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      Cortical reliability amid noise and chaos

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          Abstract

          Typical responses of cortical neurons to identical sensory stimuli appear highly variable. It has thus been proposed that the cortex primarily uses a rate code. However, other studies have argued for spike-time coding under certain conditions. The potential role of spike-time coding is directly limited by the internally generated variability of cortical circuits, which remains largely unexplored. Here, we quantify this internally generated variability using a biophysical model of rat neocortical microcircuitry with biologically realistic noise sources. We find that stochastic neurotransmitter release is a critical component of internally generated variability, causing rapidly diverging, chaotic recurrent network dynamics. Surprisingly, the same nonlinear recurrent network dynamics can transiently overcome the chaos in response to weak feed-forward thalamocortical inputs, and support reliable spike times with millisecond precision. Our model shows that the noisy and chaotic network dynamics of recurrent cortical microcircuitry are compatible with stimulus-evoked, millisecond spike-time reliability, resolving a long-standing debate.

          Abstract

          Whether cortical neurons can fire reliable spikes amid cellular noise and chaotic network dynamics remains debated. Here the authors simulate a detailed neocortical microcircuit model and show that noisy and chaotic cortical network dynamics are compatible with stimulus-evoked, millisecond spike-time reliability.

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          Most cited references57

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          Noise in the nervous system.

          Noise--random disturbances of signals--poses a fundamental problem for information processing and affects all aspects of nervous-system function. However, the nature, amount and impact of noise in the nervous system have only recently been addressed in a quantitative manner. Experimental and computational methods have shown that multiple noise sources contribute to cellular and behavioural trial-to-trial variability. We review the sources of noise in the nervous system, from the molecular to the behavioural level, and show how noise contributes to trial-to-trial variability. We highlight how noise affects neuronal networks and the principles the nervous system applies to counter detrimental effects of noise, and briefly discuss noise's potential benefits.
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            Reconstruction and Simulation of Neocortical Microcircuitry.

            We present a first-draft digital reconstruction of the microcircuitry of somatosensory cortex of juvenile rat. The reconstruction uses cellular and synaptic organizing principles to algorithmically reconstruct detailed anatomy and physiology from sparse experimental data. An objective anatomical method defines a neocortical volume of 0.29 ± 0.01 mm(3) containing ~31,000 neurons, and patch-clamp studies identify 55 layer-specific morphological and 207 morpho-electrical neuron subtypes. When digitally reconstructed neurons are positioned in the volume and synapse formation is restricted to biological bouton densities and numbers of synapses per connection, their overlapping arbors form ~8 million connections with ~37 million synapses. Simulations reproduce an array of in vitro and in vivo experiments without parameter tuning. Additionally, we find a spectrum of network states with a sharp transition from synchronous to asynchronous activity, modulated by physiological mechanisms. The spectrum of network states, dynamically reconfigured around this transition, supports diverse information processing strategies.
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              Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex.

              Neuroscience produces a vast amount of data from an enormous diversity of neurons. A neuronal classification system is essential to organize such data and the knowledge that is derived from them. Classification depends on the unequivocal identification of the features that distinguish one type of neuron from another. The problems inherent in this are particularly acute when studying cortical interneurons. To tackle this, we convened a representative group of researchers to agree on a set of terms to describe the anatomical, physiological and molecular features of GABAergic interneurons of the cerebral cortex. The resulting terminology might provide a stepping stone towards a future classification of these complex and heterogeneous cells. Consistent adoption will be important for the success of such an initiative, and we also encourage the active involvement of the broader scientific community in the dynamic evolution of this project.
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                Author and article information

                Contributors
                max.nolte@epfl.ch
                eilif.mueller@epfl.ch
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                22 August 2019
                22 August 2019
                2019
                : 10
                : 3792
                Affiliations
                [1 ]ISNI 0000000121839049, GRID grid.5333.6, Blue Brain Project, , École Polytechnique Fédérale de Lausanne, ; 1202 Geneva, Switzerland
                [2 ]ISNI 0000000121839049, GRID grid.5333.6, Laboratory of Neural Microcircuitry, Brain Mind Institute, , École Polytechnique Fédérale de Lausanne, ; 1015 Lausanne, Switzerland
                Author information
                http://orcid.org/0000-0002-9452-4926
                http://orcid.org/0000-0003-3455-2367
                Article
                11633
                10.1038/s41467-019-11633-8
                6706377
                31439838
                193cc849-2a76-465a-a211-54990814eeba
                © The Author(s) 2019

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 22 December 2018
                : 23 July 2019
                Funding
                Funded by: This work was supported by funding from the ETH Domain for the Blue Brain Project. The Blue Brain Project’s IBM BlueGene/Q system, BlueBrain IV, and HPE SGI 8600 system, BlueBrain V, were funded by the ETH Board and hosted at the Swiss National Supercomputing Center (CSCS).
                Categories
                Article
                Custom metadata
                © The Author(s) 2019

                Uncategorized
                biophysical models,network models,cortex,neural circuits
                Uncategorized
                biophysical models, network models, cortex, neural circuits

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