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      Multiple Visual Field Representations in the Visual Wulst of a Laterally Eyed Bird, the Zebra Finch ( Taeniopygia guttata)

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          Abstract

          The visual wulst is the telencephalic target of the avian thalamofugal visual system. It contains several retinotopically organised representations of the contralateral visual field. We used optical imaging of intrinsic signals, electrophysiological recordings, and retrograde tracing with two fluorescent tracers to evaluate properties of these representations in the zebra finch, a songbird with laterally placed eyes. Our experiments revealed that there is some variability of the neuronal maps between individuals and also concerning the number of detectable maps. It was nonetheless possible to identify three different maps, a posterolateral, a posteromedial, and an anterior one, which were quite constant in their relation to each other. The posterolateral map was in contrast to the two others constantly visible in each successful experiment. The topography of the two other maps was mirrored against that map. Electrophysiological recordings in the anterior and the posterolateral map revealed that all units responded to flashes and to moving bars. Mean directional preferences as well as latencies were different between neurons of the two maps. Tracing experiments confirmed previous reports on the thalamo-wulst connections and showed that the anterior and the posterolateral map receive projections from separate clusters within the thalamic nuclei. Maps are connected to each other by wulst intrinsic projections. Our experiments confirm that the avian visual wulst contains several separate retinotopic maps with both different physiological properties and different thalamo-wulst afferents. This confirms that the functional organization of the visual wulst is very similar to its mammalian equivalent, the visual cortex.

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          Most cited references54

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          Separate visual pathways for perception and action.

          Accumulating neuropsychological, electrophysiological and behavioural evidence suggests that the neural substrates of visual perception may be quite distinct from those underlying the visual control of actions. In other words, the set of object descriptions that permit identification and recognition may be computed independently of the set of descriptions that allow an observer to shape the hand appropriately to pick up an object. We propose that the ventral stream of projections from the striate cortex to the inferotemporal cortex plays the major role in the perceptual identification of objects, while the dorsal stream projecting from the striate cortex to the posterior parietal region mediates the required sensorimotor transformations for visually guided actions directed at such objects.
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            Contribution of striate inputs to the visuospatial functions of parieto-preoccipital cortex in monkeys.

            In Experiments 1 and 2, monkeys received 3-stage operations intended to serially disconnect parieto-preoccipital from striate cortex. At each stage (unilateral parieto-preoccipital removal, contralateral striate removal and posterior callosal transection) the monkeys were tested for retention of the landmark task, a visuospatial discrimination sensitive to the effects of bilateral parieto-preoccipital damage. To check the effectiveness of the disconnection, the monkeys were also tested after removal of the remaining parieto-preoccipital cortex. The results demonstrated that corticocortical inputs from striate cortex are crucial for the visuospatial functions of parieto-preoccipital cortex, just as they had been shown earlier to be crucial for the pattern discrimination functions of inferior temporal cortex. Relative to inferior temporal cortex, however, parieto-preoccipital cortex was found to be especially dependent on ipsilateral (as compared with contralateral) striate inputs. In Experiment 3, monkeys received bilateral lesions of either lateral on medial striate cortex and were tested on both a pattern discrimination task, to assess residual inferior temporal function, and the landmark task, to assess residual parieto-preoccipital function. The results indicated that the pattern discrimination functions of inferior temporal cortex are especially dependent on inputs from lateral striate cortex, whereas the visuospatial functions of parieto-preoccipital cortex are equally dependent on inputs from lateral and medial striate cortex. The relatively greater contribution to parieto-preoccipital than to inferior temporal cortex made by ipsilateral and medial striate inputs (representing contralateral and peripheral visual fields, respectively) can also be seen in the receptive field properties of parieto-preoccipital and inferior temporal neurons. The differences in the organization of striate inputs to these two cortical association areas presumably reflect differences in the processing required for spatial vs object vision.
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              Iso-orientation domains in cat visual cortex are arranged in pinwheel-like patterns.

              The mammalian cortex is organized in a columnar fashion: neurons lying below each other from the pia to the white matter usually share many functional properties. Across the cortical surface, cells with similar response properties are also clustered together, forming elongated bands or patches. Some response properties, such as orientation preference in the visual cortex, change gradually across the cortical surface forming 'orientation maps'. To determine the precise layout of iso-orientation domains, knowledge of responses not only to one but to many stimulus orientations is essential. Therefore, the exact depiction of orientation maps has been hampered by technical difficulties and remained controversial for almost thirty years. Here we use in vivo optical imaging based on intrinsic signals to gather information on the responses of a piece of cortex to gratings in many different orientations. This complete set of responses then provides detailed information on the structure of the orientation map in a large patch of cortex from area 18 of the cat. We find that cortical regions that respond best to one orientation form highly ordered patches rather than elongated bands. These iso-orientation patches are organized around 'orientation centres', producing pinwheel-like patterns in which the orientation preference of cells is changing continuously across the cortex. We have also analysed our data for fast changes in orientation preference and find that these 'fractures' are limited to the orientation centres. The pinwheels and orientation centres are such a prominent organizational feature that it should be important to understand their development as well as their function in the processing of visual information.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                3 May 2016
                2016
                : 11
                : 5
                : e0154927
                Affiliations
                [1 ]Verhaltensforschung, Universität Bielefeld, Bielefeld, Germany
                [2 ]Champalimaud Neuroscience Programme, Center for the Unknown, Lisbon, Portugal
                [3 ]Department of Systems Neuroscience, Johann-Friedrich-Blumenbach Institut für Zoologie und Anthropologie, Universität Göttingen, Göttingen, Germany
                [4 ]Center for Mind/Brain Sciences, University of Trento, Rovereto, Italy
                [5 ]Göttingen Graduate School for Neurosciences, Biophysics, and Molecular Biosciences (GGNB), Göttingen, Germany
                Utrecht University, NETHERLANDS
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: HJB. Performed the experiments: NK UM NM. Analyzed the data: HJB DE NK UM NM. Contributed reagents/materials/analysis tools: DE. Wrote the paper: HJB SL.

                Article
                PONE-D-16-09155
                10.1371/journal.pone.0154927
                4854416
                27139912
                e40ade59-99d8-4815-a5f8-f598f72a82ff
                © 2016 Bischof et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 3 March 2016
                : 21 April 2016
                Page count
                Figures: 9, Tables: 0, Pages: 23
                Funding
                Funded by: BMBF (Bundesministerium für Bildung und Forschung
                Award ID: 01GQ0810
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: Bi245/21-1
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: Lo442/8-1
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: Lo442/8-2
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: GSC226/2
                This study was funded by grants from a Federal Ministry of Education and Research (Bundesministerium für Bildung und Forschung, BMBF, http://www.bmbf.de/)-grant number 01GQ0810 (S.L.), DeutscheForschungsgemeinschaft (DFG) ( http://www.dfg.de/index.jsp) Grant numbers: BI 245/21-1 (HJB), LO 442/8-1 and LO 442/8-2 (SL), GSC 226/2, (Göttingen Graduate School for Neurosciences, Biophysics and Molecular Biosciences Grant to NM). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Animal Cells
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