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      Six Principles of Visual Cortical Dynamics

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          Abstract

          A fundamental goal in vision science is to determine how many neurons in how many areas are required to compute a coherent interpretation of the visual scene. Here I propose six principles of cortical dynamics of visual processing in the first 150 ms following the appearance of a visual stimulus. Fast synaptic communication between neurons depends on the driving neurons and the biophysical history and driving forces of the target neurons. Under these constraints, the retina communicates changes in the field of view driving large populations of neurons in visual areas into a dynamic sequence of feed-forward communication and integration of the inward current of the change signal into the dendrites of higher order area neurons (30–70 ms). Simultaneously an even larger number of neurons within each area receiving feed-forward input are pre-excited to sub-threshold levels. The higher order area neurons communicate the results of their computations as feedback adding inward current to the excited and pre-excited neurons in lower areas. This feedback reconciles computational differences between higher and lower areas (75–120 ms). This brings the lower area neurons into a new dynamic regime characterized by reduced driving forces and sparse firing reflecting the visual areas interpretation of the current scene (140 ms). The population membrane potentials and net-inward/outward currents and firing are well behaved at the mesoscopic scale, such that the decoding in retinotopic cortical space shows the visual areas’ interpretation of the current scene. These dynamics have plausible biophysical explanations. The principles are theoretical, predictive, supported by recent experiments and easily lend themselves to experimental tests or computational modeling.

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          Speed of processing in the human visual system.

          How long does it take for the human visual system to process a complex natural image? Subjectively, recognition of familiar objects and scenes appears to be virtually instantaneous, but measuring this processing time experimentally has proved difficult. Behavioural measures such as reaction times can be used, but these include not only visual processing but also the time required for response execution. However, event-related potentials (ERPs) can sometimes reveal signs of neural processing well before the motor output. Here we use a go/no-go categorization task in which subjects have to decide whether a previously unseen photograph, flashed on for just 20 ms, contains an animal. ERP analysis revealed a frontal negativity specific to no-go trials that develops roughly 150 ms after stimulus onset. We conclude that the visual processing needed to perform this highly demanding task can be achieved in under 150 ms.
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            Neural correlations, population coding and computation.

            How the brain encodes information in population activity, and how it combines and manipulates that activity as it carries out computations, are questions that lie at the heart of systems neuroscience. During the past decade, with the advent of multi-electrode recording and improved theoretical models, these questions have begun to yield answers. However, a complete understanding of neuronal variability, and, in particular, how it affects population codes, is missing. This is because variability in the brain is typically correlated, and although the exact effects of these correlations are not known, it is known that they can be large. Here, we review studies that address the interaction between neuronal noise and population codes, and discuss their implications for population coding in general.
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              Spatiotemporal dynamics of cortical sensorimotor integration in behaving mice.

              Tactile information is actively acquired and processed in the brain through concerted interactions between movement and sensation. Somatosensory input is often the result of self-generated movement during the active touch of objects, and conversely, sensory information is used to refine motor control. There must therefore be important interactions between sensory and motor pathways, which we chose to investigate in the mouse whisker sensorimotor system. Voltage-sensitive dye was applied to the neocortex of mice to directly image the membrane potential dynamics of sensorimotor cortex with subcolumnar spatial resolution and millisecond temporal precision. Single brief whisker deflections evoked highly distributed depolarizing cortical sensory responses, which began in the primary somatosensory barrel cortex and subsequently excited the whisker motor cortex. The spread of sensory information to motor cortex was dynamically regulated by behavior and correlated with the generation of sensory-evoked whisker movement. Sensory processing in motor cortex may therefore contribute significantly to active tactile sensory perception.
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                Author and article information

                Journal
                Front Syst Neurosci
                Front. Syst. Neurosci.
                Frontiers in Systems Neuroscience
                Frontiers Research Foundation
                1662-5137
                14 April 2010
                02 July 2010
                2010
                : 4
                : 28
                Affiliations
                [1] 1simpleDepartment of Neuroscience, Division of Brain Research, Karolinska Institutet, Stockholm Sweden
                Author notes

                Edited by: Robert Shapley, New York University, USA

                Reviewed by: Gustavo Deco, Universitat Pompeu Fabra, Spain; Keith P. Purpura, Weill Cornell Medical College, USA

                *Correspondence: Per E. Roland, Department of Neuroscience, Division of Brain Research, Karolinska Institutet, Retzius väg 8 S171 77 Solna, Stockholm, Sweden. e-mail: per.roland@ 123456ki.se
                Article
                10.3389/fnsys.2010.00028
                2906257
                20661451
                3260d805-66d4-4c14-a810-d22891ac9d27
                Copyright © 2010 Roland.

                This is an open-access article subject to an exclusive license agreement between the authors and the Frontiers Research Foundation, which permits unrestricted use, distribution, and reproduction in any medium, provided the original authors and source are credited.

                History
                : 23 February 2010
                : 11 June 2010
                Page count
                Figures: 12, Tables: 0, Equations: 2, References: 143, Pages: 21, Words: 19822
                Categories
                Neuroscience
                Hypothesis and Theory

                Neurosciences
                feedback,voltage-sensitive dyes,inter-area communication,cortical theory,object vision,membrane potential,laminar firing,object motion

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