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      Spatially Pooled Contrast Responses Predict Neural and Perceptual Similarity of Naturalistic Image Categories

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          Abstract

          The visual world is complex and continuously changing. Yet, our brain transforms patterns of light falling on our retina into a coherent percept within a few hundred milliseconds. Possibly, low-level neural responses already carry substantial information to facilitate rapid characterization of the visual input. Here, we computationally estimated low-level contrast responses to computer-generated naturalistic images, and tested whether spatial pooling of these responses could predict image similarity at the neural and behavioral level. Using EEG, we show that statistics derived from pooled responses explain a large amount of variance between single-image evoked potentials (ERPs) in individual subjects. Dissimilarity analysis on multi-electrode ERPs demonstrated that large differences between images in pooled response statistics are predictive of more dissimilar patterns of evoked activity, whereas images with little difference in statistics give rise to highly similar evoked activity patterns. In a separate behavioral experiment, images with large differences in statistics were judged as different categories, whereas images with little differences were confused. These findings suggest that statistics derived from low-level contrast responses can be extracted in early visual processing and can be relevant for rapid judgment of visual similarity. We compared our results with two other, well- known contrast statistics: Fourier power spectra and higher-order properties of contrast distributions (skewness and kurtosis). Interestingly, whereas these statistics allow for accurate image categorization, they do not predict ERP response patterns or behavioral categorization confusions. These converging computational, neural and behavioral results suggest that statistics of pooled contrast responses contain information that corresponds with perceived visual similarity in a rapid, low-level categorization task.

          Author Summary

          Humans excel in rapid and accurate processing of visual scenes. However, it is unclear which computations allow the visual system to convert light hitting the retina into a coherent representation of visual input in a rapid and efficient way. Here we used simple, computer-generated image categories with similar low-level structure as natural scenes to test whether a model of early integration of low-level information can predict perceived category similarity. Specifically, we show that summarized ( spatially pooled) responses of model neurons covering the entire visual field ( the population response) to low-level properties of visual input ( contrasts) can already be informative about differences in early visual evoked activity as well as behavioral confusions of these categories. These results suggest that low-level population responses can carry relevant information to estimate similarity of controlled images, and put forward the exciting hypothesis that the visual system may exploit these responses to rapidly process real natural scenes. We propose that the spatial pooling that allows for the extraction of this information may be a plausible first step in extracting scene gist to form a rapid impression of the visual input.

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          Most cited references51

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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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            Matching categorical object representations in inferior temporal cortex of man and monkey.

            Inferior temporal (IT) object representations have been intensively studied in monkeys and humans, but representations of the same particular objects have never been compared between the species. Moreover, IT's role in categorization is not well understood. Here, we presented monkeys and humans with the same images of real-world objects and measured the IT response pattern elicited by each image. In order to relate the representations between the species and to computational models, we compare response-pattern dissimilarity matrices. IT response patterns form category clusters, which match between man and monkey. The clusters correspond to animate and inanimate objects; within the animate objects, faces and bodies form subclusters. Within each category, IT distinguishes individual exemplars, and the within-category exemplar similarities also match between the species. Our findings suggest that primate IT across species may host a common code, which combines a categorical and a continuous representation of objects.
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              Sparse coding and decorrelation in primary visual cortex during natural vision.

              Theoretical studies suggest that primary visual cortex (area V1) uses a sparse code to efficiently represent natural scenes. This issue was investigated by recording from V1 neurons in awake behaving macaques during both free viewing of natural scenes and conditions simulating natural vision. Stimulation of the nonclassical receptive field increases the selectivity and sparseness of individual V1 neurons, increases the sparseness of the population response distribution, and strongly decorrelates the responses of neuron pairs. These effects are due to both excitatory and suppressive modulation of the classical receptive field by the nonclassical receptive field and do not depend critically on the spatiotemporal structure of the stimuli. During natural vision, the classical and nonclassical receptive fields function together to form a sparse representation of the visual world. This sparse code may be computationally efficient for both early vision and higher visual processing.
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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
                October 2012
                October 2012
                18 October 2012
                : 8
                : 10
                : e1002726
                Affiliations
                [1 ]Cognitive Neuroscience Group, Department of Psychology, University of Amsterdam, Amsterdam, The Netherlands
                [2 ]Intelligent Systems Lab Amsterdam, Institute of Informatics, University of Amsterdam, Amsterdam, The Netherlands
                Indiana University, United States of America
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: SG VAFL HSS. Performed the experiments: IIAG. Analyzed the data: IIAG. Contributed reagents/materials/analysis tools: SG HSS. Wrote the paper: IIAG SG VAFL HSS.

                Article
                PCOMPBIOL-D-12-00339
                10.1371/journal.pcbi.1002726
                3475684
                23093921
                61a750fe-a4fd-4707-a5c8-c5be12744c7b
                Copyright @ 2012

                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
                : 29 February 2012
                : 2 August 2012
                Page count
                Pages: 16
                Funding
                This work is part of the Research Priority Program ‘Brain & Cognition’ at the University of Amsterdam and was supported by an Advanced Investigator grant from the European Research Council ( http://erc.europa.eu/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Computational Biology
                Computational Neuroscience
                Sensory Systems
                Neuroscience
                Cognitive Neuroscience
                Cognition
                Computational Neuroscience
                Coding Mechanisms
                Sensory Systems
                Sensory Perception
                Psychophysics
                Sensory Systems
                Visual System
                Behavioral Neuroscience
                Neuroimaging

                Quantitative & Systems biology
                Quantitative & Systems biology

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