Neurobiology of the homing pigeon—a review

Homing pigeons are well known as good homers, and the knowledge of principal parameters determining their homing behaviour and the neurological basis for this have been elucidated in the last decades. Several orientation mechanisms and parameters—sun compass, earth’s magnetic field, olfactory cues, visual cues—are known to be involved in homing behaviour, whereas there are still controversial discussions about their detailed function and their importance. This paper attempts to review and summarise the present knowledge about pigeon homing by describing the known orientation mechanisms and factors, including their pros and cons. Additionally, behavioural features like motivation, experience, and track preferences are discussed. All behaviour has its origin in the brain and the neuronal basis of homing and the neuroanatomical particularities of homing pigeons are a main topic of this review. Homing pigeons have larger brains in comparison to other non-homing pigeon breeds and particularly show increased size of the hippocampus. This underlines our hypothesis that there is a relationship between hippocampus size and spatial ability. The role of the hippocampus in homing and its plasticity in response to navigational experience are discussed in support of this hypothesis.

[1]  Jackie Chappell,et al.  The orientational salience of visual cues to the homing pigeon , 1997, Animal Behaviour.

[2]  Martin Möhle,et al.  Navigational Experience Affects Hippocampus Size in Homing Pigeons , 2008, Brain, Behavior and Evolution.

[3]  R. Andrew,et al.  Right hemisphere advantage for topographical orientation in the domestic chick , 1989, Neuropsychologia.

[4]  W. Wiltschko,et al.  Magnetic orientation and magnetoreception in birds and other animals , 2005, Journal of Comparative Physiology A.

[5]  G. Matthews. The Orientation of Untrained Pigeons: a Dichotomy in the Homing Process , 1953 .

[6]  J. K. Mai,et al.  Pattern of brain glucose utilization following magnetic stimulation. , 1990, Journal fur Hirnforschung.

[7]  J. Červený,et al.  Magnetic alignment in grazing and resting cattle and deer , 2008, Proceedings of the National Academy of Sciences.

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

[9]  M. Davison,et al.  Magnetoreception and its trigeminal mediation in the homing pigeon , 2004, Nature.

[10]  J. Wild,et al.  Intratelencephalic connections of the hippocampus in pigeons (Columba livia) , 2002, The Journal of comparative neurology.

[11]  Gerald E. Hough,et al.  The Avian Hippocampus, Homing in Pigeons and the Memory Representation of Large-Scale Space1 , 2005, Integrative and comparative biology.

[12]  G. Vallortigara,et al.  Functional asymmetry of left and right avian piriform cortex in homing pigeons' navigation , 2005, The European journal of neuroscience.

[13]  C. Walcott Multi-modal Orientation Cues in Homing Pigeons1 , 2005, Integrative and comparative biology.

[14]  P. Ioalé,et al.  Homing pigeons do extract directional information from olfactory stimuli , 1990, Behavioral Ecology and Sociobiology.

[15]  R. Wiltschko,et al.  Orientation of homing pigeons: compass orientation vs piloting by familiar landmarks , 1983, Journal of comparative physiology.

[16]  J. Hounsgaard,et al.  Organization of Projection-Specific Interneurons in the Spinal Cord of the Red-Eared Turtle , 2008, Brain, Behavior and Evolution.

[17]  Gerhard Tröster,et al.  Pigeon Homing along Highways and Exits , 2004, Current Biology.

[18]  Ingo Schiffner,et al.  Homing flights of pigeons over familiar terrain , 2007, Animal Behaviour.

[19]  Walker,et al.  On a Wing and a Vector: a Model for Magnetic Navigation by Homing Pigeons. , 1998, Journal of theoretical biology.

[20]  P. Harvey,et al.  Mosaic evolution of brain structure in mammals , 2000, Nature.

[21]  N. E. Baldaccini,et al.  Olfactory navigation of pigeons: The effect of treatment with odorous air currents , 1974, Journal of comparative physiology.

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

[23]  V. Bingman,et al.  The effects of a changing ambient magnetic field on single-unit activity in the homing pigeon hippocampus , 2006, Brain Research Bulletin.

[24]  H. P. Zeigier,et al.  Vision, brain, and behavior in birds. , 1994 .

[25]  J. Terkel,et al.  Magnetic compass orientation in the blind mole rat Spalax ehrenbergi. , 2001, The Journal of experimental biology.

[26]  C. Demaine,et al.  The avian pineal gland as an independent magnetic sensor , 1985, Neuroscience Letters.

[27]  F. Moore,et al.  Calibration of magnetic and celestial compass cues in migratory birds - a review of cue-conflict experiments , 2006, Journal of Experimental Biology.

[28]  W. Wiltschko,et al.  Ultrastructural analysis of a putative magnetoreceptor in the beak of homing pigeons , 2003, The Journal of comparative neurology.

[29]  D. Sherry,et al.  Spatial memory and adaptive specialization of the hippocampus , 1992, Trends in Neurosciences.

[30]  Juan Fernández I: Evolutionary Theory , 2010 .

[31]  V. Csernus The Avian Pineal Gland , 2006, Chronobiology international.

[32]  S. Benvenuti,et al.  Pigeon homing: Combined effect of olfactory deprivation and visual impairment , 1983 .

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

[34]  W. Keeton,et al.  Magnets interfere with pigeon homing. , 1971, Proceedings of the National Academy of Sciences of the United States of America.

[35]  W. Wiltschko,et al.  Pigeon homing: Different effects of olfactory deprivation in different countries , 1987, Behavioral Ecology and Sociobiology.

[36]  J. Wild,et al.  Having the nerve to home: trigeminal magnetoreceptor versus olfactory mediation of homing in pigeons , 2006, Journal of Experimental Biology.

[37]  Wolfgang Wiltschko,et al.  Orientation of Birds in Total Darkness , 2008, Current Biology.

[38]  M. D.,et al.  Sun Compass , 1945, Nature.

[39]  W. Wiltschko,et al.  Neural basis of the magnetic compass: interactions of visual, magnetic and vestibular inputs in the pigeon's brain , 1984, Journal of Comparative Physiology A.

[40]  J. L. Gould Homing Behavior: Decisions, Dominance and Democracy , 2006, Current Biology.

[41]  P. Ioalè Pigeon orientation: effects of the application of magnets under overcast skies , 2000, Naturwissenschaften.

[42]  O. Güntürkün The functional organization of the avian visual system , 1991 .

[43]  H. Schinz Naturgeschichte der Vögel , 1853 .

[44]  A. Arnold,et al.  Song Lateralization in the Zebra Finch , 1997, Hormones and Behavior.

[45]  V. Bingman,et al.  Connections of the pigeon dorsomedial forebrain studied with WGA‐HRP and 3H‐proline , 1986, The Journal of comparative neurology.

[46]  Beason,et al.  Does the avian ophthalmic nerve carry magnetic navigational information? , 1996, The Journal of experimental biology.

[47]  Marian Stamp Dawkins,et al.  Bird Navigation: the Solution of a Mystery?, R. Robin Baker. Hodder & Stoughton, London (1984), x, +256. Price £9.75 (paperback) , 1984 .

[48]  A C Kamil,et al.  Way-finding and landmarks: the multiple-bearings hypothesis. , 2001, The Journal of experimental biology.

[49]  V. Kruska DomestikationsbedingteHirngrößenanderungen bei Säugetieren , 2009 .

[50]  C. T. Steele,et al.  Circadian organization and the role of the pineal in birds , 2001, Microscopy research and technique.

[51]  M. Walker,et al.  Evidence that pigeons orient to geomagnetic intensity during homing , 2007, Proceedings of the Royal Society B: Biological Sciences.

[52]  Wolfgang Wiltschko,et al.  Magnetoreception in birds: two receptors for two different tasks , 2007, Journal of Ornithology.

[53]  Wolfgang Wiltschko,et al.  Avian navigation: from historical to modern concepts , 2003, Animal Behaviour.

[54]  P Ioalé,et al.  The homing pigeon hippocampus and the development of landmark navigation. , 1998, Developmental psychobiology.

[55]  David P Wolfer,et al.  Miniature neurologgers for flying pigeons: multichannel EEG and action and field potentials in combination with GPS recording. , 2006, Journal of neurophysiology.

[56]  Alfonso F Davila,et al.  Magnetic pulse affects a putative magnetoreceptor mechanism. , 2005, Biophysical journal.

[57]  M. Walker,et al.  Pigeon homing: sun compass use in the southern hemisphere , 1998, Behavioral Ecology and Sociobiology.

[58]  P. Semm Neurobiological investigations on the magnetic sensitivity of the pineal gland in rodents and pigeons , 1983 .

[59]  R. Sossinka Chapter 7 – DOMESTICATION IN BIRDS , 1982 .

[60]  D. Nardi,et al.  Asymmetrical participation of the left and right hippocampus for representing environmental geometry in homing pigeons , 2007, Behavioural Brain Research.

[61]  V. Bingman,et al.  Hippocampal participation in navigational map learning in young homing pigeons is dependent on training experience , 2000, The European journal of neuroscience.

[62]  Dora Biro,et al.  Familiar route loyalty implies visual pilotage in the homing pigeon. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[63]  Beason,et al.  Behavioural evidence for the use of magnetic material in magnetoreception by a migratory bird , 1995, The Journal of experimental biology.

[64]  Martin Wild,et al.  Navigational abilities of homing pigeons deprived of olfactory or trigeminally mediated magnetic information when young , 2008, Journal of Experimental Biology.

[65]  H. G. Wallraff Navigation by homing pigeons: updated perspective , 2001 .

[66]  A. Wieraszko,et al.  Comparative, in vitro, studies of hippocampal tissue from homing and non-homing pigeon , 1996, Brain Research.

[67]  J. Krebs,et al.  Hippocampal growth and attrition in birds affected by experience. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[68]  K. Frisch Die Sonne als Kompaß im Leben der Bienen , 2005, Experientia.

[69]  Verner P Bingman,et al.  Lateralization of spatial learning in the avian hippocampal formation. , 2004, Behavioral neuroscience.

[70]  A Gagliardo,et al.  Homing in Pigeons: The Role of the Hippocampal Formation in the Representation of Landmarks Used for Navigation , 1999, The Journal of Neuroscience.

[71]  N. Clayton,et al.  Development of food-storing and the hippocampus in juvenile marsh tits (Parus palustris) , 1996, Behavioural Brain Research.

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

[73]  W. Wiltschko,et al.  Sun-compass orientation in homing pigeons: compensation for different rates of change in azimuth? , 2000, The Journal of experimental biology.

[74]  Y. Fukada,et al.  Identification of rhodopsin in the pigeon deep brain , 1998, FEBS letters.

[75]  W. Wiltschko,et al.  Bird navigation: what type of information does the magnetite-based receptor provide? , 2006, Proceedings of the Royal Society B: Biological Sciences.

[76]  G. Wagner Natural geomagnetic anomalies and homing in pigeons , 1983 .

[77]  Lynn Nadel,et al.  The spatial brain. , 2004, Neuropsychology.

[78]  H. Hemmer Domestication: the decline of environmental appreciation. , 1990 .

[79]  Gerald E. Hough,et al.  Intrahippocampal connections in the pigeon (Columba livia) as revealed by stimulation evoked field potentials , 2002, The Journal of comparative neurology.

[80]  G. Vallortigara,et al.  Encoding of geometric and landmark information in the left and right hemispheres of the Avian Brain. , 2001, Behavioral neuroscience.

[81]  Verner P. Bingman,et al.  Homing behavior of hippocampus and parahippocampus lesioned pigeons following short-distance releases , 1990, Behavioural Brain Research.

[82]  Sean H. Rice,et al.  Evolutionary Theory: Mathematical and Conceptual Foundations , 2004 .

[83]  Eric Hardy.,et al.  Bird Navigation , 1971, Nature.

[84]  W. Wiltschko,et al.  The Geomagnetic Field and its Role in Directional Orientation , 2001 .

[85]  W. Möllendorff,et al.  Handbuch der Mikroskopischen Anatomie des Menschen , 1958 .

[86]  H. Williams,et al.  Right-side dominance for song control in the zebra finch. , 1992, Journal of neurobiology.

[87]  V. Bingman,et al.  Piriform cortex ablations block navigational map learning in homing pigeons , 1997, Behavioural Brain Research.

[88]  L. Rogers,et al.  Behavioral, Structural and Neurochemical Asymmetries in the Avian Brain: A Model System for Studying Visual Development and Processing , 1996, Neuroscience & Biobehavioral Reviews.

[89]  Victoria A. Braithwaite,et al.  Viewing familiar landscapes affects pigeon homing , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[90]  G. Vallortigara,et al.  Lateral asymmetries due to preferences in eye use during visual discrimination learning in chicks , 1996, Behavioural Brain Research.

[91]  W. Wiltschko Compasses used by birds , 1983 .

[92]  Pigeon homing: Further experiments on shielded lofts , 1983 .

[93]  R. Holland,et al.  The role of visual landmarks in the avian familiar area map , 2003, Journal of Experimental Biology.

[94]  G. Vallortigara,et al.  Olfactory lateralization in homing pigeons: initial orientation of birds receiving a unilateral olfactory input , 2007, The European journal of neuroscience.

[95]  G. Dell’Omo,et al.  Finding home: the final step of the pigeons' homing process studied with a GPS data logger , 2007, Journal of Experimental Biology.

[96]  M. A. Coemans,et al.  The photopic sensitivity of the yellow field of the pigeon's retina to ultraviolet light , 1994, Vision Research.

[97]  Gerald E. Hough,et al.  Revised nomenclature for avian telencephalon and some related brainstem nuclei , 2004, The Journal of comparative neurology.

[98]  J. T. Erichsen,et al.  Lower-field myopia in birds: An adaptation that keeps the ground in focus , 1990, Vision Research.

[99]  R. Wiltschko,et al.  The function of olfactory input in pigeon orientation: does it provide navigational information or play another role? , 1996, The Journal of experimental biology.

[100]  J. Phillips,et al.  Extraocular magnetic compass in newts , 1999, Nature.

[101]  Hans-Peter Lipp,et al.  A GPS logger and software for analysis of homing in pigeons and small mammals , 2000, Physiology & Behavior.

[102]  G. Vallortigara Comparative Neuropsychology of the Dual Brain: A Stroll through Animals' Left and Right Perceptual Worlds , 2000, Brain and Language.

[103]  T. Guilford,et al.  Further evidence for visual landmark involvement in the pigeon's familiar area map , 1997, Animal Behaviour.

[104]  H. Karten,et al.  Comparison of olfactory bulb projections in pigeons and turtles. , 1985, Brain, behavior and evolution.

[105]  J. L. Gould,et al.  Homing of magnetized and demagnetized pigeons. , 1988, The Journal of experimental biology.

[106]  Dora Biro,et al.  How the viewing of familiar landscapes prior to release allows pigeons to home faster: evidence from GPS tracking. , 2002, The Journal of experimental biology.

[107]  S. Healy,et al.  Food storing and the hippocampus in corvids: amount and volume are correlated , 1992, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[108]  K. Schmidt-Koenig The sun compass , 1990, Experientia.

[109]  C. Walcott,et al.  Homing of single pigeons--analysis of tracks. , 1967, The Journal of experimental biology.

[110]  W. Cochran,et al.  Navigation: Bat orientation using Earth's magnetic field , 2006, Nature.

[111]  Hans Georg Wallraff,et al.  Avian Navigation: Pigeon Homing as a Paradigm , 2004 .

[112]  S. Healy,et al.  Hippocampal volume in migratory and non-migratory warblers: effects of age and experience , 1996, Behavioural Brain Research.

[113]  E. Visalberghi,et al.  MAGNETIC INFLUENCES ON PIGEON HOMING , 1979 .

[114]  D. Sumpter,et al.  From Compromise to Leadership in Pigeon Homing , 2006, Current Biology.

[115]  K. Schmidt-Koenig,et al.  Homing in pigeons with impaired vision. , 1972, Proceedings of the National Academy of Sciences of the United States of America.

[116]  W. Wiltschko,et al.  Pigeon homing: change in navigational strategy during ontogeny , 1985, Animal Behaviour.

[117]  A. N. Bowers,et al.  Visual circuits of the avian telencephalon: evolutionary implications , 1999, Behavioural Brain Research.

[118]  O. Güntürkün,et al.  Left-hemispheric superiority for visuospatial orientation in homing pigeons , 1999, Behavioural Brain Research.

[119]  R. Wiltschko The ontogeny of orientation in young pigeons , 1983 .

[120]  E. Mayr Animal Species and Evolution , 1964 .

[121]  W. Wiltschko,et al.  Pigeon homing: Olfactory orientation—a paradox , 1989, Behavioral Ecology and Sociobiology.

[122]  W. Wiltschko,et al.  Growing up in an altered magnetic field affects the initial orientation of young homing pigeons , 1983, Behavioral Ecology and Sociobiology.

[123]  Stephen Roberts,et al.  Pigeons combine compass and landmark guidance in familiar route navigation , 2007, Proceedings of the National Academy of Sciences.

[124]  J. L. Gould,et al.  Biogenic magnetite as a basis for magnetic field detection in animals. , 1981, Bio Systems.

[125]  D. Biro,et al.  Route recognition in the homing pigeon, Columba livia , 2006, Animal Behaviour.

[126]  P. Ioalé,et al.  Relevance of visual cues for orientation at familiar sites by homing pigeons: an experiment in a circular arena , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[127]  H. Frahm,et al.  Allometric comparison of brain weight and brain structure volumes in different breeds of the domestic pigeon, Columba livia f.d. (fantails, homing pigeons, strassers). , 1988, Brain, behavior and evolution.

[128]  J. J. Siegel,et al.  The Homing Pigeon Hippocampus and Space: In Search of Adaptive Specialization , 2003, Brain, Behavior and Evolution.

[129]  D. Nardi,et al.  A lateralized avian hippocampus: preferential role of the left hippocampal formation in homing pigeon sun compass‐based spatial learning , 2005, The European journal of neuroscience.

[130]  H. Frahm,et al.  Discontinuous Variability of Brain Composition among Domestic Chicken Breeds , 2003, Brain, Behavior and Evolution.

[131]  K. Frisch The sun as a compass in the life of a bee , 1950 .

[132]  L. Rogers,et al.  Functional lateralization of the chicken forebrain revealed by use of intracranial glutamate , 1980, Brain Research.

[133]  G. Rehkaemper Vergleichende Architektonik des Neocortex der Insectivora , 2009 .

[134]  N. Clayton Development of memory and the hippocampus: comparison of food-storing and nonstoring birds on a one-trial associative memory task , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[135]  H. Schröder,et al.  Forebrain specialization and the olfactory system in anseriform birds , 1992, Cell and Tissue Research.

[136]  H. Frahm,et al.  Mosaic Evolution and Adaptive Brain Component Alteration under Domestication Seen on the Background of Evolutionary Theory , 2007, Brain, Behavior and Evolution.

[137]  Verner P. Bingman,et al.  Rotation of visual landmark cues influences the spatial response profile of hippocampal neurons in freely-moving homing pigeons , 2008, Behavioural Brain Research.

[138]  Juan Pedro Vargas,et al.  Hippocampal formation is required for geometric navigation in pigeons , 2004, The European journal of neuroscience.

[139]  Giovanni Casini,et al.  Pigeons with ablated pyriform cortex home from familiar but not from unfamiliar sites. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[140]  K. Able,et al.  The debate over olfactory navigation by homing pigeons , 1996 .

[141]  V. Bingman,et al.  The ontogeny of the homing pigeon navigational map: evidence for a sensitive learning period , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[142]  F. Barth,et al.  Ecology of Sensing , 2001, Springer Berlin Heidelberg.

[143]  Gerald E. Hough,et al.  Internal connectivity of the homing pigeon (Columba livia) hippocampal formation: An anterograde and retrograde tracer study , 2003, The Journal of comparative neurology.

[144]  T. Yoshimura,et al.  Identification of the suprachiasmatic nucleus in birds. , 2001, American journal of physiology. Regulatory, integrative and comparative physiology.

[145]  D. Biro,et al.  Homing pigeons develop local route stereotypy , 2005, Proceedings of the Royal Society B: Biological Sciences.

[146]  J. Nelson,et al.  A mosaic pattern characterizes the evolution of the avian brain , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[147]  P. Ioalé,et al.  Pigeon Homing: The Navigational Map Developed in Adulthood is Based on Olfactory Information , 2008 .

[148]  Giorgio Vallortigara,et al.  Hemispheric processing of landmark and geometric information in male and female domestic chicks (Gallus gallus) , 2004, Behavioural Brain Research.

[149]  J. J. Siegel,et al.  Hippocampus and homing in pigeons: left and right hemispheric differences in navigational map learning , 2001, The European journal of neuroscience.

[150]  A. Della Chiesa,et al.  Multiple landmarks, the encoding of environmental geometry and the spatial logics of a dual brain , 2006, Animal Cognition.

[151]  R. Wiltschko Die Sonnenorientierung der Vögel. II. Entwicklung des Sonnenkompaß und sein Stellenwert im Orientierungssystem , 2005, Journal für Ornithologie.

[152]  C. Walcott,et al.  Homing pigeon navigation: the effects of in-flight exposure to a varying magnetic field , 1983 .

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

[154]  G. Vallortigara,et al.  Possible evolutionary origins of cognitive brain lateralization , 1999, Brain Research Reviews.

[155]  Michael Winklhofer,et al.  Superparamagnetic Magnetite in the Upper Beak Tissue of Homing Pigeons , 2000, Biometals.

[156]  G. Vallortigara,et al.  Bilateral participation of the hippocampus in familiar landmark navigation by homing pigeons , 2002, Behavioural Brain Research.

[157]  O. Güntürkün,et al.  Visual lateralization and homing in pigeons , 2004, Behavioural Brain Research.

[158]  L. Rogers,et al.  Lateralisation of function in the chicken fore-brain , 1979, Pharmacology Biochemistry and Behavior.

[159]  Lucia F. Jacobs,et al.  The Evolution of the Cognitive Map , 2003, Brain, Behavior and Evolution.

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

[161]  Giorgio Vallortigara,et al.  Separate processing mechanisms for encoding of geometric and landmark information in the avian hippocampus , 2003, The European journal of neuroscience.

[162]  V. Bingman,et al.  Further experiments on the relationship between hippocampus and orientation following phase-shift in homing pigeons , 2000, Behavioural Brain Research.

[163]  Karl Zilles,et al.  Parallel evolution in mammalian and avian brains: comparative cytoarchitectonic and cytochemical analysis , 2004, Cell and Tissue Research.

[164]  K. Schmidt-Koenig,et al.  Tracks of pigeons homing with frosted lenses , 1978, Animal Behaviour.

[165]  Wolfgang Wiltschko,et al.  Clock-shift experiments with homing pigeons: a compromise between solar and magnetic information? , 2001, Behavioral Ecology and Sociobiology.