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      Plasticity in the Structure of Visual Space

      research-article
      , ,
      eNeuro
      Society for Neuroscience
      Lateral connections, visual plasticity, visual space

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          Visual Abstract

          Abstract

          Visual space embodies all visual experiences, yet what determines the topographical structure of visual space remains unclear. Here we test a novel theoretical framework that proposes intrinsic lateral connections in the visual cortex as the mechanism underlying the structure of visual space. The framework suggests that the strength of lateral connections between neurons in the visual cortex shapes the experience of spatial relatedness between locations in the visual field. As such, an increase in lateral connection strength shall lead to an increase in perceived relatedness and a contraction in perceived distance. To test this framework through human psychophysics experiments, we used a Hebbian training protocol in which two-point stimuli were flashed in synchrony at separate locations in the visual field, to strengthen the lateral connections between two separate groups of neurons in the visual cortex. After training, participants experienced a contraction in perceived distance. Intriguingly, the perceptual contraction occurred not only between the two training locations that were linked directly by the changed connections, but also between the outward untrained locations that were linked indirectly through the changed connections. Moreover, the effect of training greatly decreased if the two training locations were too close together or too far apart and went beyond the extent of lateral connections. These findings suggest that a local change in the strength of lateral connections is sufficient to alter the topographical structure of visual space.

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          Most cited references39

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          Spike timing-dependent plasticity: a Hebbian learning rule.

          Spike timing-dependent plasticity (STDP) as a Hebbian synaptic learning rule has been demonstrated in various neural circuits over a wide spectrum of species, from insects to humans. The dependence of synaptic modification on the order of pre- and postsynaptic spiking within a critical window of tens of milliseconds has profound functional implications. Over the past decade, significant progress has been made in understanding the cellular mechanisms of STDP at both excitatory and inhibitory synapses and of the associated changes in neuronal excitability and synaptic integration. Beyond the basic asymmetric window, recent studies have also revealed several layers of complexity in STDP, including its dependence on dendritic location, the nonlinear integration of synaptic modification induced by complex spike trains, and the modulation of STDP by inhibitory and neuromodulatory inputs. Finally, the functional consequences of STDP have been examined directly in an increasing number of neural circuits in vivo.
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            Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging.

            The borders of human visual areas V1, V2, VP, V3, and V4 were precisely and noninvasively determined. Functional magnetic resonance images were recorded during phase-encoded retinal stimulation. This volume data set was then sampled with a cortical surface reconstruction, making it possible to calculate the local visual field sign (mirror image versus non-mirror image representation). This method automatically and objectively outlines area borders because adjacent areas often have the opposite field sign. Cortical magnification factor curves for striate and extrastriate cortical areas were determined, which showed that human visual areas have a greater emphasis on the center-of-gaze than their counterparts in monkeys. Retinotopically organized visual areas in humans extend anteriorly to overlap several areas previously shown to be activated by written words.
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              The relationship between cortical magnification factor and population receptive field size in human visual cortex: constancies in cortical architecture.

              Receptive field (RF) sizes and cortical magnification factor (CMF) are fundamental organization properties of the visual cortex. At increasing visual eccentricity, RF sizes increase and CMF decreases. A relationship between RF size and CMF suggests constancies in cortical architecture, as their product, the cortical representation of an RF (point image), may be constant. Previous animal neurophysiology studies of this question yield conflicting results. Here, we use fMRI to determine the relationship between the population RF (pRF) and CMF in humans. In average and individual data, the product of CMF and pRF size, the population point image, is near constant, decreasing slightly with eccentricity in V1. Interhemisphere and subject variations in CMF, pRF size, and V1 surface area are correlated, and the population point image varies less than these properties. These results suggest a V1 cortical processing architecture of approximately constant size between humans. Up the visual hierarchy, to V2, V3, hV4, and LO1, the population point image decreases with eccentricity, and both the absolute values and rate of change increase. PRF sizes increase between visual areas and with eccentricity, but when expressed in V1 cortical surface area (i.e., corticocortical pRFs), they are constant across eccentricity in V2/V3. Thus, V2/V3, and to some degree hV4, sample from a constant extent of V1. This may explain population point image changes in later areas. Consequently, the constant factor determining pRF size may not be the relationship to the local CMF, but rather pRF sizes and CMFs in visual areas from which the pRF samples.
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                Author and article information

                Journal
                eNeuro
                eNeuro
                eneuro
                eneuro
                eNeuro
                eNeuro
                Society for Neuroscience
                2373-2822
                5 June 2017
                23 June 2017
                May-Jun 2017
                : 4
                : 3
                : ENEURO.0080-17.2017
                Affiliations
                [1]Department of Psychiatry, University of Wisconsin-Madison , Madison, WI 53719
                Author notes

                Authors report no conflict of interest.

                Author contributions: CS conducted the experiment. CS and AH designed the experiment and analyzed the data. CS, AH, and GT conceived the study and wrote the paper.

                The study was supported by Templeton Foundation (GT).

                Correspondence should be addressed to Giulio Tononi, University of Wisconsin-Madison, 6001 Research Park Blvd., Madison, WI 53719. E-mail: gtononi@ 123456wisc.edu .
                Author information
                http://orcid.org/0000-0002-5418-5747
                Article
                eN-NWR-0080-17
                10.1523/ENEURO.0080-17.2017
                5482114
                28660245
                b598eff0-58c7-464c-bff1-7b8b02e8e073
                Copyright © 2017 Song et al.

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

                History
                : 10 March 2017
                : 10 May 2017
                : 1 June 2017
                Page count
                Figures: 4, Tables: 0, Equations: 0, References: 49, Pages: 7, Words: 4859
                Funding
                Funded by: John Templeton Foundation
                Award ID: 100000925
                Categories
                8
                8.1
                New Research
                Sensory and Motor Systems
                Custom metadata
                May/June 2017

                lateral connections,visual plasticity,visual space
                lateral connections, visual plasticity, visual space

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