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      Local processing in neurites of VGluT3-expressing amacrine cells differentially organizes visual information

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          Abstract

          Neurons receive synaptic inputs on extensive neurite arbors. How information is organized across arbors and how local processing in neurites contributes to circuit function is mostly unknown. Here, we used two-photon Ca 2+ imaging to study visual processing in VGluT3-expressing amacrine cells (VG3-ACs) in the mouse retina. Contrast preferences (ON vs. OFF) varied across VG3-AC arbors depending on the laminar position of neurites, with ON responses preferring larger stimuli than OFF responses. Although arbors of neighboring cells overlap extensively, imaging population activity revealed continuous topographic maps of visual space in the VG3-AC plexus. All VG3-AC neurites responded strongly to object motion, but remained silent during global image motion. Thus, VG3-AC arbors limit vertical and lateral integration of contrast and location information, respectively. We propose that this local processing enables the dense VG3-AC plexus to contribute precise object motion signals to diverse targets without distorting target-specific contrast preferences and spatial receptive fields.

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          Most cited references 49

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          Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway.

           Bin He,  Yang Hu,  Bin Cai (2008)
          The failure of axons to regenerate is a major obstacle for functional recovery after central nervous system (CNS) injury. Removing extracellular inhibitory molecules results in limited axon regeneration in vivo. To test for the role of intrinsic impediments to axon regrowth, we analyzed cell growth control genes using a virus-assisted in vivo conditional knockout approach. Deletion of PTEN (phosphatase and tensin homolog), a negative regulator of the mammalian target of rapamycin (mTOR) pathway, in adult retinal ganglion cells (RGCs) promotes robust axon regeneration after optic nerve injury. In wild-type adult mice, the mTOR activity was suppressed and new protein synthesis was impaired in axotomized RGCs, which may contribute to the regeneration failure. Reactivating this pathway by conditional knockout of tuberous sclerosis complex 1, another negative regulator of the mTOR pathway, also leads to axon regeneration. Thus, our results suggest the manipulation of intrinsic growth control pathways as a therapeutic approach to promote axon regeneration after CNS injury.
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            Neural population dynamics during reaching

            Most theories of motor cortex have assumed that neural activity represents movement parameters. This view derives from an analogous approach to primary visual cortex, where neural activity represents patterns of light. Yet it is unclear how well that analogy holds. Single-neuron responses in motor cortex appear strikingly complex, and there is marked disagreement regarding which movement parameters are represented. A better analogy might be with other motor systems, where a common principle is rhythmic neural activity. We found that motor cortex responses during reaching contain a brief but strong oscillatory component, something quite unexpected for a non-periodic behavior. Oscillation amplitude and phase followed naturally from the preparatory state, suggesting a mechanistic role for preparatory neural activity. These results demonstrate unexpected yet surprisingly simple structure in the population response. That underlying structure explains many of the confusing features of individual-neuron responses.
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              Dendritic computation.

              One of the central questions in neuroscience is how particular tasks, or computations, are implemented by neural networks to generate behavior. The prevailing view has been that information processing in neural networks results primarily from the properties of synapses and the connectivity of neurons within the network, with the intrinsic excitability of single neurons playing a lesser role. As a consequence, the contribution of single neurons to computation in the brain has long been underestimated. Here we review recent work showing that neuronal dendrites exhibit a range of linear and nonlinear mechanisms that allow them to implement elementary computations. We discuss why these dendritic properties may be essential for the computations performed by the neuron and the network and provide theoretical and experimental examples to support this view.
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                Author and article information

                Contributors
                Role: Reviewing Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                12 October 2017
                2017
                : 6
                Affiliations
                [1 ]deptDepartment of Ophthalmology and Visual Sciences Washington University School of Medicine Saint LouisUnited States
                [2 ]deptGraduate Program in Neuroscience Washington University School of Medicine Saint LouisUnited States
                [3 ]Allen Institute for Brain Science SeattleUnited States
                [4 ]deptDepartment of Neuroscience Washington University School of Medicine Saint LouisUnited States
                [5 ]deptDepartment of Biomedical Engineering Washington University School of Medicine Saint LouisUnited States
                [6 ]deptHope Center for Neurological Disorders Washington University School of Medicine Saint LouisUnited States
                Howard Hughes Medical Institute, University of Washington United States
                Howard Hughes Medical Institute, University of Washington United States
                Article
                31307
                10.7554/eLife.31307
                5653236
                29022876
                © 2017, Hsiang 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.

                Product
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000053, National Eye Institute;
                Award ID: EY023341
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100001818, Research to Prevent Blindness;
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000053, National Eye Institute;
                Award ID: EY026978
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000053, National Eye Institute;
                Award ID: EY 027411
                Award Recipient :
                Funded by: McDonnell International Scholars Academy;
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000057, National Institute of General Medical Sciences;
                Award ID: GM008151-32
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Short Report
                Neuroscience
                Custom metadata
                Neurite arbors of VGluT3-expressing amacrine cells (VG3-ACs) process visual information locally uniformly detecting object motion while varying in contrast preferences; and in spite of extensive overlap between arbors of neighboring cells population activity in the VG3-AC plexus encodes stimulus positions with subcellular precision.

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