Self-organized criticality (SOC) refers to the ability of complex systems to evolve toward a second-order phase transition at which interactions between system components lead to scale-invariant events that are beneficial for system performance. For the last two decades, considerable experimental evidence has accumulated that the mammalian cortex with its diversity in cell types, interconnectivity, and plasticity might exhibit SOC. Here, we review the experimental findings of isolated, layered cortex preparations to self-organize toward four dynamical motifs presently identified in the intact cortex in vivo: up-states, oscillations, neuronal avalanches, and coherence potentials. During up-states, the synchronization observed for nested theta/gamma oscillations embeds scale-invariant neuronal avalanches, which can be identified by robust power law scaling in avalanche sizes with a slope of −3/2 and a critical branching parameter of 1. This precise dynamical coordination, tracked in the negative transients of the local field potential (nLFP) and spiking activity of pyramidal neurons using two-photon imaging, emerges autonomously in superficial layers of organotypic cortex cultures and acute cortex slices, is homeostatically regulated, exhibits separation of time scales, and reveals unique size vs. quiet time dependencies. A subclass of avalanches, the coherence potentials, exhibits precise maintenance of the time course in propagated local synchrony. Avalanches emerge in superficial layers of the cortex under conditions of strong external drive. The balance of excitation and inhibition (E/I), as well as neuromodulators such as dopamine, establishes powerful control parameters for avalanche dynamics. This rich dynamical repertoire is not observed in dissociated cortex cultures, which lack the differentiation into cortical layers and exhibit a dynamical phenotype expected for a first-order phase transition. The precise interactions between up-states, nested oscillations, and avalanches in superficial layers of the cortex provide compelling evidence for SOC in the brain.

Cortical neurons can be strongly or weakly coupled to the network in which they are embedded, firing in sync with the majority or firing independently. Both these scenarios have potential computational advantages in motor cortex. Commands to the body might be more robustly conveyed by a strongly coupled population, whereas a motor code with greater information capacity could be implemented by neurons that fire more independently. Which of these scenarios prevails? Here we measure neuron-to-body coupling and neuron-to-population coupling for neurons in motor cortex of freely moving rats. We find that neurons with high and low population coupling coexist, and that population coupling was tunable by manipulating inhibitory signaling. Importantly, neurons with different population coupling tend to serve different functional roles. Those with strong population coupling are not involved with body movement. In contrast, neurons with high neuron-to-body coupling are weakly coupled to other neurons in the cortical population.

Neurons in cortex synchronize their spiking in response to local and distant inputs. These synchronized assemblies are fundamental to cortex function, yet basic dynamical aspects about their size and duration are largely unknown. Using 2-photon imaging of neurons in superficial cortex of awake mice, we show that synchronized assemblies organize as scale-invariant avalanches that quadratically grow with duration. This quadratic expansion was found only for correlated neurons and required temporal coarse graining to compensate for spatial subsampling when network dynamics are critical, as demonstrated in simulations. The corresponding time course of an inverted parabola with an exponent of 2 described avalanches of up to 5 s duration and maximized temporal complexity in the ongoing activity of prefrontal and somatosensory cortex and in visual responses of primary visual cortex. Our results identify a scale-invariant order in the synchronization of highly diverse cortical cell assemblies in the form of parabolic avalanches.

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Significance How does brain function falter when inhibition is not properly balanced by excitation in cerebral cortex? Here we show in rats that excessive inhibition leads to stereotyped, low-complexity relationships among neurons in motor cortex and body movements. We observed similar phenomena in rats with disrupted MeCP2 function, suggesting that imbalanced inhibition may contribute to motor dysfunction in Rett syndrome.

Neurons in the cerebral cortex fire coincident action potentials during ongoing activity and in response to sensory inputs. These synchronized cell assemblies are fundamental to cortex function, yet basic dynamical aspects of their size and duration are largely unknown. Using 2-photon imaging of neurons in the superficial cortex of awake mice, we show that synchronized cell assemblies organize as scale-invariant avalanches that quadratically grow with duration. The quadratic avalanche scaling was only found for correlated neurons, required temporal coarse-graining to compensate for spatial subsampling of the imaged cortex, and suggested cortical dynamics to be critical as demonstrated in simulations of balanced E/I-networks. The corresponding time course of an inverted parabola with exponent of χ = 2 described cortical avalanches of coincident firing for up to 5 s duration over an area of 1 mm2. These parabolic avalanches maximized temporal complexity in the ongoing activity of prefrontal and somatosensory cortex and in visual responses of primary visual cortex. Our results identify a scale-invariant temporal order in the synchronization of highly diverse cortical cell assemblies in the form of parabolic avalanches.

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Rett syndrome (RTT) is a devastating neurodevelopmental disorder, caused by disruptions to the MECP2 gene, and resulting in severe cognitive and motor impairment. Previous work strongly suggests that healthy MECP2 function is required to have a normal balance between excitatory and inhibitory neurons. However, the details of how neural circuit dynamics and motor function are disrupted remain unclear. How might imbalanced E/I cause problems for motor function in RTT? We addressed this question in the motor cortex of awake, freely behaving rats, comparing normal rats with a transgenic rat model of RTT. We recorded single-unit spiking activity while simultaneously recording body movement of the rats. We found that RTT rats tend to have excessive synchrony among neurons in the motor cortex and less complex body movements. Importantly, greater synchrony was correlated with greater stereotypy of relationships between neurons and body movements. To further test how our observations were related to an E/I imbalance, we pharmacologically altered inhibitory synaptic interactions. We were able to recapitulate many of the phenomena we found in MECP2-deficient rats by enhancing inhibition in normal rats. Our results suggest that RTT-related E/I imbalance in the motor cortex gives rise to excessive synchrony and, consequently, a stereotyped motor code, which may underlie abnormal motor function in RTT.