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Register a new userA devils advocate view on self-organized brain criticality
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Authors
Claudius Gros
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Stationarity of the constituents of the body and of its functionalities is a basic requirement for life, being equivalent to survival in first place. Assuming that the resting state activity of the brain serves essential functionalities, stationarity entails that the dynamics of the brain needs to be regulated on a time-averaged basis. The combination of recurrent and driving external inputs must therefore lead to a non-trivial stationary neural activity, a condition which is fulfilled for afferent signals of varying strengths only close to criticality. In this view, the benefits of working vicinity of a second-order phase transition, such as signal enhancements, are not the underlying evolutionary drivers, but side effects of the requirement to keep the brain functional in first place. It is hence more appropriate to use the term self-regulated in this context, instead of self-organized.
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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 avalanches, and coherence potentials. During up-states, the synchronization observed for nested theta/gamma-oscillations embeds scale-invariant neuronal avalanches that exhibit robust power law scaling in size with a slope of -3/2 and a critical branching parameter of 1. This dynamical coordination, tracked in the local field potential (nLFP) and pyramidal neuron activity using 2-photon imaging, emerges autonomously in superficial layers of organotypic cortex cultures and acute cortex slices, is homeostatically regulated, displays separation of time scales, and reveals unique size vs. quiet time dependencies. A threshold operation identifies coherence potentials; avalanches that in addition maintain the precise time course of propagated synchrony. Avalanches emerge under conditions of external driving. Control parameters are established by the balance of excitation and inhibition (E/I) and the neuromodulator dopamine. This rich dynamical repertoire is not observed in dissociated cortex cultures, which lack cortical layers and exhibit dynamics similar to a 1st-order phase transition. The precise interactions between up-states, nested oscillations, avalanches, and coherence potentials in superficial cortical layers provide compelling evidence for SOC in the brain.
The well known Sandpile model of self-organized criticality generates avalanches of all length and time scales, without tuning any parameters. In the original models the external drive is randomly selected. Here we investigate a drive which depends on the present state of the system, namely the effect of favoring sites with a certain height in the deposition process. If sites with height three are favored, the system stays in a critical state. Our numerical results indicate the same universality class as the original model with random depositition, although the stationary state is approached very differently. In constrast, when favoring sites with height two, only avalanches which cover the entire system occur. Furthermore, we investigate the distributions of sites with a certain height, as well as the transient processes of the different variants of the external drive.
During slow-wave sleep, the brain is in a self-organized regime in which slow oscillations (SOs) between up- and down-states propagate across the cortex. We address the mechanism of how SOs emerge and can recruit large parts of the brain using a whole-brain model based on empirical connectivity data. Individual brain areas generate SOs that are induced by a local adaptation mechanism. Optimal fits to human resting-state fMRI data and EEG during deep sleep are found at critical values of the adaptation strength where the model produces a balance between local and global SOs with realistic spatiotemporal statistics. Local oscillations are more frequent, last shorter, and have a lower amplitude. Global oscillations spread as waves of silence across the brain, traveling from anterior to posterior regions due to the heterogeneous network structure of the human brain. Our results demonstrate the utility of whole-brain models for explaining the origin of large-scale cortical oscillations and how they are shaped by the connectome.
Introduced by the late Per Bak and his colleagues, self-organized criticality (SOC) has been one of the most stimulating concepts to come out of statistical mechanics and condensed matter theory in the last few decades, and has played a significant role in the development of complexity science. SOC, and more generally fractals and power laws, have attacted much comment, ranging from the very positive to the polemical. The other papers in this special issue (Aschwanden et al, 2014; McAteer et al, 2014; Sharma et al, 2015) showcase the considerable body of observations in solar, magnetospheric and fusion plasma inspired by the SOC idea, and expose the fertile role the new paradigm has played in approaches to modeling and understanding multiscale plasma instabilities. This very broad impact, and the necessary process of adapting a scientific hypothesis to the conditions of a given physical system, has meant that SOC as studied in these fields has sometimes differed significantly from the definition originally given by its creators. In Baks own field of theoretical physics there are significant observational and theoretical open questions, even 25 years on (Pruessner, 2012). One aim of the present review is to address the dichotomy between the great reception SOC has received in some areas, and its shortcomings, as they became manifest in the controversies it triggered. Our article tries to clear up what we think are misunderstandings of SOC in fields more remote from its origins in statistical mechanics, condensed matter and dynamical systems by revisiting Bak, Tang and Wiesenfelds original papers.
Self-organized bistability (SOB) is the counterpart of self-organized criticality (SOC), for systems tuning themselves to the edge of bistability of a discontinuous phase transition, rather than to the critical point of a continuous one. The equations defining the mathematical theory of SOB turn out to bear strong resemblance to a (Landau-Ginzburg) theory recently proposed to analyze the dynamics of the cerebral cortex. This theory describes the neuronal activity of coupled mesoscopic patches of cortex, homeostatically regulated by short-term synaptic plasticity. The theory for cortex dynamics entails, however, some significant differences with respect to SOB, including the lack of a (bulk) conservation law, the absence of a perfect separation of timescales and, the fact that in the former, but not in the second, there is a parameter that controls the overall system state (in blatant contrast with the very idea of self-organization). Here, we scrutinize --by employing a combination of analytical and computational tools-- the analogies and differences between both theories and explore whether in some limit SOB can play an important role to explain the emergence of scale-invariant neuronal avalanches observed empirically in the cortex. We conclude that, actually, in the limit of infinitely slow synaptic-dynamics, the two theories become identical, but the timescales required for the self-organization mechanism to be effective do not seem to be biologically plausible. We discuss the key differences between self-organization mechanisms with/without conservation and with/without infinitely separated timescales. In particular, we introduce the concept of self-organized collective oscillations and scrutinize the implications of our findings in neuroscience, shedding new light into the problems of scale invariance and oscillations in cortical dynamics.
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