Asymmetry of different brain structures in homing pigeons with and without navigational experience

Journal of Experimental Biology

Volumn 213, Issue 13, 2010, Pages 2219-2224

  Mehlhorn, Julia ^a   Haastert, Burkhard ^b   Rehkämper, Gerd ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b MediStatistica Neuenrade ^*  (Germany)

Author keywords

Asymmetry; Brain; Homing pigeon; Lateralisation; Mosaic evolution; Navigation

Indexed keywords

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; BRAIN; FEMALE; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; MALE; PIGEONS AND DOVES; ANATOMY AND HISTOLOGY;

ANIMALS; BRAIN; COLUMBIDAE; FEMALE; HOMING BEHAVIOR; MALE;

ANIMALIA; AVES; COLUMBA; COLUMBA LIVIA;

EID: 77953605638     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.043208     Document Type: Article

References (85)

1. Andrew, R. J., Osorio, D. and Budaev, S. (2009). Light during embryonic development modulates patterns of lateralization strongly and similarly in both zebrafish and chick. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 364, 983-989.
2. Barton, R. A. and Harvey, P. (2000). Mosaic evolution of brain structure in mammals. Nature 405, 1055-1058.
3. Bingman, V. P. (1993). Vision, cognition and the avian hippocampus. In Vision, Brain and Behaviour in Birds (ed. H. P. Zeigler and H. J. Bischof), pp. 391-408. Cambridge: MIT Press
4. Bingman, V. P., Hough, G. E., II, Kahn, M. C. and Siegel, J. J. (2003). The homing pigeon hippocampus and space: in search of adaptive specialization. Brain Behav. Evol. 62, 117-127.
5. Bingman, V. P., Gagliardo, A., Hough, G. E., Ioalè, P., Kahn, M. C. and Siegel, J. J. (2005). The avian hippocampus, homing in pigeons and the memory representation of large scale-space, Integr. Comp. Biol. 45, 555-564. (Pubitemid 41040151)
6. Broca, P. (1865). Sur la siége de la faculté de langage articulé. Bulletins de la Société d'Anthropologie 6, 377-393.
7. Charvet, C. J. and Striedter, G. F. (2009). Developmental origins of mosaic brain evolution: morphometric analysis of the developing zebra finch brain. J. Comp. Neurol. 514, 203-213.
8. Clark, D. A., Mitra, P. P. and Wang, S. S. H. (2001). Scalable architecture in mammalian brains. Nature 411, 189-193.
9. Clayton, N. S. (1996). Development of food-storing and the hippocampus in juvenile marsh tits (Parus palustris). Behav. Brain Res. 74, 153-159.
10. Clayton, N. S. and Krebs, J. R. (1994a). Memory for spatial and object-specific cues in food-storing and non-storing birds. J. Comp. Physiol. A 174, 371-379.
11. Clayton, N. S. and Krebs, J. R. (1994b). Hippocampal growth and attrition in birds affected by experience. Proc. Nail. Acad. Sci. USA 91, 7410-7414.
12. Cnotka, J., Möhle, M. and Rehkämper, G. (2008). Navigational experience affects hippocampal size in homing pigeons. Brain Behav. Evol. 72, 179-250.
13. Della Chiesa, A., Pecchia, T., Tommasi, L. and Vallortigara, G. (2006). Multiple landmarks, the encoding of environmental geometry and the spatial logics of a dual brain. Anim. Cogn. 9, 281-293.
14. Edelmann, G. M. (1993). Neural Darwinism-selection and re-entrant signalling in higher brain-function. Neuron 10, 115-125.
15. Finlay, B. L. and Darlington, R. B. (1995). Linked regularities in the development and evolution of mammalian brains. Science 268, 1578-1584.
16. Floody, O. R. and Arnold, A. P. (1997). Song lateralization in the zebra finch. Horm. Behav. 31, 25-34.
17. Gagliardo, A., Ioalè, P., Odetti, F., Bingman, V. P., Siegel, J. J. and Vallortigara, G (2001). Hippocampus and homing in pigeons: left and right hemispheric differences in navigational map learning. Eur. J. Neurosci. 13, 1617-1624. (Pubitemid 32423347)
18. Gagliardo, A., Odetti, F., Ioalè, P., Bingman, V. P., Tuttle, S. and Vallortigara, G. (2002). Bilateral participation of the hippocampus in familiar landmark navigation by homing pigeons. Behav. Brain Res. 136, 201-209. (Pubitemid 35246405)
19. Gagliardo, A., Vallortigara, G., Nardi, D. and Bingman, V. P. (2005). A lateralized avian hippocampus: preferential role of the left hippocampal formation in homing pigeon sun compass-based learning. Eur. J. Neurosci. 22, 2549-2559. (Pubitemid 41758997)
20. Gallyas, F. (1971). A principle of silver staining of tissue elements by means of physical development. Acta Morphol. Acad. Sci. Hung. 19, 57-71.
21. Geschwind, N. and Galaburda, A. M. (1985). Cerebral lateralization- biological mechanisms, associations, and pathology. 1. A hypothesis and a program for research. Arch. Neurol. 42, 428-459. (Pubitemid 15113010)
22. Ghirlanda, S. and Vallortigara, G. (2009). The evolution of brain lateralization: a game-theoretical analysis of population structure. Proc. R. Soc. Lond. B. Biol. Sci. 271, 853-857. (Pubitemid 38491273)
23. Güntürkün, O. (1991). The functional organization of the avian visual system. In Neural and Behavioural Plasticity (ed. R. J. Andrew). Oxford: Oxford University Press.
24. Güntürkün, O. (1997). Morphological asymmetries of the tectum opticum in the pigeon. Exp. Brain Res. 116, 561-566.
25. Güntürkün, O. (2005). The avian 'prefrontal cortex' and cognition. Curr. Opin. Neurobiol. 15, 686-693.
26. Haase, E., Otto, C. and Murbach, H. (1977). Brain weight in homing and non-homing pigeons. Experientia 33, 606. (Pubitemid 8088513)
27. Halpern, M. E., Güntürkün, O., Hopkins, W. D. and Rogers, L. J. (2005). Lateralization of the vertebrate brain: taking the side of model systems. J. Neurosci. 25, 10351-10357. (Pubitemid 41628436)
28. Healy, S. D., Gwinner, E. and Krebs, J. R. (1996). Hippocampal volume in migratory and non-migratory warblers: effects of age and experience. Behav. Brain. Res. 81, 61-68. (Pubitemid 26384964)
29. Hough, G. E. and Bingman, V. P. (2004). Spatial response properties of homing pigeon hippocampal neurons: correlations with goal locations, movement between goals, and environmental context in a radial-arm arena. J. Comp. Physiol. A 190, 1047-1062.
30. Hough, G. E. and Bingman, V. P. (2008). Rotation of visual landmark cues influences the spatial response profile of hippocampal neurons in freely-moving homing pigeons. Behav. Brain Res. 187, 473-477.
31. Howard, K. J., Rogers, L. J. and Boura, A. L. A. (1980). Functional lateralization of the chicken forebrain revealed by use of intracranial glutamate. Brain Res. 188, 369-382.
32. Iwaniuk, A. N. and Hurd, P. L. (2005). The evolution of cerebrotypes in birds. Brain Behav. Evol. 65, 215-230.
33. Iwaniuk, A. N., Dean, K. M. and Nelson, J. E. (2004). A mosaic pattern characterizes the evolution of the avian brain. Proc. R. Soc. Lond. B. Biol. Sci. 271, S148-S151.
34. Kahn, M. C. and Bingman, V. (2004). Lateralization of spatial learning in the avian hippocampal formation. Behav. Neurosci. 118, 333-344.
35. Karten, H. J. (1979). Visual lemniscal pathways in birds. In Neural Mechanisms of Behaviour in the Pigeon (ed. A. M. Granda and J. M. Maxwell), pp. 409-430. New York: Plenum Press.
36. Koshiba, M., Nakamura, S., Deng, C. and Rogers, L. J. (2003). Light-dependent development of asymmetry in the ipsilateral and contralateral thalamofugal visual projections of the chick. Neurosci. Lett. 336, 81-84. (Pubitemid 36009312)
37. Lefebvre, L., Reader, S. M. and Sol, D. (2004). Brains, innovation and evolution in birds and primates. Brain Behav. Evol. 63, 233-246. (Pubitemid 38490190)
38. Lipp, H. P. (1983). Nocturnal homing in pigeons. Comp. Biochem. Physiol. A 76, 743-749.
39. Lipp, H. P. (1996). 'Columba militaris helvetica'. Biologie und Verhaltensleistungen der Schweizer Armeebrieftauben. In Beiträge zur Biologie der Haus- und Nutztiere (ed. G. Rehkämper and H. Greven), pp. 85-103. Düsseldorf: Acta Biol Benrodis.
40. MacNeilage, P. F., Rogers, L. J. and Vallortigara, G. (2009). Origins of the left and right brain. Sci. Am. 301, 60-67.
41. Mayr, E. (1963). Animal Species and Evolution. Cambridge: Belknap Press, Harvard, University Press.
42. Mehlhorn, J. and Rehkämper, G. (2009). Neurobiology of the homing pigeon - a review. Naturwissenschaften 96, 1011-1025.
43. Nardi, D. and Bingman, V. P. (2007). Asymmetrical participation of the left and right hippocampus for representing environmental geometry in homing pigeons. Behav. Brain Res. 178, 160-171. (Pubitemid 46240348)
44. Nieuwenhuys, R., ten Donkelaar, H. J. and Nicholson, C. (1998). The Central Nervous System of Vertebrates. Berlin: Springer Verlag.
45. Nottebohm, F. (1970). Ontogeny of bird song. Science 167, 950-956.
46. Papi, F., Ioalè, P., Fiaschi, V., Benvenuti, S. and Baldaccini, N. E. (1974). Olfactory navigation of pigeons: the effect of treatment with odorous air currents. J. Comp. Physiol. A94, 187-193.
47. Pfannkuche, K. A., Bouma, A. and Groothuis, A. A. G. (2009). Does testosterone affect lateralization of brain and behaviour? A meta-analysis in humans and other animal species. Phil. Trans. R. Soc. B Biol. Sci. 364, 929-943.
48. Poirier, C., Boumans, T., Verhoye, M., Balthazart, J. and Van der Linden, A. (2009). Own-song recognition in the songbird auditory pathway: selectivity and lateralization. J. Neurosci. 18, 2252-2258.
49. Prior, H., Lingenauber, F., Nitschke, J. and Güntürkün, O. (2002). Orientation and lateralized cue use in pigeons navigating a large indoor environment. J. Exp. Biol. 205, 1795-1805. (Pubitemid 34853752)
50. Prior, H., Wiltschko, R., Stapput, K., Güntürkün, O. and Wiltschko, W. (2004). Visual lateralization and homing in pigeons. Behav. Brain Res. 154, 301-310.
51. Rashid, N. and Andrew, R. J. (1989). Right hemisphere advantage for topographical orientation in the domestic chick. Neuropsychologia 27, 937-948. (Pubitemid 19206924)
52. Rehkämper, G., and Zilles, K. (1991). Parallel evolution in mammalian and avian brains: cytoarchitectonical and cytochemical analysis. Cell Tissue Res. 263, 3-28.
53. Rehkämper, G., Haase, E. and Frahm, H. D. (1988). Allometric comparison of brain weight and brain structure volumes in different breeds of the domestic pigeon, Columba livia f.d. (Fantails, Homing Pigeons, Strasser). Brain Behav. Evol. 31, 141-149. (Pubitemid 18094747)
54. Rehkämper, G., Frahm, H. D. and Mann, M. D. (2001). Evolutionary constraints of large telencephala. In Brain Evolution and Cognition (ed. G. Roth and M. F. Wullimann), pp. 265-293. New York: Wiley.
55. Rehkämper, G., Frahm, H. D. and Cnotka, J. (2008). Mosaic evolution and adaptive brain component alteration under domestication seen on the background of evolutionary theory. Brain Behav. Evol. 71, 115-126. (Pubitemid 351281707)
56. Reiner, A., Perkel, D. J., Bruce, L. L., Butler, A. B. Csillag, A., Kuenzel, W., Medina, L., Paxinos, G., Shimizu, T., Striedter, G. et al. (2004). Revised nomenclature for avian telencephalon and some related brainstem nuclei. J. Comp. Neurol. 473, 377-414. (Pubitemid 38580457)
57. Rice, S. H. (2004). Evolutionary Theory. Sunderland: Sinauer.
58. Rogers, L. J. (1982). Light experience and asymmetry of brain function in chickens. Nature 297, 223-225.
59. Rogers, L. J. (1990). Light input and the reversal of functional lateralisation in the chicken brain. Behav. Brain Res. 38, 211-221.
60. Rogers, L. (1996). Behavioral, structural and neurochemical asymmetries in the avian brain: a model system for studying visual development and processing. Neurosci. Biobehav. Rev. 20, 487-503.
61. Rogers, L. J. (2000). Evolution of hemispheric specialization: advantages and disadvantages. Brain Lang. 73, 236-253.
62. Rogers, L. J. (2009). Hand and paw preferences in relation to the lateralized brain. Philos. Trans. R. Soc. B. Biol. Sci. 364, 943-954.
63. Rogers, L. and Anson, J. M. (1979). Lateralisation of function in the chicken forebrain. Pharmacol. Biochem. Behav. 10, 679-686.
64. Rogers, L. J. and Deng, C. (1999). Light experience and lateralization of the two visual pathways in the chick. Behav. Brain Res. 98, 277-287.
65. Romeis, B. (1989). Mikroskopische Technik. München: Urban und Schwarzenberg.
66. Schaafsma, S. M., Riedstra, B. J., Pfannkuche, K. A., Bouma, A. and Groothuis, T. G. G. (2009). Epigenesis of behavioural lateralization in humans and other animals. Philos. Trans. R. Soc. B. Biol. Sci. 364, 915-927.
67. Schmidt-König, K. (1990). The sun compass. Experientia 46, 336-342.
68. Shimizu, T. and Bowers, A. N. (1999). Visual circuits of the avian telencephalon: evolutionary implications. Behav. Brain Res. 98, 183-191. (Pubitemid 29084441)
69. Siegel, J. J., Nitz, D. and Bingman, V. P. (2006). Lateralized functional components of spatial cognition in the avian hippocampal formation: evidence from single-unit recordings in freely moving homing pigeons. Hippocampus 16, 125-140.
70. Skiba, M., Diekamp, B. and Güntürkün, O. (2002). Embryonic light stimulation induces different asymmetries in visuoperceptual and visuomotor pathways of pigeons. Behav. Brain Res. 134, 149-156. (Pubitemid 34912694)
71. Stephan, H., Frahm, H. D. and Baron, G. (1981). New and revised data on volumes of brain structures in insectivores and primates. Folia Primatol. 35, 1-29.
72. Tommasi, L. (2009). Mechanisms and functions of brain and behavioural asymmetries. Phil. Trans. R. Soc. B. Biol. Sci. 364, 855-859.
73. Tommasi, L. and Vallortigara, G. (2001). Encoding of geometric and landmark information in the left and right hemisphere of the avian brain. Behav. Neurosci. 115, 602-613. (Pubitemid 32565664)
74. Tommasi, L. and Vallortigara, G. (2004). Hemispheric processing of landmark and geometric information in male and female domestic chicks (Gallus gallus). Behav. Brain Res. 155, 85-96. (Pubitemid 39119969)
75. Ulrich, C., Prior, H., Duka, T., Leshchins'ka, I., Valenti, P., Güntürkün, O. and Lipp, H. P. (1999). Left-hemispheric superiority for visuospatial orientation in homing pigeons. Behav. Brain Res. 104, 169-178.
76. Valencia-Alfonso, C. E., Verhaal, J. and Güntürkün, O. (2009). Ascending and descending mechanisms of visual lateralization in pigeons. Phil. Trans. R. Soc. B. Biol. Sci. 364, 955-963.
77. Vallortigara, G. and Rogers, L. J. (2005). Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization. Behav. Brain Sci. 28, 575-633.
78. Vallortigara, G., Regolin, L., Bortolomiol, G. and Tommasi, L. (1996). Lateral asymmetries due to preferences in eye use during visual discrimination learning in chicks. Behav. Brain Res. 74, 135-143. (Pubitemid 26060029)
79. Vallortigara, G., Rogers, L. J. and Bisazza, A. (1999). Possible evolutionary origins of cognitive brain lateralization. Brain Res. Rev. 30, 164-175. (Pubitemid 29440939)
80. Vincent, T. L. and Brown, J. S. (2005). Evolutionary Game Theory, Natural Selection and Darwinian Dynamics. Cambridge: Cambridge University Press.
81. Visalberghi, E. and Al leva, E. (1975). Magnetic influences on pigeon homing. Biol. Bull. 125, 246-256.
82. Walcott, C. (2005). Multi-modal orientation cues in homing pigeons. Integr. Comp. Biol. 45, 574-581.
83. Wallraff, H. G. (2001). Navigation by homing pigeons: updated perspective. Ethol. Ecol. Evol. 13, 1-48.
84. Wallraff, H. G. (2005). Avian Navigation: Pigeon Homing as a Paradigm. Berlin: Springer.
85. Williams, H., Crane, L. A., Hale, T. K., Esposito, M. A. and Nottebohm, F. (1992). Right-side dominance for song control in the zebra finch. J. Neurobiol. 23, 1006-1020.