Signatures of brain criticality unveiled by maximum entropy analysis across cortical states
Nastaran Lotfi, Antonio J. Fontenele, Thaís Feliciano, Leandro A. A. Aguiar, Nivaldo A. P. de Vasconcelos, Carina Soares-Cunha, Bárbara Coimbra, Ana João Rodrig… 展开作者
Nastaran Lotfi, Antonio J. Fontenele, Thaís Feliciano, Leandro A. A. Aguiar, Nivaldo A. P. de Vasconcelos, Carina Soares-Cunha, Bárbara Coimbra, Ana João Rodrigues, Nuno Sousa, Mauro Copelli, Pedro V. Carelli
It has recently been reported that statistical signatures of brain criticality, obtained from distributions of neuronal avalanches, can depend on the cortical state. We revisit these claims with a completely different and independent approach, employing a maximum entropy model to test whether signatures of criticality appear in urethane-anesthetized rats. To account for the spontaneous variation of cortical state, we parse the time series and perform the maximum entropy analysis as a function of the variability of the population spiking activity. To compare data sets with different number of neurons, we define a normalized distance to criticality that takes into account the peak and width of the specific heat curve. We found an universal collapse of the normalized distance to criticality dependence on the cortical state on an animal by animal basis. This indicates a universal dynamics and a critical point at an intermediate value of spiking variability.
Many studies have found evidence that the brain operates at a critical point, a processus known as self-organized criticality. A recent paper found remarkable scalings suggestive of criticality in systems as different as neural cultures, anesthetized or awake brains. We point out here that the diversity of these states would question any claimed role of criticality in information processing. Furthermore, we show that two non-critical systems pass all the tests for criticality, a control that was not provided in the original article. We conclude that such false positives demonstrate that the pr…
There are indications that for optimizing neural computation, neural networks - including the brain - operate at criticality. Previous approaches have, however, used diverse fingerprints of criticality, leaving open the question whether they refer to a unique critical point or whether there could be several. Using a recurrent spiking neural network as the model, we demonstrate that avalanche criticality does not necessarily lie at the dynamical edge-of-chaos and that therefore, the different fingerprints indicate distinct phenomena with an as yet unclarified relationship.
Complex systems are typically characterized as an intermediate situation between a complete regular structure and a random system. Brain signals can be studied as a striking example of such systems: cortical states can range from highly synchronous and ordered neuronal activity (with higher spiking variability) to desynchronized and disordered regimes (with lower spiking variability). It has been recently shown, by testing independent signatures of criticality, that a phase transition occurs in a cortical state of intermediate spiking variability. Here, we use a symbolic information approach t…
The branching process is the minimal model for propagation dynamics, avalanches and criticality, broadly used in neuroscience. A simple extension of it, adding inhibitory nodes, induces a much-richer phenomenology, including, an intermediate phase, between quiescence and saturation, that exhibits the key features of "asynchronous states" in cortical networks. Remarkably, in the inhibition-dominated case, it exhibits an extremely-rich phase diagram, that captures a wealth of non-trivial features of spontaneous brain activity, such as collective excitability, hysteresis, tilted avalanche shapes,…
Epileptic seizures are characterized by abnormal and excessive neural activity, where cortical network dynamics seem to become unstable. However, most of the time, during seizure-free periods, cortex of epilepsy patients shows perfectly stable dynamics. This raises the question of how recurring instability can arise in the light of this stable default state. In this work, we examine two potential scenarios of seizure generation: (i) epileptic cortical areas might generally operate closer to instability, which would make epilepsy patients generally more susceptible to seizures, or (ii) epilepti…
Spontaneous neuronal activity is a ubiquitous feature of cortex. Its spatiotemporal organization reflects past input and modulates future network output. Here we study whether a particular type of spontaneous activity is generated by a network that is optimized for input processing. Neuronal avalanches are a type of spontaneous activity observed in superficial cortical layers in vitro and in vivo with statistical properties expected from a network in a 'critical state'. Theory predicts that the critical state and, therefore, neuronal avalanches are optimal for input processing, but until now, …
Converging research suggests that the resting brain operates at the cusp of dynamic instability signified by scale-free temporal correlations. We asked if the scaling properties of these correlations differ between amplitude and phase fluctuations, which may reflect different aspects of cortical functioning. Using source-reconstructed magneto-encephalographic signals, we found power-law scaling for the collective amplitude and for phase synchronization, both capturing whole-brain activity. The temporal changes of the amplitude comprise slow, persistent memory processes, whereas phase synchroni…
The brain may be thought of as a many-body architecture with a spatio-temporal dynamics described by neuronal structures. The oscillatory nature of brain activity allows these structures (nodes) to be described as a set of coupled oscillators forming a network where the node dynamics, and that of the network topology can be studied. Quantifying its dynamics at various scales is an issue that claims to be explored for several brain activities, e.g., activity at rest. The resting-state associates the underlying brain dynamics of healthy subjects that are not actively compromised with sensory or …
Hallmarks of criticality, such as power-laws and scale invariance, have been empirically found in cortical networks and it has been conjectured that operating at criticality entails functional advantages, such as optimal computational capabilities, memory, and large dynamical ranges. As critical behavior requires a high degree of fine tuning to emerge, some type of self-tuning mechanism needs to be invoked. Here we show that, taking into account the complex hierarchical-modular architecture of cortical networks, the singular critical point is replaced by an extended critical-like region which …
A rigorous understanding of brain dynamics and function requires a conceptual bridge between multiple levels of organization, including neural spiking and network-level population activity. Mounting evidence suggests that neural networks of cerebral cortex operate at criticality. How operating near this network state impacts the variability of neuronal spiking is largely unknown. Here we show in a computational model that two prevalent features of cortical single-neuron activity, irregular spiking and the decline of response variability at stimulus onset, are both emergent properties of a recu…
Self-organized criticality (SOC) refers to the ability of complex systems to evolve towards a 2nd-order phase transition at which interactions between system components lead to scale-invariant events beneficial for system performance. For the last two decades, considerable experimental evidence accumulated that the mammalian cortex with its diversity in cell types and connections might exhibit SOC. Here we review experimental findings of isolated, layered cortex preparations to self-organize towards four dynamical motifs identified in the cortex in vivo: up-states, oscillations, neuronal avala…
Synchronization of brain activity fluctuations is believed to represent communication between spatially distant neural processes. These inter-areal functional interactions develop in the background of a complex network of axonal connections linking cortical and sub-cortical neurons, termed the human "structural connectome". Theoretical considerations and experimental evidence support the view that the human brain can be modeled as a system operating at a critical point between ordered (sub-critical) and disordered (super-critical) phases. Here, we explore the hypothesis that pathologies result…
Thermodynamic criticality describes emergent phenomena in a wide variety of complex systems. In the mammalian brain, the complex dynamics that spontaneously emerge from neuronal interactions have been characterized as neuronal avalanches, a form of critical branching dynamics. Here, we show that neuronal avalanches also reflect that the brain dynamics are organized close to a thermodynamic critical point. We recorded spontaneous cortical activity in monkeys and humans at rest using high-density intracranial microelectrode arrays and magnetoencephalography, respectively. By numerically changing…
The observation of critical-like behavior in cortical networks represents a major step forward in elucidating how the brain manages information. Understanding the origin and functionality of critical-like dynamics, as well as their robustness, is a major challenge in contemporary neuroscience. Here, we present an extensive numerical study of a family of simple dynamic models, which describe activity propagation in brain networks through the integration of different neighboring spiking potentials, mimicking basic neural interactions. The requirement of signal integration may lead to discontinuo…
Recent experimental results on spike avalanches measured in the urethane-anesthetized rat cortex have revealed scaling relations that indicate a phase transition at a specific level of cortical firing rate variability. The scaling relations point to critical exponents whose values differ from those of a branching process, which has been the canonical model employed to understand brain criticality. This suggested that a different model, with a different phase transition, might be required to explain the data. Here we show that this is not necessarily the case. By employing two different models …
