Advertisement

Journal of Comparative Physiology A

, Volume 194, Issue 3, pp 267–282 | Cite as

Relative Wulst volume is correlated with orbit orientation and binocular visual field in birds

  • Andrew N. IwaniukEmail author
  • Christopher P. Heesy
  • Margaret I. Hall
  • Douglas R. W. Wylie
Original Paper

Abstract

In mammals, species with more frontally oriented orbits have broader binocular visual fields and relatively larger visual regions in the brain. Here, we test whether a similar pattern of correlated evolution is present in birds. Using both conventional statistics and modern comparative methods, we tested whether the relative size of the Wulst and optic tectum (TeO) were significantly correlated with orbit orientation, binocular visual field width and eye size in birds using a large, multi-species data set. In addition, we tested whether relative Wulst and TeO volumes were correlated with axial length of the eye. The relative size of the Wulst was significantly correlated with orbit orientation and the width of the binocular field such that species with more frontal orbits and broader binocular fields have relatively large Wulst volumes. Relative TeO volume, however, was not significant correlated with either variable. In addition, both relative Wulst and TeO volume were weakly correlated with relative axial length of the eye, but these were not corroborated by independent contrasts. Overall, our results indicate that relative Wulst volume reflects orbit orientation and possibly binocular visual field, but not eye size.

Keywords

Evolution Wulst Optic tectum Binocularity Eye size 

Abbreviations

GLd

Nucleus geniculatus lateralis, pars dorsalis

GLv

Nucleus geniculatus lateralis, pars ventralis

HA

Apical hyperpallium

HD

Densocellular part of the hyperpallium

HI

Interstitial part of the hyperpallium

IHA

Intercalated part of the hyperpallium

LGN

Lateral geniculate nucleus

S1

Primary somatosensory cortex

TeO

Optic tectum

V1

Primary visual cortex

W

Wulst

Notes

Acknowledgments

We wish to thank Healesville Sanctuary, Springvale Veterinary Clinic, Bishop Museum, National Museum of Natural History (Washington, DC) and American Museum of Natural History for providing us with access to specimens. Funding for this study was provided to ANI from the Alberta Ingenuity Fund and Natural Sciences and Engineering Research Council of Canada (NSERC), to MIH and CPH from the Jurassic Foundation and to DRWW from NSERC and Canada Research Chairs Program. All of the research reported herein was performed in accordance with the “Principles of animal care”, publication No. 86–23, revised 1985 of the National Institute of Health and with the Canadian Council for Animal Care regulations.

References

  1. Alma SB, Bee de Speroni N (1992) Indices cerebrales y composicion cuantitativa encefalica de Athene cunicularia y Tyto alba (Strigiformes: Strigidae y Tytonidae). Facenas (Argentina) 9:19–37Google Scholar
  2. Barton RA (2004) Binocularity and brain evolution in primates. Proc Nat Acad Sci USA 101:10113–10115PubMedCrossRefGoogle Scholar
  3. Barton RA, Harvey PH (2000) Mosaic evolution of brain structure in mammals. Nature 405:1055–1058PubMedCrossRefGoogle Scholar
  4. Beyer WH (1979) CRC standard mathematical tables, 25th edn. CRC Press, Boca RatonGoogle Scholar
  5. Boire D (1989) Comparaison quantitative de l’encephale de ses grades subdivisions et de relais visuals, trijumaux et acoustiques chez 28 especes. PhD Thesis, Universite de Montreal, MontrealGoogle Scholar
  6. Brainard MS, Knudsen EI (1995) Dynamics of visually guided auditory plasticity in the optic tectum of the barn owl. J Neurophysiol 73:595–614PubMedGoogle Scholar
  7. Burton RF (2006) A new look at the scaling of size in mammalian eyes. J Zool 269:225–232Google Scholar
  8. Carezzano FJ, Bee de Speroni N (1995) Composicion volumetrica encefalica e indices cerebrales en tres aves de ambiente acuatico (Ardeidae, Podicipedidae, Rallidae). Facenas 11:75–83Google Scholar
  9. Cartmill M (1970) The orbits of arboreal mammals: a reassessment of the arboreal theory of primate evolution. Unpublished PhD dissertation, University of Chicago, ChicagoGoogle Scholar
  10. Christidis L, Schodde R, Shaw DD, Maynes SF (1991) Relationships among the Australo-Papuan parrots, lorikeets and cockatoos (Aves: Psittaciformes). Condor 93:302–317CrossRefGoogle Scholar
  11. Cotter JR (1976) Visual and nonvisual units recorded from the optic tectum of Gallus domesticus. Brain Behav Evol 13:1–21PubMedGoogle Scholar
  12. Deacon TW (1990) Fallacies of progression in theories of brain-size evolution. Int J Primatol 11:193–236CrossRefGoogle Scholar
  13. Deng C, Wang B (1993) Convergence of somatic and visual afferent impulses in the Wulst of pigeon. Exp Brain Res 96:287–290PubMedCrossRefGoogle Scholar
  14. Ebinger P (1995) Domestication and plasticity of brain organization in mallards (Anas platyrhynchos). Brain Behav Evol 45:286–300PubMedCrossRefGoogle Scholar
  15. Ebinger P, Löhmer R (1984) Comparative quantitative investigations on brains of rock doves, domestic and urban pigeons (Columba l. livia). Z zool Syst Evolut-forsch 22:136–145CrossRefGoogle Scholar
  16. Fernandez P, Carezzano F, Bee de Speroni N (1997) Análisis cuantitativo encefálico e índices cerebrales en Aratinga acuticaudata y Myopsitta monachus de Argentina (Aves: Psittacidae). Rev Chil Hist Nat 70:269–275Google Scholar
  17. Fite KV, Rosenfield-Wessels S (1975) A comparative study of deep avian foveas. Brain Behav Evol 12:97–115PubMedGoogle Scholar
  18. Funke K (1989) Somatosensory areas in the telencephalon of the pigeon. I. Response characteristics. Exp Brain REs 76:603–619PubMedCrossRefGoogle Scholar
  19. Garland T Jr, Harvey PH, Ives AR (1992) Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst Biol 41:18–32CrossRefGoogle Scholar
  20. Garamszegi LZ, Moller AP, Erritzoe J (2002) Coevolving avian eye size and brain size in relation to prey capture and nocturnality. Proc R Soc Lond B 269:961–967CrossRefGoogle Scholar
  21. Güntürkün O, Hahmann U (1999) Functional subdivisions of the ascending visual pathways in the pigeon. Behav Brain Res 98:193–201PubMedCrossRefGoogle Scholar
  22. Hall MI, Ross CF (2007) Eye shape and activity pattern in birds. J Zool 271:437–444CrossRefGoogle Scholar
  23. Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology. Oxford University Press, OxfordGoogle Scholar
  24. Heesy CP (2003) The evolution of orbit orientation in mammals and the function of the primate postorbital bar. PhD Dissertation, Stony Brook University, Stony BrookGoogle Scholar
  25. Heesy CP (2004) On the relationship between orbit orientation and binocular visual field overlap in mammals. Anat Rec 281A:1104–1110CrossRefGoogle Scholar
  26. Howland HC, Merola S, Basarab JR (2004) The allometry and scaling of the size of vertebrate eyes. Vis Res 44:2043–2065PubMedCrossRefGoogle Scholar
  27. Husband S, Shimizu T (2001) Evolution of the avian visual system. In: Cook RG (ed) Avian visual cognition. http://www.pigeon.psy.tufts.edu/avc/husband/
  28. Iwaniuk AN, Hurd PL (2005) A multivariate analysis of cerebrotypes in birds. Brain Behav Evol 65:215–230PubMedCrossRefGoogle Scholar
  29. Iwaniuk AN, Nelson JE (2002) Can endocranial volume be used as an estimate of brain size in birds? Can J Zool 80:16–23CrossRefGoogle Scholar
  30. Iwaniuk AN, Nelson JE (2001) A comparative analysis of relative brain size in waterfowl (Anseriformes). Brain Behav Evol 57:87–97PubMedCrossRefGoogle Scholar
  31. Iwaniuk AN, Wylie DRW (2006) The evolution of stereopsis and the Wulst in caprimulgiform birds: a comparative analysis. J Comp Physiol A 192:1313–1326CrossRefGoogle Scholar
  32. Iwaniuk AN, Dean KM, Nelson JE (2004) A mosaic pattern characterizes the evolution of the avian brain. Proc R Soc Lond B 271:S148–S151CrossRefGoogle Scholar
  33. Iwaniuk AN, Dean KM, Nelson JE (2005) Interspecific allometry of the brain and brain regions in parrots (Psittaciformes): comparisons with other birds and primates. Brain Behav Evol 65:40–59PubMedCrossRefGoogle Scholar
  34. Karten HJ, Hodos W, Nauta WJH, Revzin AM (1973) Neural connections of the ‘visual Wulst’ of the avian telencephalon: Experimental studies in the pigeon (Columba livia) and owl (Speotyto cunicularia). J Comp Neurol 150:253–278PubMedCrossRefGoogle Scholar
  35. Katzir G, Martin GR (1994) Visual fields in herons (Ardeidae)—panoramic vision beneath the bill. Naturwissenschaften 81:182–184Google Scholar
  36. Katzir G, Martin GR (1998) Visual fields in the Black-crowned Night Heron Nycticorax nycticorax: nocturnality does not result in owl-like features. Ibis 140:157–162Google Scholar
  37. Kaye M, Mitchell DE, Cynader M (1981) Depth perception, eye alignment and cortical ocular dominance of dark-reared cats. Brain Res 254:37–53PubMedGoogle Scholar
  38. Kimball RT, Braun EL, Zwartjes PW, Crowe TM, Ligon JD (1999) A molecular phylogeny of the pheasants and partridges suggests that these lineages are not monophyletic. Mol Phylogenet Evol 11:38–54PubMedCrossRefGoogle Scholar
  39. Knudsen EI (1982) Auditory and visual maps of space in the optic tectum of the owl. J Neurosci 2:1177–1194PubMedGoogle Scholar
  40. Knudsen EI (1984) Auditory properties of space-tuned units in owl’s optic tectum. J Neurophysiol 52:709–723PubMedGoogle Scholar
  41. Knudsen EI (2002) Instructed learning in the auditory localization pathway of the barn owl. Nature 417:322–328PubMedCrossRefGoogle Scholar
  42. Krutzfeldt NO, Wild JM (2005) Definition and novel connections of the entopallium in the pigeon (Columba livia). J Comp Neurol 490:40–56PubMedCrossRefGoogle Scholar
  43. Land MF (1980) Optics and vision in invertebrates. In: Antrum H (ed) Handbook of sensory physiology VII/6B. Springer, Berlin, pp 471–592Google Scholar
  44. Land MF, Nilsson D-E (2002) Animal eyes. Oxford University Press, New YorkGoogle Scholar
  45. Lewald J, Dorrscheidt GJ (1998) Spatial-tuning properties of auditory neurons in the optic tectum of the pigeon. Brain Res 790:339–342PubMedCrossRefGoogle Scholar
  46. Livezey BC, Zusi RL (2007) Higher-order phylogeny of modern birds (Theropoda, Aves: Neornithes) based on comparative anatomy. II. Analysis and discussion. Zool J Linn Soc 149:1–95CrossRefPubMedGoogle Scholar
  47. Lockwood CA, Lynch JM, Kimbel WH (2002) Quantifying temporal bone morphology of great apes and humans: an approach using geometric morphometrics. J Anat 201:447–464PubMedCrossRefGoogle Scholar
  48. Maddison WP, Maddison DR (2006) Mesquite: a modular system for evolutionary analysis. Version 1.12. http://mesquiteproject.org
  49. Manger PR, Elston GN, Pettigrew JD (2002) Multiple maps and activity-dependent representational plasticity in the anterior Wulst of the adult barn owl (Tyto alba). Eur J Neurosci 16:743–750PubMedCrossRefGoogle Scholar
  50. Martin GR (1984) The visual fields of the tawny owl (Strix aluco). Vis Res 24:1739–1751PubMedCrossRefGoogle Scholar
  51. Martin GR (1986) Total panoramic vision in the mallard duck, Anas platyrhynchos. Vis Res 26:1303–1305PubMedCrossRefGoogle Scholar
  52. Martin GR (1993) Producing the image. In: Zeigler HP, Bischof H-J (eds) Vision, brain, and behavior in birds. MIT, Cambridge, pp 5–24Google Scholar
  53. Martin GR (1994) Visual fields in woodcocks Scolopax rusticola (Scolopacidae; Charadriiformes). J Comp Physiol A 174:787–793CrossRefGoogle Scholar
  54. Martin GR (1999) Optical structure and visual fields in birds: their relationship with foraging behaviour and ecology. In: Archer SN, Djamgoz MBA, Loew ER, Partridge JC, Vallerga S (eds) Adaptive mechanisms in the ecology of vision. Kluwer, Norwell, pp 485–508Google Scholar
  55. Martin GR, Coetzee HC (2004) Visual fields in hornbills: precision-grasping and sunshades. Ibis 146:18–26CrossRefGoogle Scholar
  56. Martin GR, de Brooke ML (1991) The eye of a procellariiform seabird, the Manx shearwater, Puffinus puffinus: visual fields and optical structure. Brain Behav Evol 37:65–78PubMedCrossRefGoogle Scholar
  57. Martin GR, Katzir G (1999) Visual fields in short-toed eagles, Circaetus gallicus (Accipitridae), and the function of binocularity in birds. Brain Behav Evol 53:55–66PubMedCrossRefGoogle Scholar
  58. Martin GR, Rojas LM, Figueroa YMR, McNeil R (2004a) Binocular vision and nocturnal activity in oilbirds (Steatornis caripensis) and parauques (Nyctidromus albicollis): Caprimulgiformes. Orn Neotrop 15:233–242Google Scholar
  59. Martin GR, Rojas LM, Ramirez Y, McNeil R (2004b) The eyes of oilbirds (Steatornis caripensis): pushing at the limits of sensitivity. Naturwiss 91:26–29PubMedCrossRefGoogle Scholar
  60. Martin GR, Young SR (1984) The eye of the Humboldt penguin, Spheniscus humboldti: visual fields and schematic optics. Proc R Soc Lond B 223:197–222PubMedGoogle Scholar
  61. Martinoya C, LeHouezec J, Bloch S (1984) Pigeon’s eyes converge during feeding: evidence for frontal binocular fixation in a lateral-eyed bird. Neurosci Lett 45:335–339PubMedCrossRefGoogle Scholar
  62. Mayr G (2002) Osteological evidence for paraphyly of the avian order Caprimulgiformes (nightjars and allies). J Ornithol 143:82–97CrossRefGoogle Scholar
  63. McFadden SA, Wild JM (1986) Binocular depth perception in the pigeon. J Exp Anal Behav 45:149–160PubMedCrossRefGoogle Scholar
  64. McNeil R, McSween A, Lachapelle P (2005) Comparison of the retinal structure and function in four bird species as a function of the time they start singing in the morning. Brain Behav Evol 65:202–214PubMedCrossRefGoogle Scholar
  65. Medina L, Reiner A (2000) Do birds possess homologues of mammalian primary visual, somatosensory and motor cortices? Trends Neurosci 23:1–12PubMedCrossRefGoogle Scholar
  66. Miceli D, Gioanni H, Repérant J, Peyrichoux J (1979) The avian visual Wulst: I. An anatomical study of afferent and efferent pathways. II. An electrophysiological study of the functional properties of single neurons. In: Granda AM, Maxwell JH (eds) Neural mechanisms of behavior in birds. Plenum Press, New York, pp 223–354Google Scholar
  67. Murphy CJ, Howland HC (1987) The optics of comparative ophthalmology. Vis Res 27:599–607PubMedCrossRefGoogle Scholar
  68. Nguyen AP, Spetch ML, Crowder NA, Winship IR, Hurd PL, Wylie DR (2004) A dissociation of motion and spatial-pattern vision in the avian telencephalon: implications for the evolution of “visual streams”. J Neurosci 24:4962–4970PubMedCrossRefGoogle Scholar
  69. Pettigrew JD (1978) Comparison of the retinotopic organization of the visual wulst in nocturnal and diurnal raptors, with a note on the evolution of frontal vision. In: Cool SJ, Smith EL (eds) Frontiers in visual science. Springer, New York, pp 328–335Google Scholar
  70. Pettigrew JD (1979) Binocular visual processing in the owl’s telencephalon. Proc R Soc Lond, B 204:435–454Google Scholar
  71. Pettigrew JD, Konishi M (1976a) Neurons selective for orientation and binocular disparity in the visual Wulst of the barn owl (Tyto alba). Science 193:675–678PubMedCrossRefGoogle Scholar
  72. Pettigrew JD, Konishi M (1976b) Effect of monocular deprivation on binocular neurons in the owl’s visual Wulst. Nature 264:753–754PubMedCrossRefGoogle Scholar
  73. Pettigrew JD, Konishi M (1984) Some observations on the visual system of the oilbird, Steatornis caripensis. Nat Geo Soc Res Rep 16:439–450Google Scholar
  74. Proctor NS, Lynch PJ (1993) Manual of ornithology: avian structure and function. Yale University Press, New HavenGoogle Scholar
  75. Reep RL, Finlay BL, Darlington RB (2007) The limbic system in mammalian brain evolution. Brain Behav Evol 70:57–70PubMedCrossRefGoogle Scholar
  76. Rehkämper G, Frahm HD, Zilles K (1991) Quantitative development of brain and brain structures in birds (Galliformes and Passeriformes) compared to that in mammals (insectivores and primates). Brain Behav Evol 37:125–143PubMedCrossRefGoogle Scholar
  77. Reiner A, Yamamoto K, Karten HJ (2005) Organization and evolution of the avian forebrain. Anat Rec A 287:1080–1102Google Scholar
  78. Ritland S (1982) The allometry of the vertebrate eye. PhD Thesis, University of Chicago, ChicagoGoogle Scholar
  79. Sheldon FH, Jones CE, McCracken KG (2000) Relative patterns and rates of evolution in heron nuclear and mitochondrial DNA. Mol Biol Evol 17:437–450PubMedGoogle Scholar
  80. Shimizu T, Karten HJ (1993) The avian visual system and the evolution of the neocortex. In: Zeigler HP, Bischof HJ (eds) Vision, brain and behavior in birds. MIT, Cambridge, pp 103–114Google Scholar
  81. Sibley CG, Ahlquist JE (1990) Phylogeny and classification of birds. Yale University Press, New HavenGoogle Scholar
  82. Steinbach MJ, Money KE (1973) Eye movements of the owl. Vis Res 13:889–891PubMedCrossRefGoogle Scholar
  83. Steinbach MJ, Angus RG, Money KE (1974) Torsional eye movements of the owl. Vis Res 14:745–746PubMedCrossRefGoogle Scholar
  84. Stevens KA (2006) binocular vision in theropod dinosaurs. J Vert Paleontol 26:321–330CrossRefGoogle Scholar
  85. Wallman J, Pettigrew JD (1985) Conjugate and disjunctive saccades in two avian species with contrasting oculomotor strategies. J Neurosci 5:1418–1428PubMedGoogle Scholar
  86. Whiting BA, Barton RA (2003) The evolution of the cortico-cerebellar complex in primates: anatomical connections predict patterns of correlated evolution. J Hum Evol 44:3–10PubMedCrossRefGoogle Scholar
  87. Wild JM (1997) The avian somatosensory system: the pathway from wing to Wulst in a passerine (Chloris chloris). Brain Res 759:122–134PubMedCrossRefGoogle Scholar
  88. Wild JM, Williams MN (2000) Rostral wulst in passerine birds. I. Origin, course, and terminations of an avian pyramidal tract. J Comp Neurol 416:429–450PubMedCrossRefGoogle Scholar
  89. Wilson P (1980) The organization of the visual hyperstriatum in the domestic chick. II. Receptive field properties of single units. Brain Res 188:333–345PubMedCrossRefGoogle Scholar
  90. Wylie DR, Frost BJ (1990) Binocular neurons in the nucleus of the basal optic root (nBOR) of the pigeon are selective for either translational or rotational visual flow. Visual Neurosci 5:489–495CrossRefGoogle Scholar
  91. Wylie DR, Shaver SW, Frost BJ (1994) The visual response properties of neurons in the nucleus of the basal optic root of the northern saw-whet owl (Aegolius acadicus). Brain Behav Evol 43:15–25PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Andrew N. Iwaniuk
    • 1
    Email author
  • Christopher P. Heesy
    • 2
  • Margaret I. Hall
    • 3
  • Douglas R. W. Wylie
    • 1
    • 4
  1. 1.Department of PsychologyUniversity of AlbertaEdmontonCanada
  2. 2.Department of AnatomyMidwestern UniversityGlendaleUSA
  3. 3.Department of Biomedical SciencesMidwestern UniversityGlendaleUSA
  4. 4.Centre for NeuroscienceUniversity of AlbertaEdmontonCanada

Personalised recommendations