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      Response to short-term deprivation of the human adult visual cortex measured with 7T BOLD

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          Abstract

          Sensory deprivation during the post-natal ‘critical period’ leads to structural reorganization of the developing visual cortex. In adulthood, the visual cortex retains some flexibility and adapts to sensory deprivation. Here we show that short-term (2 hr) monocular deprivation in adult humans boosts the BOLD response to the deprived eye, changing ocular dominance of V1 vertices, consistent with homeostatic plasticity. The boost is strongest in V1, present in V2, V3 and V4 but absent in V3a and hMT+. Assessment of spatial frequency tuning in V1 by a population Receptive-Field technique shows that deprivation primarily boosts high spatial frequencies, consistent with a primary involvement of the parvocellular pathway. Crucially, the V1 deprivation effect correlates across participants with the perceptual increase of the deprived eye dominance assessed with binocular rivalry, suggesting a common origin. Our results demonstrate that visual cortex, particularly the ventral pathway, retains a high potential for homeostatic plasticity in the human adult.

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          The world around us changes all the time, and the brain must adapt to these changes. This process, known as neuroplasticity, peaks during development. Abnormal sensory input early in life can therefore cause lasting changes to the structure of the brain. One example of this is amblyopia or ‘lazy eye’. Infants who receive insufficient input to one eye – for example, because of cataracts – can lose their sight in that eye, even if the cataracts are later removed. This is because the brain reorganizes itself to ignore messages from the affected eye.

          Does the adult visual system also show neuroplasticity? To explore this question, Binda, Kurzawski et al. asked healthy adult volunteers to lie inside a high-resolution brain scanner with a patch covering one eye. At the start of the experiment, roughly half of the brain’s primary visual cortex responded to sensory input from each eye. But when the volunteers removed the patch two hours later, this was no longer the case.

          Some areas of the visual cortex that had previously responded to stimuli presented to the non-patched eye now responded to stimuli presented to the patched eye instead. The patched eye had also become more sensitive to visual stimuli. Indeed, these changes in visual sensitivity correlated with changes in brain activity in a pathway called the ventral visual stream. This pathway processes the fine details of images. Groups of neurons within this pathway that responded to stimuli presented to the patched eye were more sensitive to fine details after patching than before.

          Visual regions of the adult brain thus retain a high degree of neuroplasticity. They adapt rapidly to changes in the environment, in this case by increasing their activity to compensate for a lack of input. Notably, these changes are in the opposite direction to those that occur as a result of visual deprivation during development. This has important implications because lazy eye syndrome is currently considered untreatable in adulthood.

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          Most cited references72

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          Functional MRI evidence for adult motor cortex plasticity during motor skill learning.

          Performance of complex motor tasks, such as rapid sequences of finger movements, can be improved in terms of speed and accuracy over several weeks by daily practice sessions. This improvement does not generalize to a matched sequence of identical component movements, nor to the contralateral hand. Here we report a study of the neural changes underlying this learning using functional magnetic resonance imaging (MRI) of local blood oxygenation level-dependent (BOLD) signals evoked in primary motor cortex (M1). Before training, a comparable extent of M1 was activated by both sequences. However, two ordering effects were observed: repeating a sequence within a brief time window initially resulted in a smaller area of activation (habituation), but later in larger area of activation (enhancement), suggesting a switch in M1 processing mode within the first session (fast learning). By week 4 of training, concurrent with asymptotic performance, the extent of cortex activated by the practised sequence enlarged compared with the unpractised sequence, irrespective of order (slow learning). These changes persisted for several months. The results suggest a slowly evolving, long-term, experience-dependent reorganization of the adult M1, which may underlie the acquisition and retention of the motor skill.
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            The contrast sensitivity of retinal ganglion cells of the cat.

            1. Spatial summation within cat retinal receptive fields was studied by recording from optic-tract fibres the responses of ganglion cells to grating patterns whose luminance perpendicular to the bars varied sinusoidally about the mean level. 2. Summation over the receptive fields of some cells (X-cells) was found to be approximately linear, while for other cells (Y-cells) summation was very non-linear. 3. The mean discharge frequency of Y-cells (unlike that of X-cells) was greatly increased when grating patterns drifted across their receptive fields. 4. In twenty-one X-cells the relation between the contrast and spatial frequency of drifting sinusoidal gratings which evoked the same small response was measured. In every case it was found that the reciprocal of this relation, the contrast sensitivity function, could be satisfactorily described by the difference of two Gaussian functions. 5. This finding supports the hypothesis that the sensitivities of the antagonistic centre and surround summating regions of ganglion cell receptive fields fall off as Gaussian functions of the distance from the field centre. 6. The way in which the sensitivity of an X-cell for a contrast-edge pattern varied with the distance of the edge from the receptive field centre was determined and found to be consistent with the cell's measured contrast sensitivity function. 7. Reducing the retinal illumination produced changes in the contrast sensitivity function of an X-cell which suggested that the diameters of the summating regions of the receptive field increased while the surround region became relatively ineffective.
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              On the existence of neurones in the human visual system selectively sensitive to the orientation and size of retinal images.

              1. It was found that an occipital evoked potential can be elicited in the human by moving a grating pattern without changing the mean light flux entering the eye. Prolonged viewing of a high contrast grating reduces the amplitude of the potential evoked by a low contrast grating.2. This adaptation to a grating was studied psychophysically by determining the contrast threshold before and after adaptation. There is a temporary fivefold rise in contrast threshold after exposure to a high contrast grating of the same orientation and spatial frequency.3. By determining the rise of threshold over a range of spatial frequency for a number of adapting frequencies it was found that the threshold elevation is limited to a spectrum of frequencies with a bandwidth of just over an octave at half amplitude, centred on the adapting frequency.4. The amplitude of the effect and its bandwidth are very similar for adapting spatial frequencies between 3 c/deg. and 14 c/deg. At higher frequencies the bandwidth is slightly narrower. For lower adapting frequencies the peak of the effect stays at 3 c/deg.5. These and other findings suggest that the human visual system may possess neurones selectively sensitive to spatial frequency and size. The orientational selectivity and the interocular transfer of the adaptation effect implicate the visual cortex as the site of these neurones.6. This neural system may play an essential preliminary role in the recognition of complex images and generalization for magnification.
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                Author and article information

                Contributors
                Role: Reviewing Editor
                Role: Senior Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                26 November 2018
                2018
                : 7
                : e40014
                Affiliations
                [1 ]University of Pisa PisaItaly
                [2 ]deptDepartment of Neuroscience University of Florence FlorenceItaly
                [3 ]IRCCS Stella Maris PisaItaly
                [4 ]deptDépartement d’études cognitives, École normale supérieure, Laboratoire des systèmes perceptifs PSL Research University, CNRS ParisFrance
                [5 ]IMAGO Center PisaItaly
                University of Rochester United States
                University of Pennsylvania United States
                University of Rochester United States
                Author notes
                [†]

                These authors contributed equally to this work.

                Author information
                http://orcid.org/0000-0002-7200-353X
                http://orcid.org/0000-0003-2781-1236
                http://orcid.org/0000-0003-3811-5404
                http://orcid.org/0000-0003-2159-439X
                http://orcid.org/0000-0002-2515-7560
                http://orcid.org/0000-0002-1025-0316
                Article
                40014
                10.7554/eLife.40014
                6298775
                30475210
                7a5c7efb-e0c0-4524-a36f-1d6f0274a297
                © 2018, Binda et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 11 July 2018
                : 26 November 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100000781, European Research Council;
                Award ID: ERC ECSPLAIN 338866
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100010686, H2020 European Institute of Innovation and Technology;
                Award ID: NextGenVis 641805
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100003407, Ministero dell’Istruzione, dell’Università e della Ricerca;
                Award ID: PRIN2015
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000781, European Research Council;
                Award ID: ERA-NET Neuro-DREAM
                Award Recipient :
                Funded by: Fondazione Roma;
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Neuroscience
                Custom metadata
                Two hour deprivation of vision in one eye transiently boosts the representation of the deprived eye (suppressing the non-deprived eye) in adult human V1 and along the ventral pathway.

                Life sciences
                ultra-high field magnetic resonance,visual cortex,homeostatic plasticity,monocular deprivation,spatial frequency selectivity,population receptive field,human

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