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      Representation of Perceptual Color Space in Macaque Posterior Inferior Temporal Cortex (the V4 Complex)

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          Abstract

          The lateral geniculate nucleus is thought to represent color using two populations of cone-opponent neurons [L vs M; S vs (L + M)], which establish the cardinal directions in color space (reddish vs cyan; lavender vs lime). How is this representation transformed to bring about color perception? Prior work implicates populations of glob cells in posterior inferior temporal cortex (PIT; the V4 complex), but the correspondence between the neural representation of color in PIT/V4 complex and the organization of perceptual color space is unclear. We compared color-tuning data for populations of glob cells and interglob cells to predictions obtained using models that varied in the color-tuning narrowness of the cells, and the color preference distribution across the populations. Glob cells were best accounted for by simulated neurons that have nonlinear (narrow) tuning and, as a population, represent a color space designed to be perceptually uniform (CIELUV). Multidimensional scaling and representational similarity analyses showed that the color space representations in both glob and interglob populations were correlated with the organization of CIELUV space, but glob cells showed a stronger correlation. Hue could be classified invariant to luminance with high accuracy given glob responses and above-chance accuracy given interglob responses. Luminance could be read out invariant to changes in hue in both populations, but interglob cells tended to prefer stimuli having luminance contrast, regardless of hue, whereas glob cells typically retained hue tuning as luminance contrast was modulated. The combined luminance/hue sensitivity of glob cells is predicted for neurons that can distinguish two colors of the same hue at different luminance levels (orange/brown).

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          The analysis of visual motion: a comparison of neuronal and psychophysical performance.

          We compared the ability of psychophysical observers and single cortical neurons to discriminate weak motion signals in a stochastic visual display. All data were obtained from rhesus monkeys trained to perform a direction discrimination task near psychophysical threshold. The conditions for such a comparison were ideal in that both psychophysical and physiological data were obtained in the same animals, on the same sets of trials, and using the same visual display. In addition, the psychophysical task was tailored in each experiment to the physiological properties of the neuron under study; the visual display was matched to each neuron's preference for size, speed, and direction of motion. Under these conditions, the sensitivity of most MT neurons was very similar to the psychophysical sensitivity of the animal observers. In fact, the responses of single neurons typically provided a satisfactory account of both absolute psychophysical threshold and the shape of the psychometric function relating performance to the strength of the motion signal. Thus, psychophysical decisions in our task are likely to be based upon a relatively small number of neural signals. These signals could be carried by a small number of neurons if the responses of the pooled neurons are statistically independent. Alternatively, the signals may be carried by a much larger pool of neurons if their responses are partially intercorrelated.
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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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              Fast readout of object identity from macaque inferior temporal cortex.

              Understanding the brain computations leading to object recognition requires quantitative characterization of the information represented in inferior temporal (IT) cortex. We used a biologically plausible, classifier-based readout technique to investigate the neural coding of selectivity and invariance at the IT population level. The activity of small neuronal populations (approximately 100 randomly selected cells) over very short time intervals (as small as 12.5 milliseconds) contained unexpectedly accurate and robust information about both object "identity" and "category." This information generalized over a range of object positions and scales, even for novel objects. Coarse information about position and scale could also be read out from the same population.
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                Author and article information

                Journal
                eNeuro
                eNeuro
                eneuro
                eneuro
                eNeuro
                eNeuro
                Society for Neuroscience
                2373-2822
                12 August 2016
                29 August 2016
                Jul-Aug 2016
                : 3
                : 4
                : ENEURO.0039-16.2016
                Affiliations
                [1 ]Program in Neuroscience, Wellesley College , Wellesley, Massachusetts 02481
                [2 ]Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology , Cambridge, Massachusetts 02139
                [3 ]Department of Psychology, Justus Liebig University Giessen , 35396 Giessen, Germany
                Author notes

                The authors declare no competing financial interests.

                Author contributions: B.R.C. designed research; B.R.C. performed research; T.H. contributed unpublished reagents/analytic tools; K.S.B., K.L.H., and B.R.C. analyzed data; B.R.C. wrote the paper.

                This research was supported by National Institutes of Health Grant EY023322 and National Science Foundation Grant 1353571.

                [*]

                K.S.B. and K.L.H. contributed equally as co-first authors.

                [†]

                Current address: Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, Bethesda MD.

                Correspondence should be addressed to Bevil R. Conway, Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, Bethesda, Maryland 20892. E-mail: bevil@ 123456mit.edu .
                Article
                eN-NWR-0039-16
                10.1523/ENEURO.0039-16.2016
                5002982
                27595132
                cd600b5d-0ba9-4357-a8a8-29a40acda8e3
                Copyright © 2016 Bohon et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

                History
                : 24 February 2016
                : 19 July 2016
                : 4 August 2016
                Page count
                Figures: 12, Tables: 1, Equations: 21, References: 103, Pages: 27, Words: 21162
                Funding
                Funded by: NIH
                Award ID: EY023322
                Funded by: NSF
                Award ID: 1353571
                Categories
                8
                New Research
                Sensory and Motor Systems
                Custom metadata
                July/August 2016

                color,macaque,monkey,neurophysiology,v4,vision
                color, macaque, monkey, neurophysiology, v4, vision

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