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      Slow Feature Analysis on Retinal Waves Leads to V1 Complex Cells

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          Abstract

          The developing visual system of many mammalian species is partially structured and organized even before the onset of vision. Spontaneous neural activity, which spreads in waves across the retina, has been suggested to play a major role in these prenatal structuring processes. Recently, it has been shown that when employing an efficient coding strategy, such as sparse coding, these retinal activity patterns lead to basis functions that resemble optimal stimuli of simple cells in primary visual cortex (V1). Here we present the results of applying a coding strategy that optimizes for temporal slowness, namely Slow Feature Analysis (SFA), to a biologically plausible model of retinal waves. Previously, SFA has been successfully applied to model parts of the visual system, most notably in reproducing a rich set of complex-cell features by training SFA with quasi-natural image sequences. In the present work, we obtain SFA units that share a number of properties with cortical complex-cells by training on simulated retinal waves. The emergence of two distinct properties of the SFA units (phase invariance and orientation tuning) is thoroughly investigated via control experiments and mathematical analysis of the input-output functions found by SFA. The results support the idea that retinal waves share relevant temporal and spatial properties with natural visual input. Hence, retinal waves seem suitable training stimuli to learn invariances and thereby shape the developing early visual system such that it is best prepared for coding input from the natural world.

          Author Summary

          It is believed that our sensory systems are adapted to statistical properties of behaviorally relevant elements in our natural environments. In the case of vision, one adaptation principle that has been put forward is the so-called slowness principle. However, the visual system is partially structured even before eye opening, when no natural input is available yet. Thus, spontaneous neural activity in the developing visual system of mammals (so-called retinal waves) has been suggested to contribute to shaping connections in early visual areas before the onset of vision. Here we aim to bring these two ideas together. Specifically, we apply an algorithm that implements the slowness principle to simulated retinal waves. The algorithm is set to encode the retinal wave input and thus has to extract relevant features from that input. After encoding, we are able to investigate the emerged representation and we find that the extracted features bear strong similarity to features that are encoded by neurons in the early visual system. These features are the building blocks for an object representation that is independent of the object's position in the visual field.

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          SINGLE-CELL RESPONSES IN STRIATE CORTEX OF KITTENS DEPRIVED OF VISION IN ONE EYE.

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            Do we know what the early visual system does?

            We can claim that we know what the visual system does once we can predict neural responses to arbitrary stimuli, including those seen in nature. In the early visual system, models based on one or more linear receptive fields hold promise to achieve this goal as long as the models include nonlinear mechanisms that control responsiveness, based on stimulus context and history, and take into account the nonlinearity of spike generation. These linear and nonlinear mechanisms might be the only essential determinants of the response, or alternatively, there may be additional fundamental determinants yet to be identified. Research is progressing with the goals of defining a single "standard model" for each stage of the visual pathway and testing the predictive power of these models on the responses to movies of natural scenes. These predictive models represent, at a given stage of the visual pathway, a compact description of visual computation. They would be an invaluable guide for understanding the underlying biophysical and anatomical mechanisms and relating neural responses to visual perception.
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              An evaluation of the two-dimensional Gabor filter model of simple receptive fields in cat striate cortex.

              1. Using the two-dimensional (2D) spatial and spectral response profiles described in the previous two reports, we test Daugman's generalization of Marcelja's hypothesis that simple receptive fields belong to a class of linear spatial filters analogous to those described by Gabor and referred to here as 2D Gabor filters. 2. In the space domain, we found 2D Gabor filters that fit the 2D spatial response profile of each simple cell in the least-squared error sense (with a simplex algorithm), and we show that the residual error is devoid of spatial structure and statistically indistinguishable from random error. 3. Although a rigorous statistical approach was not possible with our spectral data, we also found a Gabor function that fit the 2D spectral response profile of each simple cell and observed that the residual errors are everywhere small and unstructured. 4. As an assay of spatial linearity in two dimensions, on which the applicability of Gabor theory is dependent, we compare the filter parameters estimated from the independent 2D spatial and spectral measurements described above. Estimates of most parameters from the two domains are highly correlated, indicating that assumptions about spatial linearity are valid. 5. Finally, we show that the functional form of the 2D Gabor filter provides a concise mathematical expression, which incorporates the important spatial characteristics of simple receptive fields demonstrated in the previous two reports. Prominent here are 1) Cartesian separable spatial response profiles, 2) spatial receptive fields with staggered subregion placement, 3) Cartesian separable spectral response profiles, 4) spectral response profiles with axes of symmetry not including the origin, and 5) the uniform distribution of spatial phase angles. 6. We conclude that the Gabor function provides a useful and reasonably accurate description of most spatial aspects of simple receptive fields. Thus it seems that an optimal strategy has evolved for sampling images simultaneously in the 2D spatial and spatial frequency domains.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Comput Biol
                PLoS Comput. Biol
                plos
                ploscomp
                PLoS Computational Biology
                Public Library of Science (San Francisco, USA )
                1553-734X
                1553-7358
                May 2014
                8 May 2014
                : 10
                : 5
                : e1003564
                Affiliations
                [1 ]Machine Learning Group, Department of Computer Science, Berlin Institute of Technology, Berlin, Germany
                [2 ]Institute for Theoretical Biology, Humboldt-University, Berlin, Germany
                [3 ]Bernstein Center for Computational Neuroscience, Berlin, Germany
                [4 ]Institute for Neural Computation, Ruhr-University Bochum, Bochum, Germany
                University of Rochester, United States of America
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: SD NW LW. Performed the experiments: SD NW. Analyzed the data: SD. Contributed reagents/materials/analysis tools: SD NW. Wrote the paper: SD NW LW.

                Article
                PCOMPBIOL-D-13-01132
                10.1371/journal.pcbi.1003564
                4014395
                24810948
                dfb3a390-87aa-4b2a-a878-2118b7eed6ae
                Copyright @ 2014

                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
                : 25 June 2013
                : 20 December 2013
                Page count
                Pages: 13
                Funding
                NW has been supported by the German Federal Ministry of Education and Research through a grant to the Bernstein Center of Computational Neuroscience Berlin (BMBF 01GQ0410). 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
                Computational Biology
                Computational Neuroscience
                Coding Mechanisms
                Developmental Biology
                Morphogenesis
                Pattern Formation
                Neuroscience
                Sensory Systems
                Visual System

                Quantitative & Systems biology
                Quantitative & Systems biology

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