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      Features of the Retinotopic Representation in the Visual Wulst of a Laterally Eyed Bird, the Zebra Finch ( Taeniopygia guttata)

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          Abstract

          The visual wulst of the zebra finch comprises at least two retinotopic maps of the contralateral eye. As yet, it is not known how much of the visual field is represented in the wulst neuronal maps, how the organization of the maps is related to the retinal architecture, and how information from the ipsilateral eye is involved in the activation of the wulst. Here, we have used autofluorescent flavoprotein imaging and classical anatomical methods to investigate such characteristics of the most posterior map of the multiple retinotopic representations. We found that the visual wulst can be activated by visual stimuli from a large part of the visual field of the contralateral eye. Horizontally, the visual field representation extended from -5° beyond the beak tip up to +125° laterally. Vertically, a small strip from -10° below to about +25° above the horizon activated the visual wulst. Although retinal ganglion cells had a much higher density around the fovea and along a strip extending from the fovea towards the beak tip, these areas were not overrepresented in the wulst map. The wulst area activated from the foveal region of the ipsilateral eye, overlapped substantially with the middle of the three contralaterally activated regions in the visual wulst, and partially with the other two. Visual wulst activity evoked by stimulation of the frontal visual field was stronger with contralateral than with binocular stimulation. This confirms earlier electrophysiological studies indicating an inhibitory influence of the activation of the ipsilateral eye on wulst activity elicited by stimulating the contralateral eye. The lack of a foveal overrepresentation suggests that identification of objects may not be the primary task of the zebra finch visual wulst. Instead, this brain area may be involved in the processing of visual information necessary for spatial orientation.

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          New paradigm for optical imaging: temporally encoded maps of intrinsic signal.

          We present a new technique for acquiring and analyzing intrinsic signal optical images of brain activity, using continuous stimulus presentation and data acquisition. The main idea is to present a temporally periodic stimulus and to analyze the component of the response at the stimulus frequency. Advantages of the new technique include the removal of heart, respiration, and vasomotor artifacts, a dramatic increase in spatial resolution, and a 30-fold or greater reduction in acquisition time. We also present a novel approach to localizing instantaneous neuronal responses using time-reversed stimuli that is widely applicable to brain imaging. To demonstrate the power of the technique, we present high-resolution retinotopic maps of five visual areas in mouse cortex and orientation maps in cat visual cortex.
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            Visual but not trigeminal mediation of magnetic compass information in a migratory bird.

            Magnetic compass information has a key role in bird orientation, but the physiological mechanisms enabling birds to sense the Earth's magnetic field remain one of the unresolved mysteries in biology. Two biophysical mechanisms have become established as the most promising magnetodetection candidates. The iron-mineral-based hypothesis suggests that magnetic information is detected by magnetoreceptors in the upper beak and transmitted through the ophthalmic branch of the trigeminal nerve to the brain. The light-dependent hypothesis suggests that magnetic field direction is sensed by radical pair-forming photopigments in the eyes and that this visual signal is processed in cluster N, a specialized, night-time active, light-processing forebrain region. Here we report that European robins with bilateral lesions of cluster N are unable to show oriented magnetic-compass-guided behaviour but are able to perform sun compass and star compass orientation behaviour. In contrast, bilateral section of the ophthalmic branch of the trigeminal nerve in European robins did not influence the birds' ability to use their magnetic compass for orientation. These data show that cluster N is required for magnetic compass orientation in this species and indicate that it may be specifically involved in processing of magnetic compass information. Furthermore, the data strongly suggest that a vision-mediated mechanism underlies the magnetic compass in this migratory songbird, and that the putative iron-mineral-based receptors in the upper beak connected to the brain by the trigeminal nerve are neither necessary nor sufficient for magnetic compass orientation in European robins.
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              A Visual Pathway Links Brain Structures Active during Magnetic Compass Orientation in Migratory Birds

              The magnetic compass of migratory birds has been suggested to be light-dependent. Retinal cryptochrome-expressing neurons and a forebrain region, “Cluster N”, show high neuronal activity when night-migratory songbirds perform magnetic compass orientation. By combining neuronal tracing with behavioral experiments leading to sensory-driven gene expression of the neuronal activity marker ZENK during magnetic compass orientation, we demonstrate a functional neuronal connection between the retinal neurons and Cluster N via the visual thalamus. Thus, the two areas of the central nervous system being most active during magnetic compass orientation are part of an ascending visual processing stream, the thalamofugal pathway. Furthermore, Cluster N seems to be a specialized part of the visual wulst. These findings strongly support the hypothesis that migratory birds use their visual system to perceive the reference compass direction of the geomagnetic field and that migratory birds “see” the reference compass direction provided by the geomagnetic field.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                8 April 2015
                2015
                : 10
                : 4
                : e0124917
                Affiliations
                [1 ]Department of Systems Neuroscience, Johann-Friedrich-Blumenbach Institut für Zoologie und Anthropologie, Universität Göttingen, Göttingen, Germany
                [2 ]Verhaltensforschung, Universität Bielefeld, Bielefeld, Germany
                [3 ]Göttingen Graduate School for Neurosciences, Biophysics, and Molecular Biosciences (GGNB), Göttingen, Germany
                Universität Bielefeld, GERMANY
                Author notes

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

                Conceived and designed the experiments: NM SL HJB. Performed the experiments: NM. Analyzed the data: NM SL HJB. Wrote the paper: NM SL HJB.

                Article
                PONE-D-15-02365
                10.1371/journal.pone.0124917
                4390349
                25853253
                71ae8c4e-b67f-47b8-ab31-68de3b9ef708
                Copyright @ 2015

                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
                : 17 January 2015
                : 13 March 2015
                Page count
                Figures: 10, Tables: 0, Pages: 26
                Funding
                This study was funded by grants from the Federal Ministry of Education and Research (Bundesministerium für Bildung und Forschung, BMBF, http://www.bmbf.de/)-grant number 01GQ0810 (S.L), the Deutsche Forschungsgemeinschaft (DFG) ( http://www.dfg.de/index.jsp)-grant numbers BI 245/21-1, LO 442/8-1 and LO 442/8-2, Göttingen Graduate School for Neurosciences, Biophysics and Molecular Biosciences (DFG Grant GSC 226/2). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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