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      Criticality meets learning: Criticality signatures in a self-organizing recurrent neural network

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      PLoS ONE
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          Abstract

          Many experiments have suggested that the brain operates close to a critical state, based on signatures of criticality such as power-law distributed neuronal avalanches. In neural network models, criticality is a dynamical state that maximizes information processing capacities, e.g. sensitivity to input, dynamical range and storage capacity, which makes it a favorable candidate state for brain function. Although models that self-organize towards a critical state have been proposed, the relation between criticality signatures and learning is still unclear. Here, we investigate signatures of criticality in a self-organizing recurrent neural network (SORN). Investigating criticality in the SORN is of particular interest because it has not been developed to show criticality. Instead, the SORN has been shown to exhibit spatio-temporal pattern learning through a combination of neural plasticity mechanisms and it reproduces a number of biological findings on neural variability and the statistics and fluctuations of synaptic efficacies. We show that, after a transient, the SORN spontaneously self-organizes into a dynamical state that shows criticality signatures comparable to those found in experiments. The plasticity mechanisms are necessary to attain that dynamical state, but not to maintain it. Furthermore, onset of external input transiently changes the slope of the avalanche distributions – matching recent experimental findings. Interestingly, the membrane noise level necessary for the occurrence of the criticality signatures reduces the model’s performance in simple learning tasks. Overall, our work shows that the biologically inspired plasticity and homeostasis mechanisms responsible for the SORN’s spatio-temporal learning abilities can give rise to criticality signatures in its activity when driven by random input, but these break down under the structured input of short repeating sequences.

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          Most cited references44

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          Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type.

          Q Bi, G Bi, M Poo (1998)
          In cultures of dissociated rat hippocampal neurons, persistent potentiation and depression of glutamatergic synapses were induced by correlated spiking of presynaptic and postsynaptic neurons. The relative timing between the presynaptic and postsynaptic spiking determined the direction and the extent of synaptic changes. Repetitive postsynaptic spiking within a time window of 20 msec after presynaptic activation resulted in long-term potentiation (LTP), whereas postsynaptic spiking within a window of 20 msec before the repetitive presynaptic activation led to long-term depression (LTD). Significant LTP occurred only at synapses with relatively low initial strength, whereas the extent of LTD did not show obvious dependence on the initial synaptic strength. Both LTP and LTD depended on the activation of NMDA receptors and were absent in cases in which the postsynaptic neurons were GABAergic in nature. Blockade of L-type calcium channels with nimodipine abolished the induction of LTD and reduced the extent of LTP. These results underscore the importance of precise spike timing, synaptic strength, and postsynaptic cell type in the activity-induced modification of central synapses and suggest that Hebb's rule may need to incorporate a quantitative consideration of spike timing that reflects the narrow and asymmetric window for the induction of synaptic modification.
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            Real-time computation at the edge of chaos in recurrent neural networks.

            Depending on the connectivity, recurrent networks of simple computational units can show very different types of dynamics, ranging from totally ordered to chaotic. We analyze how the type of dynamics (ordered or chaotic) exhibited by randomly connected networks of threshold gates driven by a time-varying input signal depends on the parameters describing the distribution of the connectivity matrix. In particular, we calculate the critical boundary in parameter space where the transition from ordered to chaotic dynamics takes place. Employing a recently developed framework for analyzing real-time computations, we show that only near the critical boundary can such networks perform complex computations on time series. Hence, this result strongly supports conjectures that dynamical systems that are capable of doing complex computational tasks should operate near the edge of chaos, that is, the transition from ordered to chaotic dynamics.
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              Spontaneous cortical activity in awake monkeys composed of neuronal avalanches.

              Spontaneous neuronal activity is an important property of the cerebral cortex but its spatiotemporal organization and dynamical framework remain poorly understood. Studies in reduced systems--tissue cultures, acute slices, and anesthetized rats--show that spontaneous activity forms characteristic clusters in space and time, called neuronal avalanches. Modeling studies suggest that networks with this property are poised at a critical state that optimizes input processing, information storage, and transfer, but the relevance of avalanches for fully functional cerebral systems has been controversial. Here we show that ongoing cortical synchronization in awake rhesus monkeys carries the signature of neuronal avalanches. Negative LFP deflections (nLFPs) correlate with neuronal spiking and increase in amplitude with increases in local population spike rate and synchrony. These nLFPs form neuronal avalanches that are scale-invariant in space and time and with respect to the threshold of nLFP detection. This dimension, threshold invariance, describes a fractal organization: smaller nLFPs are embedded in clusters of larger ones without destroying the spatial and temporal scale-invariance of the dynamics. These findings suggest an organization of ongoing cortical synchronization that is scale-invariant in its three fundamental dimensions--time, space, and local neuronal group size. Such scale-invariance has ontogenetic and phylogenetic implications because it allows large increases in network capacity without a fundamental reorganization of the system.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                2017
                26 May 2017
                : 12
                : 5
                : e0178683
                Affiliations
                [1 ]Frankfurt Institute for Advanced Studies, Johann Wolfgang Goethe University, Frankfurt am Main, Germany
                [2 ]International Max Planck Research School for Neural Circuits, Max Planck Institute for Brain Research, Frankfurt am Main, Germany
                [3 ]Department of Non-linear Dynamics, Max Planck Institute for Dynamics and Self-Organization, Göttingen, Germany
                [4 ]Bernstein Center for Computational Neuroscience, Göttingen, Germany
                Consejo Nacional de Investigaciones Cientificas y Tecnicas, ARGENTINA
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                • Conceptualization: BDP VP JT.

                • Data curation: BDP.

                • Formal analysis: BDP.

                • Funding acquisition: VP JT.

                • Methodology: BDP VP JT.

                • Project administration: JT.

                • Resources: BDP VP JT.

                • Software: BDP.

                • Supervision: VP JT.

                • Validation: BDP.

                • Visualization: BDP.

                • Writing – original draft: BDP VP JT.

                • Writing – review & editing: BDP VP JT.

                Author information
                http://orcid.org/0000-0001-8166-2441
                Article
                PONE-D-16-41854
                10.1371/journal.pone.0178683
                5446191
                28552964
                8d90173a-6829-4051-97d9-e7775acf784a
                © 2017 Del Papa et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 24 October 2016
                : 17 May 2017
                Page count
                Figures: 7, Tables: 0, Pages: 21
                Funding
                This work was supported by the Quandt foundation. Viola Priesemann received financial support from the German Ministry for Education and Research (BMBF) via the Bernstein Center for Computational Neuroscience (BCCN) Göttingen under Grant No. 01GQ1005B. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Animal Cells
                Neurons
                Biology and Life Sciences
                Neuroscience
                Cellular Neuroscience
                Neurons
                Biology and Life Sciences
                Neuroscience
                Cellular Neuroscience
                Neuronal Plasticity
                Computer and Information Sciences
                Neural Networks
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                Neural Networks
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                Cognitive Science
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                Learning and Memory
                Learning
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                Synaptic Plasticity
                Biology and Life Sciences
                Neuroscience
                Developmental Neuroscience
                Synaptic Plasticity
                Physical Sciences
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                Statistics (Mathematics)
                Statistical Noise
                Gaussian Noise
                Biology and Life Sciences
                Anatomy
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                Medicine and Health Sciences
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                Custom metadata
                The corresponding code is available at: https://github.com/delpapa/SORN.

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