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      Light-incubation effects on lateralisation of single unit responses in the visual Wulst of domestic chicks

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          Abstract

          Since the ground-breaking discovery that in-egg light exposure triggers the emergence of visual lateralisation, domestic chicks became a crucial model for research on the interaction of environmental and genetic influences for brain development. In domestic chick embryos, light exposure induces neuroanatomical asymmetries in the strength of visual projections from the thalamus to the visual Wulst. Consequently, the right visual Wulst receives more bilateral information from the two eyes than the left one. How this impacts visual Wulst’s physiology is still unknown. This paper investigates the visual response properties of neurons in the left and right Wulst of dark- and light-incubated chicks, studying the effect of light incubation on bilaterally responsive cells that integrate information from both eyes. We recorded from a large number of visually responsive units, providing the first direct evidence of lateralisation in the neural response properties of units of the visual Wulst. While we confirm that some forms of lateralisation are induced by embryonic light exposure, we found also many cases of light-independent asymmetries. Moreover, we found a strong effect of in-egg light exposure on the general development of the functional properties of units in the two hemispheres. This indicates that the effect of embryonic stimulation goes beyond its contribution to the emergence of some forms of lateralisation, with influences on the maturation of visual units in both hemispheres.

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            Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization.

            Recent evidence in natural and semi-natural settings has revealed a variety of left-right perceptual asymmetries among vertebrates. These include preferential use of the left or right visual hemifield during activities such as searching for food, agonistic responses, or escape from predators in animals as different as fish, amphibians, reptiles, birds, and mammals. There are obvious disadvantages in showing such directional asymmetries because relevant stimuli may be located to the animal's left or right at random; there is no a priori association between the meaning of a stimulus (e.g., its being a predator or a food item) and its being located to the animal's left or right. Moreover, other organisms (e.g., predators) could exploit the predictability of behavior that arises from population-level lateral biases. It might be argued that lateralization of function enhances cognitive capacity and efficiency of the brain, thus counteracting the ecological disadvantages of lateral biases in behavior. However, such an increase in brain efficiency could be obtained by each individual being lateralized without any need to align the direction of the asymmetry in the majority of the individuals of the population. Here we argue that the alignment of the direction of behavioral asymmetries at the population level arises as an "evolutionarily stable strategy" under "social" pressures occurring when individually asymmetrical organisms must coordinate their behavior with the behavior of other asymmetrical organisms of the same or different species.
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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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                Author and article information

                Contributors
                giorgio.vallortigara@unitn.it
                Journal
                Brain Struct Funct
                Brain Struct Funct
                Brain Structure & Function
                Springer Berlin Heidelberg (Berlin/Heidelberg )
                1863-2653
                1863-2661
                30 March 2021
                30 March 2021
                2022
                : 227
                : 2
                : 497-513
                Affiliations
                [1 ]GRID grid.11696.39, ISNI 0000 0004 1937 0351, Center for Mind/Brain Science, , University of Trento, ; Piazza Manifattura 1, 38068 Rovereto, TN Italy
                [2 ]GRID grid.419542.f, ISNI 0000 0001 0705 4990, Max Planck Institute for Ornithology, ; Seewiesen, Germany
                Author information
                http://orcid.org/0000-0001-8192-9062
                Article
                2259
                10.1007/s00429-021-02259-y
                8844149
                33783595
                93261744-63de-456d-8cb2-9476131bb996
                © The Author(s) 2021

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 15 February 2021
                : 16 March 2021
                Funding
                Funded by: European Research Council (Horizon 2020)
                Award ID: 833504
                Award Recipient :
                Funded by: PRIN 2017 ERC-SH4–A
                Award ID: 2017PSRHPZ
                Award Recipient :
                Funded by: Università degli Studi di Trento
                Categories
                Original Article
                Custom metadata
                © Springer-Verlag GmbH Germany, part of Springer Nature 2022

                Neurology
                lateralisation,visual wulst,domestic chicks,development,light exposure,electrophysiology
                Neurology
                lateralisation, visual wulst, domestic chicks, development, light exposure, electrophysiology

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