1932

Abstract

Migratory birds can navigate over tens of thousands of kilometers with an accuracy unobtainable for human navigators. To do so, they use their brains. In this review, we address how birds sense navigation- and orientation-relevant cues and where in their brains each individual cue is processed. When little is currently known, we make educated predictions as to which brain regions could be involved. We ask where and how multisensory navigational information is integrated and suggest that the hippocampus could interact with structures that represent maps and compass information to compute and constantly control navigational goals and directions. We also suggest that the caudolateral nidopallium could be involved in weighing conflicting pieces of information against each other, making decisions, and helping the animal respond to unexpected situations. Considering the gaps in current knowledge, some of our suggestions may be wrong. However, our main aim is to stimulate further research in this fascinating field.

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2016-02-10
2024-04-18
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Literature Cited

  1. Frost B, Mouritsen H. 1.  2006. The neural mechanisms of long distance animal navigation. Curr. Opin. Neurobiol. 16:481–88 [Google Scholar]
  2. Perdeck AC. 2.  1958. Two types of orientation in migrating Sturnus vulgaris and Fringilla coelebs as revealed by displacement experiments. Ardea 46:1–37 [Google Scholar]
  3. Berthold P. 3.  1991. Spatiotemporal programmes and genetics of orientation. Orientation in Birds P Berthold 86–105 Basel, Switz.: Birkhäuser [Google Scholar]
  4. Mouritsen H, Larsen ON. 4.  1998. Migrating young pied flycatchers Ficedula hypoleuca do not compensate for geographical displacements. J. Exp. Biol. 201:2927–34 [Google Scholar]
  5. Mouritsen H, Mouritsen O. 5.  2000. A mathematical expectation model for bird navigation based on the clock-and-compass strategy. J. Theor. Biol. 207:283–91 [Google Scholar]
  6. Mouritsen H. 6.  2003. Spatiotemporal orientation strategies of long-distance migrants. Avian Migration P Berthold, E Gwinner, E Sonnenschein 493–513 Berlin: Springer [Google Scholar]
  7. Holland RA. 7.  2014. True navigation in birds: from quantum physics to global migration. J. Zool. 293:1–15 [Google Scholar]
  8. Mouritsen H. 8.  2001. Navigation in birds and other animals. J. Image Vis. Comput. 19:713–31 [Google Scholar]
  9. Berthold P. 9.  1999. A comprehensive theory for the evolution, control and adaptability of avian migration. Ostrich 70:1–11 [Google Scholar]
  10. Gwinner E. 10.  1996. Circadian and circannual programmes in avian migration. J. Exp. Biol. 199:39–48 [Google Scholar]
  11. Schmidt-König K. 11.  1960. Sun azimuth compass: one factor in the orientation of homing pigeons. Science 131:826–28 [Google Scholar]
  12. Wiltschko R, Wiltschko W. 12.  1990. The development of sun compass orientation in young homing pigeons. J. Ornithol. 131:1–19 [Google Scholar]
  13. Emlen ST. 13.  1970. Celestial rotation: its importance in the development of migratory orientation. Science 170:1198–201 [Google Scholar]
  14. Emlen ST. 14.  1975. The stellar-orientation system of a migratory bird. Sci. Am. 233:102–11 [Google Scholar]
  15. Merkel FW, Wiltschko W. 15.  1965. Magnetismus und Richtungsfinden zugunruhiger Rotkehlchen. Vogelwarte 23:71–77 [Google Scholar]
  16. Wiltschko W, Wiltschko R. 16.  1972. Magnetic compass of European robins. Science 176:62–64The classic paper showing that birds have a magnetic inclination compass. [Google Scholar]
  17. Cochran WW, Mouritsen H, Wikelski M. 17.  2004. Migrating songbirds recalibrate their magnetic compass daily from twilight cues. Science 304:405–8 [Google Scholar]
  18. Mouritsen H. 18.  1998. Redstarts, Phoenicurus phoenicurus, can orient in a true-zero magnetic field. Anim. Behav 55:1311–24 [Google Scholar]
  19. Gwinner E, Schwabl-Benzinger I, Schabl H, Dittami J. 19.  1993. Twenty-four hour melatonin profiles in a nocturnally migrating bird during and between migratory seasons. Gen. Comp. Endocrinol. 90:119–24 [Google Scholar]
  20. Cassone VM. 20.  2014. Avian circadian organization: a chorus of clocks. Front. Neuroendocrinol. 35:76–88 [Google Scholar]
  21. Bell-Pedersen D, Cassone VM, Earnest DJ, Golden SS, Hardin PE. 21.  et al. 2005. Circadian rhythms from multiple oscillators: lessons from diverse organisms. Nat. Rev. Genet. 6:544–56 [Google Scholar]
  22. Brandstätter R, Abraham U. 22.  2003. Hypothalamic circadian organization in birds. I. Anatomy, functional morphology, and terminology of the suprachiasmatic region. Chronobiol. Int. 20:637–55 [Google Scholar]
  23. Norgren R, Silver R. 23.  1989. Retinohypothalamic projections and the suprachiasmatic nucleus in birds. Brain Behav. Evol. 34:73–83 [Google Scholar]
  24. Cassone VM, Brooks DS. 24.  1991. The sites of melatonin action in the brain of the house sparrow, Passer domesticus. J. Exp. Zool 260:302–9 [Google Scholar]
  25. Ebihara S, Kawamura H. 25.  1981. The role of the pineal organ and the suprachiasmatic nucleus in the control of circadian locomotor rhythms in the Java sparrow, Padda oryzivora. J. Comp. Physiol. A 141:207–14 [Google Scholar]
  26. Simpson SM, Follett BK. 26.  1981. Pineal and hypothalamic pacemakers: their role in regulating circadian rhythmicity in Japanese quail. J. Comp. Physiol. A 144:381–89 [Google Scholar]
  27. Takahashi J, Menaker M. 27.  1982. Role of the suprachiasmatic nuclei in the circadian system of the house sparrow, Passer domesticus. J. Neurosci. 2:815–28 [Google Scholar]
  28. de la Iglesia HO, Meyer J, Schwartz WJ. 28.  2004. Using Per gene expression to search for photoperiodic oscillators in the hamster suprachiasmatic nucleus. Mol. Brain Res. 127:121–27 [Google Scholar]
  29. Piggins HD, Loudon A. 29.  2005. Circadian biology: clocks within clocks. Curr. Biol. 15:455–57 [Google Scholar]
  30. Chernetsov N, Kishkinev D, Mouritsen H. 30.  2008. A long-distance avian migrant compensates for longitudinal displacement during spring migration. Curr. Biol. 18:188–90 [Google Scholar]
  31. Kishkinev D, Chernetsov N, Mouritsen H. 31.  2010. A double clock or jetlag mechanism is unlikely to be involved in detection of east-west displacements in a long-distance avian migrant. Auk 127:773–80 [Google Scholar]
  32. Wiltschko W, Daum P, Fergenbauer-Kimmel A, Wiltschko R. 32.  1987. The development of the star compass in garden warblers. Sylvia borin. Ethology 74:285–92 [Google Scholar]
  33. Mouritsen H, Larsen ON. 33.  2001. Migrating songbirds tested in computer-controlled Emlen funnels use stellar cues for a time-independent compass. J. Exp. Biol. 204:3855–65 [Google Scholar]
  34. Wiltschko R, Wiltschko W. 34.  1980. The process of learning sun compass orientation in young homing pigeons. Naturwissenschaften 67:512–14 [Google Scholar]
  35. Able KP, Able MA. 35.  1990. Ontogeny of migratory orientation in the Savannah sparrow, Passerculus sandwichensis: calibration of the magnetic compass. Anim. Behav. 39:905–13 [Google Scholar]
  36. Able KP, Able MA. 36.  1993. Daytime calibration of magnetic orientation in a migratory bird requires a view of skylight polarization. Nature 364:523–25 [Google Scholar]
  37. Able KP, Able MA. 37.  1990. Calibration of the magnetic compass of a migratory bird by celestial rotation. Nature 347:378–80 [Google Scholar]
  38. Alert B, Michalik A, Helduser S, Mouritsen H, Güntürkün O. 38.  2015. Perceptual strategies of pigeons to detect a rotational centre—a hint for star compass learning?. PLOS ONE 10:e0119919 [Google Scholar]
  39. Wolf-Oberhollenzer F, Kirschfeld K. 39.  1994. Motion sensitivity in the nucleus of the basal optic root of the pigeon. J. Neurophysiol. 71:1559–73 [Google Scholar]
  40. Frost BJ. 40.  2010. A taxonomy of different forms of visual motion detection and their underlying neural mechanisms. Brain Behav. Evol. 75:218–35 [Google Scholar]
  41. Pecchia T, Gagliardo A, Vallortigara G. 41.  2011. Stable panoramic views facilitate snap-shot like memories for spatial reorientation in homing pigeons. PLOS ONE 6:e22657 [Google Scholar]
  42. Yang J, Zhang C, Wang SR. 42.  2005. Comparisons of visual properties between tectal and thalamic neurons with overlapping receptive fields in the pigeon. Brain Behav. Evol. 65:33–39 [Google Scholar]
  43. Budzynski CA, Bingman VP. 43.  2004. Participation of the thalamofugal visual pathway in a coarse pattern discrimination task in an open arena. Behav. Brain Res. 153:543–56 [Google Scholar]
  44. Kahn MC, Bingman VP. 44.  2009. Avian hippocampal role in space and content memory. Eur. J. Neurosci. 30:1900–8 [Google Scholar]
  45. Gagliardo A, Vallortigara G, Nardi D, Bingman VP. 45.  2005. A lateralized avian hippocampus: preferential role of the left hippocampal formation in homing pigeon sun compass–based spatial learning. Eur. J. Neurosci. 22:2549–59 [Google Scholar]
  46. Jonckers E, Güntürkün O, De Groof G, Van der Linden A, Bingman VP. 46.  2015. Network structure of functional hippocampal lateralization in birds. Hippocampus. In press; doi: 10.1002/hipo.22462
  47. Wiltschko R, Wiltschko W. 47.  1995. Magnetic Orientation in Animals Berlin: Springer
  48. Michalik A, Alert B, Engels S, Lefeldt N, Mouritsen H. 48.  2014. Star compass learning: How long does it take?. J. Ornithol. 155:225–34 [Google Scholar]
  49. Mouritsen H, Feenders G, Liedvogel M, Kropp W. 49.  2004. Migratory birds use head scans to detect the direction of the Earth's magnetic field. Curr. Biol. 14:1946–49 [Google Scholar]
  50. Ritz T, Ahmad M, Mouritsen H, Wiltschko R, Wiltschko W. 50.  2010. Photoreceptor-based magnetoreception: optimal design of receptor molecules, cells, and neuronal processing. J. R. Soc. Interface 7:S135–46 [Google Scholar]
  51. Mouritsen H. 51.  2013. The magnetic senses. Neurosciences—From Molecule to Behavior: A University Textbook CG Galizia, PM Lledo 427–43 Berlin: Springer [Google Scholar]
  52. Blakemore R. 52.  1975. Magnetotactic bacteria. Science 190:377–79 [Google Scholar]
  53. Kirschvink JL, Winklhofer M, Walker MM. 53.  2010. Biophysics of magnetic orientation: strengthening the interface between theory and experimental design. J. R. Soc. Interface 7:179–91 [Google Scholar]
  54. Fleissner G, Holtkamp-Rotzler E, Hanzlik M, Winklhofer M. 54.  et al. 2003. Ultrastructural analysis of a putative magnetoreceptor in the beak of homing pigeons. J. Comp. Neurol. 458:350–60 [Google Scholar]
  55. Falkenberg G, Fleissner G, Schuchardt K, Kuehbacher M, Thalau P. 55.  et al. 2010. Avian magnetoreception: Elaborate iron mineral containing dendrites in the upper beak seem to be a common feature of birds. PLOS ONE 5:e9231 [Google Scholar]
  56. Treiber CD, Salzer MC, Riegler J, Edelman N, Sugar C. 56.  et al. 2012. Clusters of iron rich cells in the upper beak of pigeons are macrophages not magnetosensitive neurons. Nature 484:367–70 [Google Scholar]
  57. Treiber CD, Salzer M, Breuss M, Ushakova L, Lauwers M. 57.  et al. 2013. High resolution anatomical mapping confirms the absence of a magnetic sense system in the rostral upper beak of pigeons. Commun. Integr. Biol. 6:e24859 [Google Scholar]
  58. Mouritsen H. 58.  2012. Sensory biology: search for the compass needles. Nature 484:320–21 [Google Scholar]
  59. Schulten K, Swenberg CE, Weller A. 59.  1978. A biomagnetic sensory mechanism based on magnetic field modulated coherent electron spin motion. Z. Phys. Chem. 1111–5
  60. Ritz T, Adem S, Schulten K. 60.  2000. A model for photoreceptor-based magnetoreception in birds. Biophys. J. 78:707–18 [Google Scholar]
  61. Rodgers CT, Hore P. 61.  2009. Chemical magnetoreception in birds: the radical pair mechanism. PNAS 106:353–60 [Google Scholar]
  62. Mouritsen H, Hore PJ. 62.  2012. The magnetic retina: light-dependent and trigeminal magnetoreception in migratory birds. Curr. Opin. Neurobiol. 22:343–52 [Google Scholar]
  63. Engels S, Schneider N-L, Lefeldt N, Hein CM, Zapka M. 63.  et al. 2014. Anthropogenic electromagnetic noise disrupts magnetic compass orientation in a migratory bird. Nature 509:353–56Shows that weak electromagnetic noise disrupts birds' magnetic compass, presenting evidence for quantum mechanical–based magnetoreception. [Google Scholar]
  64. Mouritsen H, Janssen-Bienhold U, Liedvogel M, Feenders G, Stalleicken J. 64.  et al. 2004. Cryptochromes and neuronal-activity markers colocalize in the retina of migratory birds during magnetic orientation. PNAS 101:14294–99 [Google Scholar]
  65. Möller A, Sagasser S, Wiltschko W, Schierwater B. 65.  2004. Retinal cryptochrome in a migratory passerine bird: a possible transducer for the avian magnetic compass. Naturwissenschaften 91:585–88 [Google Scholar]
  66. Liedvogel M, Maeda K, Henbest K, Schleicher E, Simon T. 66.  et al. 2007. Chemical magnetoreception: Bird cryptochrome 1a is excited by blue light and forms long-lived radical-pairs. PLOS ONE 2:e1106 [Google Scholar]
  67. Liedvogel M, Mouritsen H. 67.  2010. Cryptochromes—a potential magnetoreceptor: What do we know and what do we want to know?. J. R. Soc. Interface 7:S147–62 [Google Scholar]
  68. Nießner C, Denzau S, Gross JC, Peichl L, Bischof HJ. 68.  et al. 2011. Avian ultraviolet/violet cones identified as probable magnetoreceptors. PLOS ONE 6:e20091 [Google Scholar]
  69. Schneider T, Thalau HP, Semm P, Wiltschko W. 69.  1994. Melatonin is crucial for the migratory orientation of pied flycatchers Ficedula hypoleuca pallas. J. Exp. Biol. 194:255–62 [Google Scholar]
  70. Mouritsen H, Feenders G, Liedvogel M, Wada K, Jarvis ED. 70.  2005. Night vision brain area in migratory songbirds. PNAS 102:8339–44 [Google Scholar]
  71. Liedvogel M, Feenders G, Wada K, Troje NF, Jarvis ED, Mouritsen H. 71.  2007. Lateralized activation of Cluster N in the brains of migratory songbirds. Eur. J. Neurosci. 25:1166–73 [Google Scholar]
  72. Zapka M, Heyers D, Hein CM, Engels S, Schneider N-L. 72.  et al. 2009. Visual but not trigeminal mediation of magnetic compass information in a migratory bird. Nature 461:1274–77Demonstrates that magnetic compass information is processed in Cluster N; thus, birds “see” magnetic fields. [Google Scholar]
  73. Hein CM, Zapka M, Heyers D, Kutzschbauch S, Schneider N-L. 73.  et al. 2010. Night-migratory garden warblers can orient with their magnetic compass using the left, the right or both eyes. J. R. Soc. Interface 7:S227–33 [Google Scholar]
  74. Heyers D, Manns M, Luksch H, Güntürkün O, Mouritsen H. 74.  2007. A visual pathway links brain structures active during magnetic compass orientation in migratory birds. PLOS ONE 2:e937 [Google Scholar]
  75. Zapka M, Heyers D, Liedvogel M, Jarvis ED, Mouritsen H. 75.  2010. Night-time neuronal activation of Cluster N in a day- and night-migrating songbird. Eur. J. Neurosci. 32:619–24 [Google Scholar]
  76. Semm P, Demaine C. 76.  1986. Neurophysiological properties of magnetic cells in the pigeons' visual-system. J. Comp. Physiol. A 159:619–25 [Google Scholar]
  77. Heyers D, Zapka M, Hoffmeister M, Wild JM, Mouritsen H. 77.  2010. Magnetic field changes activate the trigeminal brainstem complex in a migratory bird. PNAS 107:9394–99Demonstrates that the trigeminal nerve is also involved in magnetoreception that is probably map related (see Reference 88). [Google Scholar]
  78. Lefeldt N, Heyers D, Schneider N-L, Engels S, Elbers D. 78.  et al. 2014. Magnetic field-driven induction of ZENK in the trigeminal system of pigeons (Columba livia). J. R. Soc. Interface 11:20140777 [Google Scholar]
  79. Ramírez E, Marín G, Mpodozis J, Letelier JC. 79.  2014. Extracellular recordings reveal absence of magneto sensitive units in the avian optic tectum. J. Comp. Physiol. A 200:983–96 [Google Scholar]
  80. Wu LQ, Dickman JD. 80.  2011. Magnetoreception in an avian brain in part mediated by inner ear lagena. Curr. Biol. 21:418–23 [Google Scholar]
  81. Wu LQ, Dickman JD. 81.  2012. Neural correlates of a magnetic sense. Science 336:1054–57 [Google Scholar]
  82. Atoji Y, Wild JM. 82.  2012. Afferent and efferent projections of the mesopallium in the pigeon (Columba livia). J. Comp. Neurol 520:717–41 [Google Scholar]
  83. Montagnese CM, Székely AD, Ádám Á, Csillag A. 83.  2004. Efferent connections of septal nuclei of the domestic chick (Gallus domesticus): an anterograde pathway tracing study with a bearing on functional circuits. J. Comp. Neurol. 469:437–56 [Google Scholar]
  84. Wild JM. 84.  1988. Vestibular projections to the thalamus of the pigeon: an anatomical study. J. Comp. Neurol. 271:451–60 [Google Scholar]
  85. Korzeniewska E, Güntürkün O. 85.  1990. Sensory properties and afferents of the N. dorsolateralis posterior thalami of the pigeon. J. Comp. Neurol. 292:457–79 [Google Scholar]
  86. Vollrath FW, Delius JD. 86.  1976. Vestibular projections to the thalamus of the pigeon. Brain Behav. Evol. 13:58–68 [Google Scholar]
  87. Thorup K, Bisson IA, Bowlin MS, Holland RA, Wingfield JC. 87.  et al. 2007. Evidence for a navigational map stretching across the continental US in a migratory songbird. PNAS 104:18115–19 [Google Scholar]
  88. Kishkinev D, Chernetsov N, Heyers D, Mouritsen H. 88.  2013. Migratory reed warblers need intact trigeminal nerves to correct for a 1,000 km eastward displacement. PLOS ONE 8:e65847 [Google Scholar]
  89. Wallraff HG. 89.  2005. Avian Navigation: Pigeon Homing as a Paradigm Berlin: Springer
  90. Gagliardo A, Ioalè P, Savini M, Wild M. 90.  2009. Navigational abilities of adult and experienced homing pigeons deprived of olfactory or trigeminally mediated magnetic information. J. Exp. Biol. 212:3119–24The last of three papers by the same research group showing that the olfactory nerve is essential for pigeon homing. [Google Scholar]
  91. Gagliardo A, Bried J, Lambardi Luschi P, Wikelski M, Bonadonna F. 91.  2013. Oceanic navigation in Cory's shearwaters: evidence for a crucial role of olfactory cues for homing after displacement. J. Exp. Biol. 216:2798–805 [Google Scholar]
  92. Guilford T, Biro D. 92.  2014. Route following and the pigeon's familiar area map. J. Exp. Biol. 217:169–79 [Google Scholar]
  93. Dennis TE, Rayner MJ, Walker MM. 93.  2007. Evidence that pigeons orient to geomagnetic intensity during homing. Proc. R. Soc. B 274:1153–58 [Google Scholar]
  94. Wallraff HG. 94.  2001. Navigation by homing pigeons: updated perspective. Ethol. Ecol. Evol. 13:1–48 [Google Scholar]
  95. Fransson T, Jakobsson S, Johansson P, Kullberg C, Lind J. 95.  et al. 2001. Bird migration—magnetic cues trigger extensive refuelling. Nature 414:35–36 [Google Scholar]
  96. Kishkinev D, Chernetsov N, Pakhomov A, Heyers D, Mouritsen H. 96.  2015. Eurasian reed warblers compensate for virtual magnetic displacement. Curr. Biol. 25:R822–24 [Google Scholar]
  97. Mora CV, Davison M, Wild JM, Walker MM. 97.  2004. Magnetoreception and its trigeminal mediation in the homing pigeon. Nature 432:508–11 [Google Scholar]
  98. Beason RC, Semm P. 98.  1996. Does the avian ophthalmic nerve carry magnetic navigational information?. J. Exp. Biol. 199:1241–44 [Google Scholar]
  99. Holland RA. 99.  2010. Differential effects of magnetic pulses on the orientation of naturally migrating birds. J. R. Soc. Interface 7:1617–25 [Google Scholar]
  100. Wild JM, Zeigler HP. 100.  1996. Central projections and somatotopic organisation of trigeminal primary afferents in pigeon (Columba livia). J. Comp. Neurol. 368:136–52 [Google Scholar]
  101. Arends JJA, Woelders-Block A, Dubbeldam JL. 101.  1984. The efferent connections of the nuclei of the descending trigeminal tract in the mallard (Anas platyrhyncos L.). Neuroscience 13:797–817 [Google Scholar]
  102. Wild JM, Farabaugh SM. 102.  1996. Organization of afferent and efferent projections of the nucleus basalis prosencephali in a passerine, Taeniopygia guttata. J. Comp. Neurol. 365:306–28 [Google Scholar]
  103. Wild JM, Arends JJ, Zeigler HP. 103.  1985. Telencephalic connections of the trigeminal system in the pigeon (Columba livia). J. Comp. Neurol 234:441–64 [Google Scholar]
  104. Kröner S, Güntürkün O. 104.  1999. Afferent and efferent connections of the caudolateral neostriatum in the pigeon (Columba livia): a retro- and anterograde pathway tracing study. J. Comp. Neurol 407:228–60 [Google Scholar]
  105. Benvenuti S, Wallraff HG. 105.  1985. Pigeon navigation: site simulation by means of atmospheric odours. J. Comp. Physiol. A 156:737–46 [Google Scholar]
  106. Ioalè P, Nozzolini M, Papi F. 106.  1990. Homing pigeons do extract directional information from olfactory stimuli. Behav. Ecol. Sociobiol. 26:301–5Elegantly demonstrates that olfactory cues provide directional information for pigeon homing. [Google Scholar]
  107. Gagliardo A. 107.  2013. Forty years of olfactory navigation in birds. J. Exp. Biol. 216:2165–71 [Google Scholar]
  108. Wallraff HG, Andreae MO. 108.  2000. Spatial gradients in ratios of atmospheric trace gases: a study stimulated by experiments on bird navigation. Tellus B 52:1138–57 [Google Scholar]
  109. Patzke N, Manns M, Güntürkün O. 109.  2011. Telencephalic organisation of the olfactory system in homing pigeons (Columba livia). Neuroscience 194:53–61 [Google Scholar]
  110. Atoji Y, Wild JM. 110.  2014. Efferent and afferent connections of the olfactory bulb and prepiriform cortex in the pigeon (Columba livia). J. Comp. Neurol 522:1728–52 [Google Scholar]
  111. Rehkämper G, Frahm HD, Cnotka J. 111.  2008. Mosaic evolution and adaptive brain component alteration under domestication seen on the background of evolutionary theory. Brain Behav. Evol. 71:115–26 [Google Scholar]
  112. Gagliardo A, Pecchia T, Savini M, Odetti F, Ioalè P, Vallortigara G. 112.  2007. Olfactory lateralization in homing pigeons: initial orientation of birds receiving a unilateral olfactory input. Eur. J. Neurosci. 25:1511–16 [Google Scholar]
  113. Wallraff HG. 113.  1988. Olfactory deprivation in pigeons: examination of methods applied in homing experiments. Comp. Biochem. Physiol. A 89:621–29 [Google Scholar]
  114. Papi F, Fiore L, Fiaschi V, Benvenuti S. 114.  1971. The influence of olfactory nerve section on the homing capacity of carrier pigeons. Monit. Zool. Ital. 5:265–67 [Google Scholar]
  115. Papi F, Casini G. 115.  1990. Pigeons with ablated pyriform cortex home from familiar but not from unfamiliar sites. PNAS 87:3783–87 [Google Scholar]
  116. Patzke N, Manns M, Güntürkün O, Ioalè P, Gagliardo A. 116.  2010. Navigation induced ZENK expression in the olfactory system of pigeons (Columba livia). Eur. J. Neurosci. 31:2062–72 [Google Scholar]
  117. Gagliardo A, Ioalè P, Savini M, Dell'Omo G, Bingman VP. 117.  2009. Hippocampal-dependent familiar area map supports corrective re-orientation following navigational error during pigeon homing: a GPS-tracking study. Eur. J. Neurosci. 29:2389–400Demonstrates that the pigeon hippocampus, among other functions, processes landscape features to adjust navigational direction. [Google Scholar]
  118. Meade J, Biro D, Guilford T. 118.  2006. Route recognition in the homing pigeon, Columba livia. Anim. Behav 72:975–80 [Google Scholar]
  119. Lipp HP, Vyssotski AL, Wolfer DP, Renaudineau S, Savini M. 119.  et al. 2004. Pigeon homing along highways and exits. Curr. Biol. 1:1239–49 [Google Scholar]
  120. Mora CV, Ross JD, Gorsevski PV, Chowdhury B, Bingman VP. 120.  2012. Evidence for discrete landmark use by pigeons during homing. J. Exp. Biol. 215:3379–87 [Google Scholar]
  121. Prior H, Lingenauber F, Nitschke J, Güntürkün O. 121.  2002. Orientation and lateralized cue use in pigeons navigating a large indoor environment. J. Exp. Biol. 205:1795–805 [Google Scholar]
  122. Della Chiesa A, Pecchia T, Tommasi L, Vallortigara G. 122.  2006. Multiple landmarks, the encoding of environmental geometry and the spatial logics of a dual brain. Anim. Cogn. 9:281–93 [Google Scholar]
  123. Clayton NS. 123.  1993. Lateralization and unilateral transfer of spatial memory in marsh tits. J. Comp. Physiol. A 171:799–806 [Google Scholar]
  124. Herold C, Coppola VJ, Bingman VP. 124.  2015. The maturation of research into the avian hippocampal formation: recent discoveries from one of the nature's foremost navigators. Hippocampus. In press; doi: 10.1002/hipo.22463
  125. Krebs JR, Sherry DF, Healy SD, Perry VH, Vaccarino AL. 125.  1989. Hippocampal specialization of food-storing birds. PNAS 86:1388–92 [Google Scholar]
  126. Pravosudov VV, Kitaysky AS, Omanska A. 126.  2006. The relationship between migratory behavior, memory and the hippocampus: an intraspecific comparison. Proc. Biol. Sci. 273:2641–49 [Google Scholar]
  127. Bingman VP, Cheng K. 127.  2005. Mechanisms of animal global navigation: comparative perspectives and enduring challenges. Ethol. Ecol. Evol. 17:295–318 [Google Scholar]
  128. Gagliardo A, Pollonara E, Coppola VJ, Santos CD, Wikelski M. 128.  et al. 2014. Evidence for perceptual neglect of environmental features in hippocampal-lesioned pigeons during homing. Eur. J. Neurosci. 40:3102–10 [Google Scholar]
  129. Tommasi L, Gagliardo A, Andrew RJ, Vallortigara G. 129.  2003. Separate processing mechanisms for encoding of geometric and landmark information in the avian hippocampus. Eur. J. Neurosci. 17:1695–702 [Google Scholar]
  130. Nardi D, Bingman VP. 130.  2007. Asymmetrical participation of the left and right hippocampus for representing environmental geometry in homing pigeons. Behav. Brain Res. 178:160–71 [Google Scholar]
  131. Yamazaki Y, Aust U, Huber L, Hausmann M, Güntürkün O. 131.  2007. Lateralized cognition: asymmetrical and complementary strategies of pigeons during discrimination of the “human concept”. Cognition 104:315–44 [Google Scholar]
  132. Gagliardo A, Odetti F, Ioalè P. 132.  2001. Relevance of visual cues for orientation at familiar sites by homing pigeons: an experiment in a circular arena. Proc. R. Soc. B 268:2065–70 [Google Scholar]
  133. Taube JS, Muller RU, Ranck JB. 133.  1990. Head-direction cells recorded from the postsubiculum in freely moving rats. 1. Description and quantitative analysis. J. Neurosci. 10:420–35 [Google Scholar]
  134. Taube JS. 134.  2007. The head direction signal: origins and sensory-motor integration. Annu. Rev. Neurosci. 30:181–207 [Google Scholar]
  135. O'Keefe J. 135.  1976. Place units in the hippocampus of the freely moving rat. Exp. Neurol. 51:78–109 [Google Scholar]
  136. Hafting T, Fyhn M, Molden S, Moser M-B, Moser EI. 136.  2005. Microstructure of a spatial map in the entorhinal cortex. Nature 436:801–6 [Google Scholar]
  137. Yartsev MM, Ulanovsky N. 137.  2013. Representation of three-dimensional space in the hippocampus of flying bats. Science 340:367–72 [Google Scholar]
  138. Geva-Sagiv M, Las L, Yovel Y, Ulanovsky N. 138.  2015. Spatial cognition in bats and rats: from sensory acquisition to multiscale maps and navigation. Nat. Rev. Neurosci. 16:94–108Summarizes excellent work on bat head direction and place cells that encode three-dimensional space. [Google Scholar]
  139. Finkelstein A, Derdikman D, Rubin A, Foerster JN, Las L. 139.  et al. 2014. Three-dimensional head-direction coding in the bat brain. Nature 517:159–64 [Google Scholar]
  140. Lever C, Burton S, Jeewajee A, O'Keefe J, Burgess N. 140.  2009. Boundary vector cells in the subiculum of the hippocampal formation. J. Neurosci. 29:9771–77 [Google Scholar]
  141. Siegel JJ, Nitz D, Bingman VP. 141.  2006. Lateralized functional components of spatial cognition in the avian hippocampal formation: evidence from single-unit recordings in freely moving homing pigeons. Hippocampus 16:125–40 [Google Scholar]
  142. Herold C, Bingman VP, Ströckens F, Letzner S, Sauvage M. 142.  et al. 2014. Distribution of neurotransmitter receptors and zinc in the pigeon (Columba livia) hippocampal formation: a basis for further comparison with the mammalian hippocampus. J. Comp. Neurol. 522:2553–75 [Google Scholar]
  143. Shanahan M, Bingman VP, Shimizu T, Wild M, Güntürkün O. 143.  2013. Large-scale network organization in the avian forebrain: a connectivity matrix and theoretical analysis. Front. Comp. Neurosci. 7:89A comprehensive connectome reference for neuronal connections in the entire avian forebrain. [Google Scholar]
  144. Güntürkün O. 144.  2005. The avian ‘prefrontal cortex’ and cognition. Curr. Opin. Neurobiol. 15:686–93Shows that mammals and birds independently evolved a prefrontal area that orchestrates executive functions. [Google Scholar]
  145. Güntürkün O. 145.  2012. The convergent evolution of neural substrates for cognition. Psychol. Res. 76:212–19 [Google Scholar]
  146. Dubbeldam JL, den Boer–Visser AM, Bout RG. 146.  1997. Organization and efferent connections of the archistriatum of the mallard Anas platyrhynchos, an anterograde and retrograde tracing study. J. Comp. Neurol. 388:632–57 [Google Scholar]
  147. Wild JM, Williams MN. 147.  2000. Origin, course, and terminations of an avian pyramidal tract. J. Comp. Neurol. 416:429–50 [Google Scholar]
  148. Dubbeldam JL. 148.  2014. A reappraisal of the existence of an avian pyramidal tract, a review. Anim. Biol. 64:129–40 [Google Scholar]
  149. Feenders G, Liedvogel M, Rivas M, Zapka M, Horita H. 149.  et al. 2008. Molecular mapping of movement-associated areas in the avian brain: a motor theory for vocal learning origin. PLOS ONE 3:e1768 [Google Scholar]
  150. Güntürkün O, Miceli D, Watanabe M. 150.  1993. Anatomy of the avian thalamofugal pathway. Vision, Brain and Behavior in Birds HP Zeigler, HI Bischof 115–35 Cambridge: MIT Press [Google Scholar]
  151. Güntürkün O. 151.  2000. 1. Sensory physiology: vision. Sturkie's Avian Physiology PD Sturkie, GC Whittow, pp. 1–19. San Diego, CA: Academic
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