it is this more irregular firing that gives rise to neuronal avalanches, and that this occurs only when the animals are awake. Further experiments on individual pyramidal cells grown in the laboratory confirmed that neuronal avalanches emerge spontaneously from the irregular firing of individual neurons. These avalanches depend on there being a balance between two types of activity among the cells: ‘excitatory’ activity that causes other neurons to fire, and ‘inhibitory’ activity that prevents neuronal firing.

      Given that resting activity influences the brain's responses to the outside world, the origins of neuronal avalanches are likely to provide clues about the way the brain processes information. Future experiments should also examine the possibility that the emergence of neuronal avalanches marks the transition from unconsciousness to wakefulness within the brain.

      DOI: http://dx.doi.org/10.7554/eLife.07224.002

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      Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging.

      The majority of functional neuroscience studies have focused on the brain's response to a task or stimulus. However, the brain is very active even in the absence of explicit input or output. In this Article we review recent studies examining spontaneous fluctuations in the blood oxygen level dependent (BOLD) signal of functional magnetic resonance imaging as a potentially important and revealing manifestation of spontaneous neuronal activity. Although several challenges remain, these studies have provided insight into the intrinsic functional architecture of the brain, variability in behaviour and potential physiological correlates of neurological and psychiatric disease.
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        Power-law distributions in empirical data

        Power-law distributions occur in many situations of scientific interest and have significant consequences for our understanding of natural and man-made phenomena. Unfortunately, the detection and characterization of power laws is complicated by the large fluctuations that occur in the tail of the distribution -- the part of the distribution representing large but rare events -- and by the difficulty of identifying the range over which power-law behavior holds. Commonly used methods for analyzing power-law data, such as least-squares fitting, can produce substantially inaccurate estimates of parameters for power-law distributions, and even in cases where such methods return accurate answers they are still unsatisfactory because they give no indication of whether the data obey a power law at all. Here we present a principled statistical framework for discerning and quantifying power-law behavior in empirical data. Our approach combines maximum-likelihood fitting methods with goodness-of-fit tests based on the Kolmogorov-Smirnov statistic and likelihood ratios. We evaluate the effectiveness of the approach with tests on synthetic data and give critical comparisons to previous approaches. We also apply the proposed methods to twenty-four real-world data sets from a range of different disciplines, each of which has been conjectured to follow a power-law distribution. In some cases we find these conjectures to be consistent with the data while in others the power law is ruled out.
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          Default-mode network activity distinguishes Alzheimer's disease from healthy aging: evidence from functional MRI.

          Recent functional imaging studies have revealed coactivation in a distributed network of cortical regions that characterizes the resting state, or default mode, of the human brain. Among the brain regions implicated in this network, several, including the posterior cingulate cortex and inferior parietal lobes, have also shown decreased metabolism early in the course of Alzheimer's disease (AD). We reasoned that default-mode network activity might therefore be abnormal in AD. To test this hypothesis, we used independent component analysis to isolate the network in a group of 13 subjects with mild AD and in a group of 13 age-matched elderly controls as they performed a simple sensory-motor processing task. Three important findings are reported. Prominent coactivation of the hippocampus, detected in all groups, suggests that the default-mode network is closely involved with episodic memory processing. The AD group showed decreased resting-state activity in the posterior cingulate and hippocampus, suggesting that disrupted connectivity between these two regions accounts for the posterior cingulate hypometabolism commonly detected in positron emission tomography studies of early AD. Finally, a goodness-of-fit analysis applied at the individual subject level suggests that activity in the default-mode network may ultimately prove a sensitive and specific biomarker for incipient AD.
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            Author and article information

            Affiliations
            [1 ]deptSection on Critical Brain Dynamics , National Institute of Mental Health , Bethesda, United States
            University Health Network, and University of Toronto , Canada
            University Health Network, and University of Toronto , Canada
            Author notes
            [* ]For correspondence: plenzd@ 123456mail.nih.gov
            [†]

            These authors contributed equally to this work.

            Contributors
            Role: Reviewing editor,
            University Health Network, and University of Toronto , Canada
            Journal
            eLife
            eLife
            eLife
            eLife
            eLife Sciences Publications, Ltd
            2050-084X
            2050-084X
            07 July 2015
            2015
            : 4
            26151674
            4492006
            07224
            10.7554/eLife.07224
            (Reviewing editor)

            This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

            Product
            Funding
            Funded by: FundRef http://dx.doi.org/10.13039/100000025, National Institute of Mental Health (NIMH);
            Award ID: Division of Intramural Research
            Award Recipient :
            The funder had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
            Categories
            Research Article
            Neuroscience
            Custom metadata
            2.3
            Spontaneous, irregular spiking in single cortical pyramidal neurons assembles as neuronal avalanches at the group level identifying a robust scale-invariant organization of resting activity in the awake state.

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