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      Contextual modulation of sensitivity to naturalistic image structure in macaque V2

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          Abstract

          The stimulus selectivity of neurons in V1 is well known, as is the finding that their responses can be affected by visual input to areas outside of the classical receptive field. Less well understood are the ways selectivity is modified as signals propagate to visual areas beyond V1, such as V2. We recently proposed a role for V2 neurons in representing the higher order statistical dependencies found in images of naturally occurring visual texture. V2 neurons, but not V1 neurons, respond more vigorously to “naturalistic” images that contain these dependencies than to “noise” images that lack them. In this work, we examine the dependency of these effects on stimulus size. For most V2 neurons, the preference for naturalistic over noise stimuli was modest when presented in small patches and gradually strengthened with increasing size, suggesting that the mechanisms responsible for this enhanced sensitivity operate over regions of the visual field that are larger than the classical receptive field. Indeed, we found that surround suppression was stronger for noise than for naturalistic stimuli and that the preference for large naturalistic stimuli developed over a delayed time course consistent with lateral or feedback connections. These findings are compatible with a spatially broad facilitatory mechanism that is absent in V1 and suggest that a distinct role for the receptive field surround emerges in V2 along with sensitivity for more complex image structure.

          NEW & NOTEWORTHY The responses of neurons in visual cortex are often affected by visual input delivered to regions of the visual field outside of the conventionally defined receptive field, but the significance of such contextual modulations are not well understood outside of area V1. We studied the importance of regions beyond the receptive field in establishing a novel form of selectivity for the statistical dependencies contained in natural visual textures that first emerges in area V2.

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          Most cited references52

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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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            Circuits for local and global signal integration in primary visual cortex.

            Contrast-dependent changes in spatial summation and contextual modulation of primary visual cortex (V1) neuron responses to stimulation of their receptive field reveal long-distance integration of visual signals within V1, well beyond the classical receptive field (cRF) of single neurons. To identify the cortical circuits mediating these long-distance computations, we have used a combination of anatomical and physiological recording methods to determine the spatial scale and retinotopic logic of intra-areal V1 horizontal connections and inter-areal feedback connections to V1. We have then compared the spatial scales of these connectional systems to the spatial dimensions of the cRF, spatial summation field (SF), and modulatory surround field of macaque V1 neurons. We find that monosynaptic horizontal connections within area V1 are of an appropriate spatial scale to mediate interactions within the SF of V1 neurons and to underlie contrast-dependent changes in SF size. Contrary to common beliefs, these connections cannot fully account for the dimensions of the surround field. The spatial scale of feedback circuits from extrastriate cortex to V1 is, instead, commensurate with the full spatial range of center-surround interactions. Thus these connections could represent an anatomical substrate for contextual modulation and global-to-local integration of visual signals. Feedback projections connect corresponding and equal-sized regions of the visual field in striate and extrastriate cortices and cover anisotropic parts of visual space, unlike V1 horizontal connections that are isotropic in the macaque. V1 isotropic connectivity demonstrates that anisotropic horizontal connections are not necessary to generate orientation selectivity. Anisotropic feedback connections may play a role in contour completion.
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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

                Journal
                J Neurophysiol
                J. Neurophysiol
                jn
                J Neurophysiol
                JN
                Journal of Neurophysiology
                American Physiological Society (Bethesda, MD )
                0022-3077
                1522-1598
                1 August 2018
                11 April 2018
                11 April 2018
                : 120
                : 2
                : 409-420
                Affiliations
                [1] 1Center for Neural Science, New York University , New York, New York
                [2] 2Howard Hughes Medical Institute, New York University , New York, New York
                Author notes
                Address for reprint requests and other correspondence: J. A. Movshon, Center for Neural Science, New York University, 4 Washington Pl., Rm. 809, New York, NY 10003 (e-mail: movshon@ 123456nyu.edu ).
                Article
                JN-00900-2017 JN-00900-2017
                10.1152/jn.00900.2017
                6139455
                29641304
                fbcd1a9b-287a-4b15-abab-88a287924f70
                Copyright © 2018 the American Physiological Society

                Licensed under Creative Commons Attribution CC-BY 4.0: © the American Physiological Society.

                History
                : 18 December 2017
                : 6 April 2018
                : 6 April 2018
                Funding
                Funded by: NIH
                Award ID: EY04440
                Award ID: EY022428
                Funded by: HHMI
                Funded by: NSF
                Award ID: GRFP
                Categories
                Research Article
                Sensory Processing

                Neurology
                natural image statistics,surround suppression,texture,v2,visual cortex
                Neurology
                natural image statistics, surround suppression, texture, v2, visual cortex

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