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

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