Navigating Through an Asymmetrical Brain: Lateralisation and Homing in Pigeon

  • Tommaso Pecchia
  • Anna Gagliardo
  • Caterina Filannino
  • Paolo Ioalè
  • Giorgio Vallortigara


The ability of homing pigeons to find their way back home after displacement has fascinated researchers for more than a century. Pigeons rely on a map-and-compass system to navigate, especially when released from an unfamiliar site. Olfactory cues and the sun’s azimuth provide, respectively, primarily a navigational map and compass information to accomplish this task. Magnetic cues provide subsidiary compass information. In addition, pigeons can also rely on a spatial representation of the visual landmarks when navigating over familiar terrains. The neural structures underlying these capabilities have been thoroughly investigated. Taking advantage of the neuroanatomical organisation of the avian brain, several studies have addressed lateralisation (i.e. the functional contribution of the left and the right sides of the brain) of homing behaviour. A survey of the most recent contribution to this topic will be presented, with particular attention to the olfactory system, the visual system and the hippocampus.


Release Site Hippocampal Formation Homing Pigeon Homing Behaviour Homing Performance 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Dorsal arcopallium


Commissura tectalis


Commissura tectalis


Dorsolateral corticoid arena


Decussatio supraoptica dorsalis


Piriform cortex


Prepiriform cortex




Nucleus geniculatus lateralis, pars doralis


Hyperpallium densocellulare


Hippocampal formation


Hyperpallium laterale


Medial striatum


Frontolateral nidopallium


Olfactory bulb


Nucleus rotundus


Medial septum


Tractus septomesencephalicus


Tectum opticum


Nucleus taeniae




  1. Atoij Y, Wild M (2006) Anatomy of the avian hippocampal formation. Rev Neurosci 17:3–15Google Scholar
  2. Benvenuti S, Gagliardo A (1996) Homing behaviour of pigeons subjected to unilateral zinc sulfate treatment of their olfactory mucosa. J Exp Biol 199:2531–2535PubMedGoogle Scholar
  3. Bingman VP, Jones TJ (1994) Hippocampal lesions disrupt sun compass directional learning in homing pigeons. J Neurosci 14:6687–6694PubMedGoogle Scholar
  4. Bingman VP, Mench JA (1990) Homing behaviour of hippocampus and parahipppocampus lesioned pigeons following short-distance releases. Behav Brain Res 40:227–238PubMedGoogle Scholar
  5. Bingman VP, Bagnoli P, Ioalè P, Casini G (1984) Homing behaviour in pigeons after telencephalic ablations. Brain Behav Evol 24:94–106PubMedGoogle Scholar
  6. Bingman VP, Ioalè P, Casini G, Bagnoli P (1987) Impaired retention of preoperatively acquired spatial reference memory in homing pigeons following hippocampal ablation. Behav Brain Res 24:147–156PubMedGoogle Scholar
  7. Bingman VP, Ioalè P, Casini G, Bagnoli P (1988) Hippocampal ablated homing pigeons show a persistent impairment in the time taken to return home. J Comp Physiol A 163:559–563Google Scholar
  8. Bingman VP, Casini G, Nocjar C, Jones TJ (1994) Connections of the piriform cortex in homing pigeons (Columba livia) studied with fast blue and WGA-HRP. Brain Behav Evol 43:206–218PubMedGoogle Scholar
  9. Bingman VP, Gagliardo A, Hough GE, Ioalè P, Kahn MC, Siegel JJ (2005) The avian hippocampus, homing in pigeons and the memory representation of large-scale space. Integr Comp Biol 45:555–564PubMedGoogle Scholar
  10. Bingman VP, Siegel JJ, Gagliardo A, Erichsen JT (2006a) Representing the richness of avian spatial cognition: properties of a lateralized homing pigeon hippocampus. Rev Neurosci 17:17–28PubMedGoogle Scholar
  11. Bingman VP, Erichsen JT, Anderson JD, Good MA, Pearce JM (2006b) Spared feature-structure discrimination but diminished salience of environmental geometry in hippocampal-lesioned homing pigeons (Columba livia). Behav Neurosci 120:835–841PubMedGoogle Scholar
  12. Biro D, Guilford T, Dawkins M (2003) Mechanisms of visually mediated site recognition by the homing pigeon. Anim Behav 65:115–122Google Scholar
  13. Biro D, Meade J, Guilford T (2004) Familiar route loyalty implies visual pilotage in the homing pigeon. Proc Natl Acad Sci USA 101:17440–17443PubMedGoogle Scholar
  14. Bonadonna F, Holland R, Dall’Antonia L, Guilford T, Benvenuti S (2000) Tracking clock-shifted homing pigeons from familiar release sites. J Exp Biol 203:207–212Google Scholar
  15. Braithwaite V, Guilford T (1991) Viewing familiar landscapes affects pigeon homing. Proc Royal Soc Lond B 245:183–186Google Scholar
  16. Burt T, Holland R, Guilford T (1997) Further evidence for visual landmark involvement in the pigeon’s familiar area map. Anim Behav 53:1203–1209PubMedGoogle Scholar
  17. Chappell J, Guilford T (1995) Homing pigeons primarily use the sun compass rather than fixed directional visual cues in an open-field arena food-searching task. Proc Royal Soc Lond B 260:59–63Google Scholar
  18. Chelazzi G, Pardi L (1972) Experiments on the homing behaviour of caged pigeons. Monit Zool Italy 6:63–73Google Scholar
  19. Cheng K, Spetch ML, Kelly DM, Bingman VP (2006) Small-scale spatial cognition in pigeons. Behav Process 72:115–127Google Scholar
  20. Clayton NS, Lee DW (1998) Memory and the hippocampus in food-storing birds. In: Balda RP, Pepperberg IM, Kamil AC (eds) Animal cognition in nature. Academic Press, San DiegoGoogle Scholar
  21. Dennis TE, Rayner MJ, Walker MM (2007) Evidence that pigeons orient to geomagnetic intensity during homing. Proc Royal Soc Lond B 274:1153–1158Google Scholar
  22. Diekamp B, Prior H, Ioalè P, Odetti F, Güntürkün O, Gagliardo A (2002) Effects of monocular viewing on orientation in an arena at the release site and homing performance in pigeons. Behav Brain Res 136:103–111PubMedGoogle Scholar
  23. Fleissner G, Hoòtkamp-Rötzler E, Hanzlik M, Winklhofer M, Fleissner G, Petersen N, Wiltschko W (2003) Magnetoreceptor in the beak of homing pigeons. J Comp Neurol 458:350–360PubMedGoogle Scholar
  24. Foà A, Bagnoli P, Giongo F (1986) Homing pigeons subjected to section of the anterior commissure can build up two olfactory maps in the deflector loft. J Comp Physiol A 159:465–472PubMedGoogle Scholar
  25. Gagliardo A, Mazzotto M, Bingman VP (1996) Hipocampal lesion effects on learning strategies in homing pigeons. Proc Royal Soc Lond B 263:529–534Google Scholar
  26. Gagliardo A, Ioalè P, Bingman VP (1999) Homing in pigeons: the role of the hippocampal formation in the representation of landmarks used for navigation. J Neurosci 19:311–315PubMedGoogle Scholar
  27. Gagliardo A, Ioalè P, Odetti F, Bingman VP (2001a) The ontogeny of the homing pigeon navigational map: evidence for a sensitive learning period. Proc Royal Soc Lond B 268:197–202Google Scholar
  28. Gagliardo A, Ioalè P, Odetti F, Bingman VP, Siegel JJ, Vallortigara G (2001b) Hippocampus and homing in pigeons: left and right hemispheric differences in navigational map learning. Eur J Neurosci 13:1617–1624PubMedGoogle Scholar
  29. Gagliardo A, Ioalè P, Odetti F (2001c) Role of visual cues for orientation at familiar sites by homing pigeons: an experiment in a circular arena. Proc Royal Soc Lond B 268:2065–2070Google Scholar
  30. Gagliardo A, Odetti F, Ioalè P, Bingman VP, Tuttle S, Vallortigara G (2002) Bilateral participation of the hippocampus in familiar landmark navigation by homing pigeons. Behav Brain Res 136:201–209PubMedGoogle Scholar
  31. Gagliardo A, Odetti F, Ioalè P, Pecchia T, Vallortigara G (2005a) Functional asymmetry of left and right avian piriform cortex in homing pigeons’ navigation. Eur J Neurosci 22:189–194PubMedGoogle Scholar
  32. Gagliardo A, Vallortigara G, Nardi D, Bingman VP (2005b) A lateralized avian hippocampus: preferential role of the left hippocampal formation in homing pigeon sun compass-based spatial learning. Eur J Neurosci 22:2549–2559PubMedGoogle Scholar
  33. Gagliardo A, Odetti F, Ioalè P (2005c) Factors reducing the expected deflection in initial orientation in clock-shifted homing pigeons. J Exp Biol 208:469–478PubMedGoogle Scholar
  34. Gagliardo A, Ioalè P, Savini M, Wild JM (2006) Having the nerve to home: trigeminal magnetoreceptor versus olfactory mediation of homing in pigeons. J Exp Biol 209:2888–2892PubMedGoogle Scholar
  35. Gagliardo A, Ioalè P, Savini M, Lipp HP, Dell’Omo G (2007a) Finding home: the final step of the pigeons’ homing process studied with a GPS data logger. J Exp Biol 210:1132–1138PubMedGoogle Scholar
  36. Gagliardo A, Pecchia T, Savini M, Odetti F, Ioalè P, Vallortigara G (2007b) Olfactory lateralization in homing pigeons: initial orientation of birds receiving a unilateral olfactory input. Eur J Neurosci 25:1511–1516PubMedGoogle Scholar
  37. Gagliardo A, Ioalè P, Savini M, Wild M (2008) Navigational abilities of homing pigeons deprived of olfactory or trigeminally mediated magnetic information when young. J Exp Biol 211:2046–2051PubMedGoogle Scholar
  38. Gagliardo A, Ioalè P, Savini M, Wild JM (2009a) Navigational abilities of homing pigeons deprived of olfactory or trigeminally mediated magnetic information. J Exp Biol 212:3119–3124PubMedGoogle Scholar
  39. Gagliardo A, Ioalè P, Savini M, Dell’Omo G, Bingman VP (2009b) Hippocampal-dependent familiar area map supports corrective re-orientation following navigational error during pigeon homing: a GPS-tracking study. Eur J Neurosci 29:2389–2400PubMedGoogle Scholar
  40. Gagliardo A, Filannino C, Ioalè P, Pecchia T, Wikelski M, Vallortigara G (2011a) Olfactory lateralization in homing pigeons: a GPS study on birds released with unilateral olfactory inputs. J Exp Biol 214:593–598PubMedGoogle Scholar
  41. Gagliardo A, Ioalè P, Filannino C, Wikelski M (2011b) Homing pigeons only navigate in air with intact environmental odours: a test of the olfactory activation hypothesis with GPS data loggers. PLoS ONE 6(8):e22385PubMedGoogle Scholar
  42. Griffin DR (1952) Bird navigation. Biol Rev Camb Philos Soc 27:359–400Google Scholar
  43. Güntürkün O (1997) Avian visual lateralization: a review. NeuroReport 8:3–11Google Scholar
  44. Hein CM, Engels S, Kishkinev D, Mouritsen H (2011) Robins have a magnetic compass in both eyes. Nature 471:E11–E12PubMedGoogle Scholar
  45. Holland RS (2003) The role of visual landmarks in the avian familiar area map. J Exp Biol 206:1773–1778PubMedGoogle Scholar
  46. Holland RA, Bonadona F, Dall’Antonia L, Benvenuti S, Burt de Perera T, Guilford TC (2000) Short distance phase shifts revisited: tracking clock-shifted homing pigeons (Rock dove Columba livia) close to the loft. Ibis 142:111–118Google Scholar
  47. Hough GE, Bingman VP (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 190:1047–1062Google Scholar
  48. Ioalè P, Gagliardo A, Bingman VP (2000) Hippocampal participation in navigational map learning in young homing pigeons is dependent on training experience. Eur J Neurosci 12:1–9Google Scholar
  49. Kahn M, Bingman VP (2004) Lateralization of spatial learning in the avian hippocampal formation. Behav Neurosci 118:333–344PubMedGoogle Scholar
  50. Keeton WT (1971) Magnets interfere with pigeon homing. Proc Natl Acad Sci USA 68:102–106PubMedGoogle Scholar
  51. Kelly DM, Kippenbrock S, Templeton J, Kamil AC (2008) Use of a geometric rule or absolute vectors: landmark use by Clark’s nutcrackers (Nucifraga columbiana). Brain Res Bull 76:293–299PubMedGoogle Scholar
  52. Kelly DM, Chiandetti C, Vallortigara G (2011) Re-orienting in space: do animals use global or local geometry strategies? Biol Lett 7:372–375PubMedGoogle Scholar
  53. Kramer G (1950) Weitere Analyse der Faktoren, welche die Zugaktivität des gekäfigten Vogels orientieren. Naturwissenschaften 37:377–378Google Scholar
  54. Kramer G (1953) Wird die Sonnenhöhe bei der Heimfindeorientierung verwertet? J Ornithol 94:201–219Google Scholar
  55. Mazzotto M, Nacci L, Gagliardo A (1999) Homeward orientation of pigeons confined in a circular arena. Behav Process 46:217–225Google Scholar
  56. Meade J, Biro D, Guilford T (2005) Homing pigeons develop local route stereotypy. Proc Royal Soc Lond B 272:17–23Google Scholar
  57. Meade J, Biro D, Guilford T (2006) Route recognition in the homing pigeon, Columba livia. Anim Behav 72:975–980Google Scholar
  58. Mehlhorn J, Haastert B, Rehkämper G (2010) Asymmetry of different brain structures in homing pigeons with and without navigational experience. J Exp Biol 213:2219–2224PubMedGoogle Scholar
  59. Mora CV, Walker M (2009) Do release-site biases reflect response to the earth’s magnetic field during position determination by homing pigeons? Proc Royal Soc Lond B 276:3295–3302Google Scholar
  60. Mora CV, Davison M, Wild JM, Walker MN (2004) Magnetoreception and its trigeminal mediation in the homing pigeon. Nature 432:508–511PubMedGoogle Scholar
  61. Mouritsen H, Janssen-Bienhold U, Liedvogel M, Feenders G, Staillecken J, Dirks P, Weiler R (2004) Cryptochromes and activity markers co-localize in bird retina during magnetic orientation. Proc Natl Acad Sci U S A 101:14294–14299PubMedGoogle Scholar
  62. Nardi D, Bingman VP (2007) Asymmetrical participation of the left and right hippocampus for representing environmental geometry in homing pigeons. Behav Brain Res 178:160–171PubMedGoogle Scholar
  63. Odetti F, Ioalè P, Gagliardo A (2003) Development of the navigational map in homing pigeons: effects of flight experience on orientation performance. Anim Behav 66:1093–1099Google Scholar
  64. O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Oxford University Press, OxfordGoogle Scholar
  65. Papi F, Fiore L, Fiaschi V, Benvenuti S (1972) Olfaction and homing in pigeons. Monitore zool ital (N S) 6:85–95Google Scholar
  66. Patzke N, Manns M, Güntürkün O, Ioalè P, Gagliardo A (2010) Navigation-induced ZENK expression in the olfactory system of pigeons (Columba livia). Eur J Neurosci 31:2062–2072PubMedGoogle Scholar
  67. Patzke N, Manns M, Güntürkün O (2011) Telencephalic organisation of the olfactory system in homing pigeons (Columba livia). J Neurosci 194:53–56Google Scholar
  68. Prior H (2006) Lateralization of spatial orientation in birds. In: Malashichev Y, Deckel AW (eds) Behavioral and morphological asymmetries in vertebrates. Landes Bioscience, AustinGoogle Scholar
  69. Prior H, Güntürkün O (2001) Parallel working memory for spatial location and food-related object-cues in foraging pigeons: binocular and lateralized monocular performance. Learn Mem 8:44–51PubMedGoogle Scholar
  70. Prior H, Lingenauber F, Nitschke J, Güntürkün O (2002) Orientation and lateralized cue use in pigeons navigating a large indoor environment. J Exp Biol 205:1795–1805PubMedGoogle Scholar
  71. Prior H, Wiltschko R, Stapput K, Güntürkün O, Wiltschko W (2004) Visual lateralization and homing in pigeons. Behav Brain Res 154:301–310PubMedGoogle Scholar
  72. Rashid N, Andrew RJ (1989) Right hemisphere advantage for topographical orientation in the domestic chick. Neuropsychologia 27:937–948PubMedGoogle Scholar
  73. Reiner A, Karten HJ (1985) Comparison of olfactory bulb projections in pigeons and turtles. Brain Behav Evol 27:11–27PubMedGoogle Scholar
  74. Reiner A, Perkel DJ, Bruce LL, Butler AB, Csillag A, Kuenzel W, Medina L et al (2004) Revised nomenclature for avian telencephalon and some related brainstem nuclei. J Comp Neurol 473:377–414PubMedGoogle Scholar
  75. Rieke GK, Wenzel BM (1975) The ipsilateral olfactory projection field in the pigeon. In: Denton VD, Coghlan JP (eds) Olfaction and taste. Academic Press, New YorkGoogle Scholar
  76. Rieke GK, Wenzel BM (1978) Forebrain projections of the pigeon olfactory bulb. J Morphol 158:41–55PubMedGoogle Scholar
  77. Ritz T, Adem S, Schulten K (2000) A model for photoreceptor-based magnetoreception in birds. Biophys J 78:707–718PubMedGoogle Scholar
  78. Rogers LJ, Andrew RJ (2002) Comparative vertebrate lateralizaton. Cambridge University Press, CambridgeGoogle Scholar
  79. Schlund W (1992) Intra-nasal zinc sulphate irrigation in pigeons: effects on olfactory capabilities and homing. J Exp Biol 164:171–187Google Scholar
  80. Schlund W, Schmid J (1991) Auswirkungen von ZnSO4 auf die olfaktorische Wahrnehmung, die Anfangsorientierung und den Heimkehrerfolg von Brieftauben (Columba livia). Verh dt Zool Ges 84:360Google Scholar
  81. Schmid J, Schlund W (1993) Anosmia in ZnSO4 treated pigeons: loss of olfactory information during ontogeny and the role of site familiarity in homing experiments. J Exp Biol 185:3–49Google Scholar
  82. Shimizu T, Bowers AN, Budzynski C, Kahn MC, Bingman VP (2004) What does a pigeon brain look like during homing? Selective examination of ZENK expression in the telencephalon of pigeons navigating home. Behav Neurosci 118:845–851PubMedGoogle Scholar
  83. Siegel JJ, Nitz D, Bingman VP (2005) Spatial-specificity of single-units in the hippocampal formation of freely moving homing pigeons. Hippocampus 15:26–40PubMedGoogle Scholar
  84. Siegel JJ, Nitz D, Bingman VP (2006) Lateralized functional components of spatial cognition in the avian hippocampal formation: evidence from single-unit recordings in freely moving homing pigeons. Hippocampus 16:125–140PubMedGoogle Scholar
  85. Tommasi L, Vallortigara G (2001) Encoding of geometric and landmark information in the left and right hemispheres of the avian brain. Behav Neurosci 115:602–613PubMedGoogle Scholar
  86. Tommasi L, Andrew RJ, Vallortigara G (2000) Eye use in search is determined by the nature of task in the domestic chick (Gallus gallus). Behav Brain Res 112:119–126PubMedGoogle Scholar
  87. Tommasi L, Gagliardo A, Andrew RJ, Vallortigara G (2003) Separate processing mechanisms for encoding geometric and landmark information in the avian hippocampus. Eur J Neurosci 17:1695–1702PubMedGoogle Scholar
  88. Treiber CD, Salzer MC, Riegler J, Edelman N, Sugar C, Breuss M, Pichler P, Cadiou H, Saunders M, Lythgoe M, Shaw J, Keays DA (2012) Clusters of iron-rich cells in the upper beak of pigeons are macrophages not magnetosensitive neurons. Nature 484:367–370Google Scholar
  89. Ülrich C, Prior H, Duka T, Leshchins’ka I, Valenti P, Güntürkün O, Lipp HP (1999) Left-hemispheric superiority for visuospatial orientation in homing pigeons. Behav Brain Res 104:169–178PubMedGoogle Scholar
  90. Valencia-Alfonso CE, Verhaal J, Güntürkün O (2009) Ascending and descending mechanisms of visual lateralization in pigeons. Phil Trans Royal Soc B 364:955–963Google Scholar
  91. Vallortigara G, Pagni P, Sovrano VA (2004) Separate geometric and non-geometric modules for spatial reorientation: evidence from a lopsided animal brain. J Cognitive Neurosci 16:390–400Google Scholar
  92. Vargas JP, Petruso EJ, Bingman VP (2004) Hippocampal formation is required for geometric navigation in pigeons. Eur J Neurosci 20:1937–1944PubMedGoogle Scholar
  93. Von Hünerbein K, Hamann HJ, Ruter E, Wiltschko W (2000) A GPS-based system for recording the flight paths of birds. Naturwissenschaften 87:278–279Google Scholar
  94. Walcott C (1978) Anomalies in the earth’s magnetic field increase the scatter of pigeon’s vanishing bearings. In: Schmidt-Koenig K, Keeton WT (eds) Animal migration, navigation and homing. Springer, HeidelbergGoogle Scholar
  95. Walcott C (1991) Magnetic maps in pigeons. In: Berthold P (ed) Orientation in birds. Birkhauser, BostonGoogle Scholar
  96. Walker MM (1999) Magnetic position determination by homing pigeons. J Theor Biol 197:271–276PubMedGoogle Scholar
  97. Wallraff HG (1966) Über die Hebimfindeleistungen von Brieftauben nach Haltung in vershiedenartig abgeshiermten Volieren. Z Vergl Physiol 52:215–259Google Scholar
  98. Wallraff HG (1970) Weitere Volierenversuche mit Brieftauben: wahrscheinlicher einflussdynamischer Faktoren der Atmosphäre auf die Orientierung. Z Vergl Physiol 68:182–201Google Scholar
  99. Wallraff HG (1979) Goal-oriented and compass-oriented movements of displaced homing pigeons after confinement in differentially shielded aviaries. Behav Ecol Sociobiol 5:201–225Google Scholar
  100. Wallraff HG (2000) Simulated navigation based on observed gradients of atmospheric trace gases (models on pigeon homing, part 3). J Theor Biol 205:133–145PubMedGoogle Scholar
  101. Wallraff HG (2004) Avian olfactory navigation: its empirical foundation and conceptual state. Anim Behav 67:189–204Google Scholar
  102. Wallraff HG (2005) Avian navigation: pigeon homing as a paradigm. Springer, BerlinGoogle Scholar
  103. Wikelski M, Kays RW, Kasdin NJ, Thorup K, Smith JA, Swenson GW (2011) Going wild: what a global small-animal tracking system could do for experimental biologists. J Exp Biol 210:181–186Google Scholar
  104. Wiltschko R, Wiltschko W (1995) Magnetic orientation in animals. Springer, BerlinGoogle Scholar
  105. Wiltschko W, Wiltschko R (2005) Magnetic orientation and magnetoreception in birds and other animals. J Comp Physiol A 191:675–693Google Scholar
  106. Wiltschko W, Traudt J, Güntürkün O, Prior H, Wiltschko R (2002) Lateralization of magnetic compass orientation in a migratory bird. Nature 419:467–470PubMedGoogle Scholar
  107. Wilzeck C, Prior H, Kelly DM (2009) Geometry and landmark representation by pigeons: evidence for species-differences in the hemispheric organization of spatial information processing? Eur J Neurosci 29:813–822PubMedGoogle Scholar
  108. Wilzeck C, Wiltschko W, Güntürkün O, Wiltschko R, Prior H (2010) Lateralization of magnetic compass orientation in pigeons. J Royal Soc Interface 7:S235–S240Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Tommaso Pecchia
    • 1
  • Anna Gagliardo
    • 2
  • Caterina Filannino
    • 2
  • Paolo Ioalè
    • 2
  • Giorgio Vallortigara
    • 1
  1. 1.Center for Mind/Brain Sciences (CIMeC)University of TrentoRoveretoItaly
  2. 2.Department of BiologyUniversity of PisaPisaItaly

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