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      Second Order Dimensionality Reduction Using Minimum and Maximum Mutual Information Models

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          Abstract

          Conventional methods used to characterize multidimensional neural feature selectivity, such as spike-triggered covariance (STC) or maximally informative dimensions (MID), are limited to Gaussian stimuli or are only able to identify a small number of features due to the curse of dimensionality. To overcome these issues, we propose two new dimensionality reduction methods that use minimum and maximum information models. These methods are information theoretic extensions of STC that can be used with non-Gaussian stimulus distributions to find relevant linear subspaces of arbitrary dimensionality. We compare these new methods to the conventional methods in two ways: with biologically-inspired simulated neurons responding to natural images and with recordings from macaque retinal and thalamic cells responding to naturalistic time-varying stimuli. With non-Gaussian stimuli, the minimum and maximum information methods significantly outperform STC in all cases, whereas MID performs best in the regime of low dimensional feature spaces.

          Author Summary

          Neurons are capable of simultaneously encoding information about multiple features of sensory stimuli in their spikes. The dimensionality reduction methods that currently exist to extract those relevant features are either biased for non-Gaussian stimuli or fall victim to the curse of dimensionality. In this paper we introduce two information theoretic extensions of the spike-triggered covariance method. These new methods use the concepts of minimum and maximum mutual information to identify the stimulus features encoded in the spikes of a neuron. Using simulated and experimental neural data, these methods are shown to perform well both in situations where conventional approaches are appropriate and where they fail. These new techniques should improve the characterization of neural feature selectivity in areas of the brain where the application of currently available approaches is restricted.

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          Most cited references50

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          Normalization of cell responses in cat striate cortex.

          D. Heeger (1992)
          Simple cells in the striate cortex have been depicted as half-wave-rectified linear operators. Complex cells have been depicted as energy mechanisms, constructed from the squared sum of the outputs of quadrature pairs of linear operators. However, the linear/energy model falls short of a complete explanation of striate cell responses. In this paper, a modified version of the linear/energy model is presented in which striate cells mutually inhibit one another, effectively normalizing their responses with respect to stimulus contrast. This paper reviews experimental measurements of striate cell responses, and shows that the new model explains a significantly larger body of physiological data.
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            Linearity and normalization in simple cells of the macaque primary visual cortex.

            Simple cells in the primary visual cortex often appear to compute a weighted sum of the light intensity distribution of the visual stimuli that fall on their receptive fields. A linear model of these cells has the advantage of simplicity and captures a number of basic aspects of cell function. It, however, fails to account for important response nonlinearities, such as the decrease in response gain and latency observed at high contrasts and the effects of masking by stimuli that fail to elicit responses when presented alone. To account for these nonlinearities we have proposed a normalization model, which extends the linear model to include mutual shunting inhibition among a large number of cortical cells. Shunting inhibition is divisive, and its effect in the model is to normalize the linear responses by a measure of stimulus energy. To test this model we performed extracellular recordings of simple cells in the primary visual cortex of anesthetized macaques. We presented large stimulus sets consisting of (1) drifting gratings of various orientations and spatiotemporal frequencies; (2) plaids composed of two drifting gratings; and (3) gratings masked by full-screen spatiotemporal white noise. We derived expressions for the model predictions and fitted them to the physiological data. Our results support the normalization model, which accounts for both the linear and the nonlinear properties of the cells. An alternative model, in which the linear responses are subject to a compressive nonlinearity, did not perform nearly as well.
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              Nature and interaction of signals from the receptive field center and surround in macaque V1 neurons.

              Information is integrated across the visual field to transform local features into a global percept. We now know that V1 neurons provide more spatial integration than originally thought due to the existence of their nonclassical inhibitory surrounds. To understand spatial integration in the visual cortex, we have studied the nature and extent of center and surround influences on neuronal response. We used drifting sinusoidal gratings in circular and annular apertures to estimate the sizes of the receptive field's excitatory center and suppressive surround. We used combinations of stimuli inside and outside the receptive field to explore the nature of the surround influence on the receptive field center as a function of the relative and absolute contrast of stimuli in the two regions. We conclude that the interaction is best explained as a divisive modulation of response gain by signals from the surround. We then develop a receptive field model based on the ratio of signals from Gaussian-shaped center and surround mechanisms. We show that this model can account well for the variations in receptive field size with contrast that we and others have observed and for variations in size with the state of contrast adaptation. The model achieves this success by simple variations in the relative gain of the two component mechanisms of the receptive field. This model thus offers a parsimonious explanation of a variety of phenomena involving changes in apparent receptive field size and accounts for these phenomena purely in terms of two receptive field mechanisms that do not themselves change in size. We used the extent of the center mechanism in our model as an indicator of the spatial extent of the central excitatory portion of the receptive field. We compared the extent of the center to measurements of horizontal connections within V1 and determined that horizontal intracortical connections are well matched in extent to the receptive field center mechanism. Input to the suppressive surround may come in part from feedback signals from higher areas.
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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
                : e1002249
                Affiliations
                [1 ]Computational Neurobiology Laboratory, The Salk Institute for Biological Studies, La Jolla, California, United States of America
                [2 ]Center for Theoretical Biological Physics and Department of Physics, University of California, San Diego, California, United States of America
                [3 ]Department of Vision Sciences, University of Alabama at Birmingham, Birmingham, Alabama, United States of America
                Indiana University, United States of America
                Author notes

                Conceived and designed the experiments: JDF RJR LCS TOS. Performed the experiments: LCS. Analyzed the data: JDF RJR LCS TOS. Wrote the paper: JDF RJR LCS TOS.

                Article
                PCOMPBIOL-D-11-01062
                10.1371/journal.pcbi.1002249
                3203063
                22046122
                c853df41-68b5-4e55-a65a-2ea777686873
                Fitzgerald 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
                : 21 July 2011
                : 7 September 2011
                Page count
                Pages: 9
                Categories
                Research Article
                Biology
                Neuroscience
                Computational Neuroscience
                Coding Mechanisms
                Sensory Systems
                Sensory Systems
                Visual System
                Computer Science
                Algorithms

                Quantitative & Systems biology
                Quantitative & Systems biology

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