Lateralization of the Avian Magnetic Compass: Analysis of Its Early Plasticity

In European Robins, Erithacus rubecula, the magnetic compass is lateralized in favor of the right eye/left hemisphere of the brain. This lateralization develops during the first winter and initially shows a great plasticity. During the first spring migration, it can be temporarily removed by covering the right eye. In the present paper, we used the migratory orientation of robins to analyze the circumstances under which the lateralization can be undone. Already a period of 1½ h being monocularly left-eyed before tests began proved sufficient to restore the ability to use the left eye for orientation, but this effect was rather short-lived, as lateralization recurred again within the next 1½ h. Interpretable magnetic information mediated by the left eye was necessary for removing the lateralization. In addition, monocularly, the left eye seeing robins could adjust to magnetic intensities outside the normal functional window, but this ability was not transferred to the “right-eye system”. Our results make it clear that asymmetry of magnetic compass perception is amenable to short-term changes, depending on lateralized stimulation. This could mean that the left hemispheric dominance for the analysis of magnetic compass information depends on lateralized interhemispheric interactions that in young birds can swiftly be altered by environmental effects.

[1]  H. Mouritsen,et al.  Night-migratory garden warblers can orient with their magnetic compass using the left, the right or both eyes , 2010, Journal of The Royal Society Interface.

[2]  P. Kukura,et al.  Radio frequency magnetic field effects on a radical recombination reaction: a diagnostic test for the radical pair mechanism. , 2004, Journal of the American Chemical Society.

[3]  W. Singer,et al.  Abnormal interhemispheric motor interactions in patients with callosal agenesis , 2015, Behavioural Brain Research.

[4]  G. Vallortigara,et al.  Laterality in the wild: preferential hemifield use during predatory and sexual behaviour in the black-winged stilt , 2005, Animal Behaviour.

[5]  M. Dadda,et al.  Does brain asymmetry allow efficient performance of simultaneous tasks? , 2006, Animal Behaviour.

[6]  O. Güntürkün,et al.  Development of lateralization of the magnetic compass in a migratory bird , 2012, Proceedings of the Royal Society B: Biological Sciences.

[7]  L. Peichl,et al.  Avian Ultraviolet/Violet Cones Identified as Probable Magnetoreceptors , 2011, PloS one.

[8]  G. Vallortigara,et al.  survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization , 2005, Behavioral and Brain Sciences.

[9]  G. Vallortigara,et al.  Brain asymmetry (animal). , 2011, Wiley interdisciplinary reviews. Cognitive science.

[10]  O. Güntürkün,et al.  Asymmetrical Modes of Visual Bottom-Up and Top-Down Integration in the Thalamic Nucleus Rotundus of Pigeons , 2004, The Journal of Neuroscience.

[11]  L. Rogers,et al.  Lateralized response of chicks to magnetic cues , 2008, Behavioural Brain Research.

[12]  A. Wohlschläger,et al.  Unihemispheric memory in pigeons-knowledge, the left hemisphere is reluctant to share , 2002, Behavioural Brain Research.

[13]  O. Güntürkün,et al.  Lateralization of magnetic compass orientation in pigeons , 2010, Journal of The Royal Society Interface.

[14]  W. Wiltschko,et al.  Lateralisation of magnetic compass orientation in silvereyes, Zosterops lateralis , 2003 .

[15]  O. Güntürkün,et al.  Asymmetry pays: visual lateralization improves discrimination success in pigeons , 2000, Current Biology.

[16]  Thorsten Ritz,et al.  Resonance effects indicate a radical-pair mechanism for avian magnetic compass , 2004, Nature.

[17]  K. Schulten,et al.  A model for photoreceptor-based magnetoreception in birds. , 2000, Biophysical journal.

[18]  G. Vallortigara,et al.  Advantages of having a lateralized brain , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[19]  E. Jarvis,et al.  Night-time neuronal activation of Cluster N in a day- and night-migrating songbird , 2010, The European journal of neuroscience.

[20]  O. Güntürkün,et al.  Lateralization of magnetic compass orientation in a migratory bird , 2002, Nature.

[21]  Henrik Mouritsen,et al.  Visual but not trigeminal mediation of magnetic compass information in a migratory bird , 2009, Nature.

[22]  O. Güntürkün,et al.  Evidence for physiological asymmetries in the intertectal connections of the pigeon (Columba livia) and their potential role in brain lateralisation , 2000, Brain Research.

[23]  O. Güntürkün,et al.  Ascending and descending mechanisms of visual lateralization in pigeons , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[24]  E. Kandel,et al.  Structural Components of Synaptic Plasticity and Memory Consolidation. , 2015, Cold Spring Harbor perspectives in biology.

[25]  O. Güntürkün,et al.  Monocular deprivation alters the direction of functional and morphological asymmetries in the pigeon's (Columba livia) visual system. , 1999, Behavioral neuroscience.

[26]  W. Wiltschko,et al.  Oscillating magnetic field disrupts magnetic orientation in Zebra finches, Taeniopygia guttata , 2009, Frontiers in Zoology.

[27]  O. Güntürkün.  Morphological asymmetries of the tectum opticum in the pigeon , 1997, Experimental Brain Research.

[28]  O. Güntürkün,et al.  Natural split-brain? Lateralized memory for task contingencies in pigeons , 2009, Neuroscience Letters.

[29]  O. Güntürkün,et al.  Embryonic light stimulation induces different asymmetries in visuoperceptual and visuomotor pathways of pigeons , 2002, Behavioural Brain Research.

[30]  H. Mouritsen,et al.  Thermal paper can replace typewriter correction paper in Emlen funnels , 2009, Journal of Ornithology.

[31]  T. Ritz,et al.  Magnetoreception in birds: the effect of radio-frequency fields , 2015, Journal of the Royal Society Interface.

[32]  B. Hellmann,et al.  Asymmetries of representation in the visual system of pigeons , 1998, Neuroreport.

[33]  O. Güntürkün,et al.  Visual acuity and hemispheric asymmetries in pigeons , 1994, Behavioural Brain Research.

[34]  N. Troje,et al.  Lateralized activation of Cluster N in the brains of migratory songbirds , 2007, The European journal of neuroscience.

[35]  H. Mouritsen,et al.  Night-Migratory Songbirds Possess a Magnetic Compass in Both Eyes , 2012, PloS one.

[36]  L. Huber,et al.  Lateralized cognition: Asymmetrical and complementary strategies of pigeons during discrimination of the “human concept” , 2007, Cognition.

[37]  L. Peichl,et al.  Magnetoreception: activated cryptochrome 1a concurs with magnetic orientation in birds , 2013, Journal of The Royal Society Interface.

[38]  G. Vallortigara.  The evolutionary psychology of left and right: costs and benefits of lateralization. , 2006, Developmental psychobiology.

[39]  C. Demaine,et al.  Neurophysiological properties of magnetic cells in the pigeon's visual system , 1986, Journal of Comparative Physiology A.

[40]  Harald Luksch,et al.  A Visual Pathway Links Brain Structures Active during Magnetic Compass Orientation in Migratory Birds , 2007, PloS one.

[41]  L. Rogers.  Asymmetry of brain and behavior in animals: Its development, function, and human relevance , 2014, Genesis.

[42]  W. Wiltschko,et al.  Avian magnetic compass: fast adjustment to intensities outside the normal functional window , 2006, Naturwissenschaften.

[43]  O. Güntürkün,et al.  The Neural Basis of Long-Distance Navigation in Birds. , 2016, Annual review of physiology.

[44]  K. Hoffmann,et al.  Magnetoreception of Directional Information in Birds Requires Nondegraded Vision , 2010, Current Biology.

[45]  K. Kavokin,et al.  Magnetic orientation of garden warblers (Sylvia borin) under 1.4 MHz radiofrequency magnetic field , 2014, Journal of The Royal Society Interface.

[46]  O. Güntürkün,et al.  Asymmetric top-down modulation of ascending visual pathways in pigeons , 2016, Neuropsychologia.

[47]  O. Güntürkün,et al.  UK Laterality : Asymmetries of Body , Brain and Cognition , 2012 .

[48]  L. Rogers.  Light input and the reversal of functional lateralization in the chicken brain , 1990, Behavioural Brain Research.

[49]  O. Güntürkün,et al.  Visual asymmetries in Japanese quail (Coturnix japonica) retain a lifelong potential for plasticity. , 2009, Behavioral neuroscience.

[50]  O. Güntürkün,et al.  Limb preferences in non-human vertebrates , 2013, Laterality.

[51]  W. Wiltschko,et al.  Sensing Magnetic Directions in Birds: Radical Pair Processes Involving Cryptochrome , 2014, Biosensors.

[52]  M. Hausmann.  Why sex hormones matter for neuroscience: A very short review on sex, sex hormones, and functional brain asymmetries , 2017, Journal of neuroscience research.

[53]  K. Hugdahl,et al.  How brain asymmetry relates to performance – a large-scale dichotic listening study , 2014, Front. Psychol..

[54]  T. Ritz,et al.  The magnetic compass of domestic chickens, Gallus gallus , 2007, Journal of Experimental Biology.

[55]  O. Güntürkün,et al.  Visual asymmetries and the ascending thalamofugal pathway in pigeons , 2013, Brain Structure and Function.

[56]  Thorsten Ritz,et al.  Magnetic compass orientation of migratory birds in the presence of a 1.315 MHz oscillating field , 2005, Naturwissenschaften.

[57]  O. Güntürkün,et al.  'Natural' and artificial monocular deprivation effects on thalamic soma sizes in pigeons. , 1999, Neuroreport.

[58]  E. Batschelet.  Circular statistics in biology , 1981 .