Relatively recent work has reported that networks of neurons can produce avalanches of activity whose sizes follow a power law distribution. This suggests that these networks may be operating near a critical point, poised between a phase where activity rapidly dies out and a phase where activity is amplified over time. The hypothesis that the electrical activity of neural networks in the brain is critical is potentially important, as many simulations suggest that information processing functions would be optimized at the critical point. This hypothesis, however, is still controversial. Here we will explain the concept of criticality and review the substantial objections to the criticality hypothesis raised by skeptics. Points and counter points are presented in dialog form.

Understanding how neural systems integrate, encode, and compute information is central to understanding brain function. Frequently, data from neuroscience experiments are multivariate, the interactions between the variables are nonlinear, and the landscape of hypothesized or possible interactions between variables is extremely broad. Information theory is well suited to address these types of data, as it possesses multivariate analysis tools, it can be applied to many different types of data, it can capture nonlinear interactions, and it does not require assumptions about the structure of the underlying data (i.e., it is model independent). In this article, we walk through the mathematics of information theory along with common logistical problems associated with data type, data binning, data quantity requirements, bias, and significance testing. Next, we analyze models inspired by canonical neuroscience experiments to improve understanding and demonstrate the strengths of information theory analyses. To facilitate the use of information theory analyses, and an understanding of how these analyses are implemented, we also provide a free MATLAB software package that can be applied to a wide range of data from neuroscience experiments, as well as from other fields of study.

The performance of complex networks, like the brain, depends on how effectively their elements communicate. Despite the importance of communication, it is virtually unknown how information is transferred in local cortical networks, consisting of hundreds of closely spaced neurons. To address this, it is important to record simultaneously from hundreds of neurons at a spacing that matches typical axonal connection distances, and at a temporal resolution that matches synaptic delays. We used a 512-electrode array (60 μm spacing) to record spontaneous activity at 20 kHz from up to 500 neurons simultaneously in slice cultures of mouse somatosensory cortex for 1 h at a time. We applied a previously validated version of transfer entropy to quantify information transfer. Similar toin vivoreports, we found an approximately lognormal distribution of firing rates. Pairwise information transfer strengths also were nearly lognormally distributed, similar to reports of synaptic strengths. Some neurons transferred and received much more information than others, which is consistent with previous predictions. Neurons with the highest outgoing and incoming information transfer were more strongly connected to each other than chance, thus forming a “rich club.” We found similar results in networks recordedin vivofrom rodent cortex, suggesting the generality of these findings. A rich-club structure has been found previously in large-scale human brain networks and is thought to facilitate communication between cortical regions. The discovery of a small, but information-rich, subset of neurons within cortical regions suggests that this population will play a vital role in communication, learning, and memory.SIGNIFICANCE STATEMENTMany studies have focused on communication networks between cortical brain regions. In contrast, very few studies have examined communication networks within a cortical region. This is the first study to combine such a large number of neurons (several hundred at a time) with such high temporal resolution (so we can know the direction of communication between neurons) for mapping networks within cortex. We found that information was not transferred equally through all neurons. Instead, ∼70% of the information passed through only 20% of the neurons. Network models suggest that this highly concentrated pattern of information transfer would be both efficient and robust to damage. Therefore, this work may help in understanding how the cortex processes information and responds to neurodegenerative diseases.

Neural systems include interactions that occur across many scales. Two divergent methods for characterizing such interactions have drawn on the physical analysis of critical phenomena and the mathematical study of information. Inferring criticality in neural systems has traditionally rested on fitting power laws to the property distributions of ''neural avalanches'' (contiguous bursts of activity), but the fractal nature of avalanche shapes has recently emerged as another signature of criticality. On the other hand, neural complexity, an information theoretic measure, has been used to capture the interplay between the functional localization of brain regions and their integration for higher cognitive functions. Unfortunately, treatments of all three methods - power-law fitting, avalanche shape collapse, and neural complexity – have suffered from shortcomings. Empirical data often contain biases that introduce deviations from true power law in the tail and head of the distribution, but deviations in the tail have often been unconsidered; avalanche shape collapse has required manual parameter tuning; and the estimation of neural complexity has relied on small data sets or statistical assumptions for the sake of computational efficiency. In this paper we present technical advancements in the analysis of criticality and complexity in neural systems. We use maximum-likelihood estimation to automatically fit power laws with left and right cutoffs, present the first automated shape collapse algorithm, and describe new techniques to account for large numbers of neural variables and small data sets in the calculation of neural complexity. In order to facilitate future research in criticality and complexity, we have made the software utilized in this analysis freely available online in the MATLAB NCC (Neural Complexity and Criticality) Toolbox.

Recent work has shown that functional connectivity among cortical neurons is highly varied, with a small percentage of neurons having many more connections than others. Also, recent theoretical developments now make it possible to quantify how neurons modify information from the connections they receive. Therefore, it is now possible to investigate how information modification, or computation, depends on the number of connections a neuron receives (in-degree) or sends out (out-degree). To do this, we recorded the simultaneous spiking activity of hundreds of neurons in cortico-hippocampal slice cultures using a high-density 512-electrode array. This preparation and recording method combination produced large numbers of neurons recorded at temporal and spatial resolutions that are not currently available in any in vivo recording system. We utilized transfer entropy (a well-established method for detecting linear and nonlinear interactions in time series) and the partial information decomposition (a powerful, recently developed tool for dissecting multivariate information processing into distinct parts) to quantify computation between neurons where information flows converged. We found that computations did not occur equally in all neurons throughout the networks. Surprisingly, neurons that computed large amounts of information tended to receive connections from high out-degree neurons. However, the in-degree of a neuron was not related to the amount of information it computed. To gain insight into these findings, we developed a simple feedforward network model. We found that a degree-modified Hebbian wiring rule best reproduced the pattern of computation and degree correlation results seen in the real data. Interestingly, this rule also maximized signal propagation in the presence of network-wide correlations, suggesting a mechanism by which cortex could deal with common random background input. These are the first results to show that the extent to which a neuron modifies incoming information streams depends on its topological location in the surrounding functional network. We recorded the electrical activity of hundreds of neurons simultaneously in brain tissue from mice and we analyzed these signals using state-of-the-art tools from information theory. These tools allowed us to ascertain which neurons were transmitting information to other neurons and to characterize the computations performed by neurons using the inputs they received from two or more other neurons. We found that computations did not occur equally in all neurons throughout the networks. Surprisingly, neurons that computed large amounts of information tended to be recipients of information from neurons with a large number of outgoing connections. Interestingly, the number of incoming connections to a neuron was not related to the amount of information that neuron computed. To better understand these results, we built a network model to match the data. Unexpectedly, the model also maximized information transfer in the presence of network-wide correlations. This suggested a way that networks of cortical neurons could deal with common random background input. These results are the first to show that the amount of information computed by a neuron depends on where it is located in the surrounding network.