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      A Sparse Coding Model with Synaptically Local Plasticity and Spiking Neurons Can Account for the Diverse Shapes of V1 Simple Cell Receptive Fields

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          Abstract

          Sparse coding algorithms trained on natural images can accurately predict the features that excite visual cortical neurons, but it is not known whether such codes can be learned using biologically realistic plasticity rules. We have developed a biophysically motivated spiking network, relying solely on synaptically local information, that can predict the full diversity of V1 simple cell receptive field shapes when trained on natural images. This represents the first demonstration that sparse coding principles, operating within the constraints imposed by cortical architecture, can successfully reproduce these receptive fields. We further prove, mathematically, that sparseness and decorrelation are the key ingredients that allow for synaptically local plasticity rules to optimize a cooperative, linear generative image model formed by the neural representation. Finally, we discuss several interesting emergent properties of our network, with the intent of bridging the gap between theoretical and experimental studies of visual cortex.

          Author Summary

          In a sparse coding model, individual input stimuli are represented by the activities of model neurons, the majority of which are inactive in response to any particular stimulus. For a given class of stimuli, the neurons are optimized so that the stimuli can be faithfully represented with the minimum number of co-active units. This has been proposed as a model for visual cortex. While it has previously been demonstrated that sparse coding model neurons, when trained on natural images, learn to represent the same features as do neurons in primate visual cortex, it remains to be demonstrated that this can be achieved with physiologically realistic plasticity rules. In particular, learning in cortex appears to occur by the modification of synaptic connections between neurons, which must depend only on information available locally, at the synapse, and not, for example, on the properties of large numbers of distant cells. We provide the first demonstration that synaptically local plasticity rules are sufficient to learn a sparse image code, and to account for the observed response properties of visual cortical neurons: visual cortex actually could learn a sparse image code.

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          Most cited references50

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          Neurons with graded response have collective computational properties like those of two-state neurons.

          J Hopfield (1984)
          A model for a large network of "neurons" with a graded response (or sigmoid input-output relation) is studied. This deterministic system has collective properties in very close correspondence with the earlier stochastic model based on McCulloch - Pitts neurons. The content- addressable memory and other emergent collective properties of the original model also are present in the graded response model. The idea that such collective properties are used in biological systems is given added credence by the continued presence of such properties for more nearly biological "neurons." Collective analog electrical circuits of the kind described will certainly function. The collective states of the two models have a simple correspondence. The original model will continue to be useful for simulations, because its connection to graded response systems is established. Equations that include the effect of action potentials in the graded response system are also developed.
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            Some informational aspects of visual perception.

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              Decorrelated neuronal firing in cortical microcircuits.

              Correlated trial-to-trial variability in the activity of cortical neurons is thought to reflect the functional connectivity of the circuit. Many cortical areas are organized into functional columns, in which neurons are believed to be densely connected and to share common input. Numerous studies report a high degree of correlated variability between nearby cells. We developed chronically implanted multitetrode arrays offering unprecedented recording quality to reexamine this question in the primary visual cortex of awake macaques. We found that even nearby neurons with similar orientation tuning show virtually no correlated variability. Our findings suggest a refinement of current models of cortical microcircuit architecture and function: Either adjacent neurons share only a few percent of their inputs or, alternatively, their activity is actively decorrelated.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Comput Biol
                plos
                ploscomp
                PLoS Computational Biology
                Public Library of Science (San Francisco, USA )
                1553-734X
                1553-7358
                October 2011
                October 2011
                27 October 2011
                : 7
                : 10
                : e1002250
                Affiliations
                [1 ]Department of Physics, University of California, Berkeley, California, United States of America
                [2 ]Redwood Center for Theoretical Neuroscience, University of California, Berkeley, California, United States of America
                [3 ]Helen Wills Neuroscience Institute, University of California, Berkeley, California, United States of America
                Indiana University, United States of America
                Author notes

                Conceived and designed the experiments: JZ. Performed the experiments: JZ. Analyzed the data: JZ. Contributed reagents/materials/analysis tools: JTM. Wrote the paper: JZ MRD.

                Article
                PCOMPBIOL-D-11-01106
                10.1371/journal.pcbi.1002250
                3203062
                22046123
                c75e39e7-635d-4225-b2d3-63cd8b91aa44
                Zylberberg 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
                : 26 July 2011
                : 8 September 2011
                Page count
                Pages: 12
                Categories
                Research Article
                Biology
                Neuroscience
                Computational Neuroscience
                Coding Mechanisms
                Sensory Systems
                Sensory Systems
                Visual System
                Systems Biology
                Theoretical Biology
                Physics
                Biophysics
                Biophysics Theory

                Quantitative & Systems biology
                Quantitative & Systems biology

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