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      Specialized contributions of mid-tier stages of dorsal and ventral pathways to stereoscopic processing in macaque

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          Abstract

          The division of labor between the dorsal and ventral visual pathways has been well studied, but not often with direct comparison at the single-neuron resolution with matched stimuli. Here we directly compared how single neurons in MT and V4, mid-tier areas of the two pathways, process binocular disparity, a powerful cue for 3D perception and actions. We found that MT neurons transmitted disparity signals more quickly and robustly, whereas V4 or its upstream neurons transformed the signals into sophisticated representations more prominently. Therefore, signaling speed and robustness were traded for transformation between the dorsal and ventral pathways. The key factor in this tradeoff was disparity-tuning shape: V4 neurons had more even-symmetric tuning than MT neurons. Moreover, the tuning symmetry predicted the degree of signal transformation across neurons similarly within each area, implying a general role of tuning symmetry in the stereoscopic processing by the two pathways.

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          The cortical organization of speech processing.

          Despite decades of research, the functional neuroanatomy of speech processing has been difficult to characterize. A major impediment to progress may have been the failure to consider task effects when mapping speech-related processing systems. We outline a dual-stream model of speech processing that remedies this situation. In this model, a ventral stream processes speech signals for comprehension, and a dorsal stream maps acoustic speech signals to frontal lobe articulatory networks. The model assumes that the ventral stream is largely bilaterally organized--although there are important computational differences between the left- and right-hemisphere systems--and that the dorsal stream is strongly left-hemisphere dominant.
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            Ventral and dorsal pathways for language.

            Built on an analogy between the visual and auditory systems, the following dual stream model for language processing was suggested recently: a dorsal stream is involved in mapping sound to articulation, and a ventral stream in mapping sound to meaning. The goal of the study presented here was to test the neuroanatomical basis of this model. Combining functional magnetic resonance imaging (fMRI) with a novel diffusion tensor imaging (DTI)-based tractography method we were able to identify the most probable anatomical pathways connecting brain regions activated during two prototypical language tasks. Sublexical repetition of speech is subserved by a dorsal pathway, connecting the superior temporal lobe and premotor cortices in the frontal lobe via the arcuate and superior longitudinal fascicle. In contrast, higher-level language comprehension is mediated by a ventral pathway connecting the middle temporal lobe and the ventrolateral prefrontal cortex via the extreme capsule. Thus, according to our findings, the function of the dorsal route, traditionally considered to be the major language pathway, is mainly restricted to sensory-motor mapping of sound to articulation, whereas linguistic processing of sound to meaning requires temporofrontal interaction transmitted via the ventral route.
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              Some informational aspects of visual perception.

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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
                24 February 2021
                2021
                : 10
                : e58749
                Affiliations
                [1 ]Laboratory for Cognitive Neuroscience, Graduate School of Frontier Biosciences, Osaka University SuitaOsakaJapan
                [2 ]Center for Information and Neural Networks, Osaka University and National Institute of Information and Communications Technology SuitaOsakaJapan
                [3 ]Department of Psychology, University of Pennsylvania PhiladelphiaUnited States
                [4 ]Laboratory for Neural Circuits and Behavior, RIKEN Center for Brain Science (CBS) WakoJapan
                Zhejiang University China
                National Institute of Mental Health, National Institutes of Health United States
                Zhejiang University China
                Zhejiang University China
                University of Oxford United Kingdom
                Author notes
                [†]

                Brain Science Institute, Tamagawa University, Tokyo, Japan.

                Author information
                https://orcid.org/0000-0001-6475-4627
                https://orcid.org/0000-0002-9650-972X
                https://orcid.org/0000-0003-3658-2623
                https://orcid.org/0000-0003-3293-8610
                Article
                58749
                10.7554/eLife.58749
                7959693
                33625356
                bdb7a6d9-a80e-440e-9150-1918124f75c3
                © 2021, Yoshioka 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
                : 09 May 2020
                : 18 February 2021
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001700, Ministry of Education, Culture, Sports, Science and Technology;
                Award ID: 2324007
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001700, Ministry of Education, Culture, Sports, Science and Technology;
                Award ID: 15H01437
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001700, Ministry of Education, Culture, Sports, Science and Technology;
                Award ID: 17H01381
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001700, Ministry of Education, Culture, Sports, Science and Technology;
                Award ID: 18H05007
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100009105, Ministry of Internal Affairs and Communications;
                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
                Visual area MT signals binocular disparity quickly and robustly, whereas area V4 or its upstream area transforms the nature of the signals to derive a more sophisticated depth representation.

                Life sciences
                stereopsis,binocular vision,extrastriate visual cortex,disparity energy model,false-match rejection,japanese macaque,rhesus macaque

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