1. Neuronal avalanches are increasingly recognized to be important for cortex function. Given the 200+ related articles that have been published since our first report on neuronal avalanches, the field has been readied itself for its first major conference. My Section took the lead in organizing the first conference on Criticality in Neural Systems in collaboration with Ernst Niebur, Johns Hopkins University. The 2-day conference took place on the NIH campus in Bethesda at the Natcher Conference center with about 100 attendees and featured 19 international and national speakers and posters. Most speakers have already contributed their book chapters, which will appear in a book Criticality in Neural Systems, 2013, Wiley. 2. DARPA initiated a project on Physical Intelligence to design a physical device that can replace the current von-Neumann based computer chips. Participating groups working in the physical and computer sciences converged on neuronal avalanche dynamics and my Section joined for a 2-year collaboration. 3. We identified for the first time rules that describe weighted, functional networks of neuronal avalanches in monkey cortex and in vitro and found these also to describe complex biological and human communication systems (Pajevic and Plenz, 2012). Abstract: Many complex systems reveal a small-world topology, which allows simultaneously local and global efficiency in the interaction between system constituents. Here, we report the results of a comprehensive study that investigates the relation between the clustering properties in such small-world systems and the strength of interactions between its constituents, quantified by the link weight. For brain, gene, social and language networks, we find a local integrative weight organization in which strong links preferentially occur between nodes with overlapping neighbourhoods;we relate this to global robustness of the clustering to removal of the weakest links. Furthermore, we identify local learning rules that establish integrative networks and improve network traffic in response to past traffic failures. Our findings identify a general organization for complex systems that strikes a balance between efficient local and global communication in their strong interactions, while allowing for robust, exploratory development of weak interactions. 4. Many high-level cognitive functions in cortex are thought to underlie transient, yet highly organized synchronization between neuronal groups. We demonstrated experimentally for the first time that cortical networks with neuronal avalanche dynamics maximize their ability to transiently synchronize diverse groups (Yang et al., 2012). Abstract: Ongoing interactions among cortical neurons often manifest as network-level synchrony. Understanding the spatiotemporal dynamics of such spontaneous synchrony is important because it may (1) influence network response to input, (2) shape activity-dependent microcircuit structure, and (3) reveal fundamental network properties, such as an imbalance of excitation (E) and inhibition (I). Here we delineate the spatiotemporal character of spontaneous synchrony in rat cortex slice cultures and a computational model over a range of different EI conditions including disfacilitated (antagonized AMPA, NMDA receptors), unperturbed, and disinhibited (antagonized GABAA receptors). Local field potential was recorded with multielectrode arrays during spontaneous burst activity. Synchrony among neuronal groups was quantified based on phase-locking among recording sites. As network excitability was increased from low to high, we discovered three phenomena at an intermediate excitability level: (1) onset of synchrony, (2) maximized variability of synchrony, and (3) neuronal avalanches. Our computational model predicted that these three features occur when the network operates near a unique balanced EI condition called criticality. These results were invariant to changes in the measurement spatial extent, spatial resolution, and frequency bands. Our findings indicate that moderate average synchrony, which is required to avoid pathology, occurs over a limited range of EI conditions and emerges together with maximally variable synchrony. If variable synchrony is detrimental to cortical function, this is a cost paid for moderate average synchrony. However, if variable synchrony is beneficial, then by operating near criticality the cortex may doubly benefit from moderate mean and maximized variability of synchrony. 5. Two of our most advanced experimental findings on cortical dynamics, neuronal avalanches and coherence potentials, have been reviewed and put into a larger theoretical and conceptual perspective. This review also features numerous previously unpublished analysis from our in vitro and in vivo experiments. The Special Topic of this top physics journal was focused on advanced theoretical and experimental understanding of complex systems (Plenz, 2011). Abstract: The mammalian cortex consists of a vast network of weakly interacting excitable cells called neurons. Neurons must synchronize their activities in order to trigger activity in neighboring neurons. Moreover, interactions must be carefully regulated to remain weak (but not too weak) such that cascades of active neuronal groups avoid explosive growth yet allow for activity propagation over long-distances. Such a balance is robustly realized for neuronal avalanches, which are defined as cortical activity cascades that follow precise power laws. In experiments, scale-invariant neuronal avalanche dynamics have been observed during spontaneous cortical activity in isolated preparations in vitro as well as in the ongoing cortical activity of awake animals and in humans. Theory, models, and experiments suggest that neuronal avalanches are the signature of brain function near criticality at which the cortex optimally responds to inputs and maximizes its information capacity. Importantly, avalanche dynamics allow for the emergence of a subset of avalanches, the coherence potentials. They emerge when the synchronization of a local neuronal group exceeds a local threshold, at which the system spawns replicas of the local group activity at distant network sites. The functional importance of coherence potentials will be discussed in the context of propagating structures, such as gliders in balanced cellular automata. Gliders constitute local population dynamics that replicate in space after a finite number of generations and are thought to provide cellular automata with universal computation. Avalanches and coherence potentials are proposed to constitute a modern framework of cortical synchronization dynamics that underlies brain function. 6. We summarized our experimental findings on functional advantages of neuronal avalanches for the cortex in a review addressed to general neuroscience audiences. Abstract: Rapidly growing empirical evidence supports the hypothesis that the cortex operates near criticality. Although the confirmation of this hypothesis would mark a significant advance in fundamental understanding of cortical physiology, a natural question arises: What functional benefits are endowed to cortical circuits that operate at criticality? In this review, we first describe an introductory-level thought experiment to provide the reader with an intuitive understanding of criticality. Second, we discuss some practical approaches for investigating criticality. Finally, we review quantitative evidence that three functional properties of the cortex are optimized at criticality: 1) dynamic range, 2) information transmission, and 3) information capacity. We focus on recently reported experimental evidence and briefly discuss the theory and history of these ideas. (Shew and Plenz, 2012).

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11
Fiscal Year
2012
Total Cost
$1,224,947
Indirect Cost
Name
U.S. National Institute of Mental Health
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Lombardi, F; Herrmann, H J; Plenz, D et al. (2016) Temporal correlations in neuronal avalanche occurrence. Sci Rep 6:24690
Bai, Ruiliang; Stewart, Craig V; Plenz, Dietmar et al. (2016) Assessing the sensitivity of diffusion MRI to detect neuronal activity directly. Proc Natl Acad Sci U S A 113:E1728-37
Massobrio, Paolo; de Arcangelis, Lucilla; Pasquale, Valentina et al. (2015) Criticality as a signature of healthy neural systems. Front Syst Neurosci 9:22
Bellay, Timothy; Klaus, Andreas; Seshadri, Saurav et al. (2015) Irregular spiking of pyramidal neurons organizes as scale-invariant neuronal avalanches in the awake state. Elife 4:e07224
Stepp, Nigel; Plenz, Dietmar; Srinivasa, Narayan (2015) Synaptic plasticity enables adaptive self-tuning critical networks. PLoS Comput Biol 11:e1004043
Bai, Ruiliang; Klaus, Andreas; Bellay, Tim et al. (2015) Simultaneous calcium fluorescence imaging and MR of ex vivo organotypic cortical cultures: a new test bed for functional MRI. NMR Biomed 28:1726-38
Meisel, Christian; Klaus, Andreas; Kuehn, Christian et al. (2015) Critical slowing down governs the transition to neuron spiking. PLoS Comput Biol 11:e1004097
Meisel, Christian; Schulze-Bonhage, Andreas; Freestone, Dean et al. (2015) Intrinsic excitability measures track antiepileptic drug action and uncover increasing/decreasing excitability over the wake/sleep cycle. Proc Natl Acad Sci U S A 112:14694-9
Alstott, Jeff; Bullmore, Ed; Plenz, Dietmar (2014) Powerlaw: a Python package for analysis of heavy-tailed distributions. PLoS One 9:e85777
Lombardi, Fabrizio; Herrmann, Hans J; Plenz, Dietmar et al. (2014) On the temporal organization of neuronal avalanches. Front Syst Neurosci 8:204

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