Brain, Behavior and Evolution

Original Paper

Comparative Morphology of the Avian Cerebellum: I. Degree of Foliation

Iwaniuk A.N.a · Hurd P.L.a · Wylie D.R.W.a, b

Author affiliations

aDepartment of Psychology, bCentre for Neuroscience, University of Alberta, Edmonton, Canada

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Brain Behav Evol 2006;68:45–62

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Article / Publication Details

First-Page Preview
Abstract of Original Paper

Received: October 27, 2005
Accepted: March 15, 2006
Published online: June 14, 2006
Issue release date: June 2006

Number of Print Pages: 18
Number of Figures: 6
Number of Tables: 5

ISSN: 0006-8977 (Print)
eISSN: 1421-9743 (Online)

For additional information: https://www.karger.com/BBE

Abstract

Despite the conservative circuitry of the cerebellum, there is considerable variation in the shape of the cerebellum among vertebrates. One aspect of cerebellar morphology that is of particular interest is the degree of folding, or foliation, of the cerebellum and its functional significance. Here, we present the first comprehensive analysis of variation in cerebellar foliation in birds with the aim of determining the effects that allometry, phylogeny and development have on species differences in the degree of cerebellar foliation. Using both conventional and phylogenetically based statistics, we assess the effects of these variables on cerebellar foliation among 91 species of birds. Overall, our results indicate that allometry exerts the strongest effect and accounts for more than half of the interspecific variation in cerebellar foliation. In addition, we detected a significant phylogenetic effect. A comparison among orders revealed that several groups, corvids, parrots and seabirds, have significantly more foliated cerebella than other groups, after accounting for allometric effects. Lastly, developmental mode was weakly correlated with relative cerebellar foliation, but incubation period and fledging age were not. From our analyses, we conclude that allometric and phylogenetic effects exert the strongest effects and developmental mode a weak effect on avian cerebellar foliation. The phylogenetic distribution of highly foliated cerebella also suggests that cognitive and/or behavioral differences play a role in the evolution of the cerebellum.

© 2006 S. Karger AG, Basel




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References

  1. Altshuler DL, Dudley R, McGuire JA (2004) Resolution of a paradox: hummingbird flight at high elevation does not come without a cost. Proc Nat Acad Sci USA 101:17731–17736.
  2. Barker FK, Cibois A, Schikler P, Feinstein J, Cracraft J (2004) Phylogeny and diversification of the largest avian radiation. Proc Nat Acad Sci USA 101:11040–11045.
  3. Bennett PM, Harvey PH (1985) Relative brain size and ecology in birds. J Zool 207:151–169.
  4. Bennett PM, Owens IPF (2002) Evolutionary Ecology of Birds: Life Histories, Mating Systems and Evolution. Oxford UK: Oxford University Press.
  5. Blomberg SP, Garland T Jr, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745.
  6. Böhning-Gaese K, Oberrath R (1999) Phylogenetic effects on morphological, life-history, behavioural and ecological traits of birds. Evol Ecol Res 1:347–364.
  7. Boire D, Baron G (1994) Allometric comparison of brain and main brain subdivisions in birds. J Hirnforsch 35:49–66.
  8. Bower JM (1997) Control of sensory data acquisition. Int Rev Neurobiol 41:489–513.
  9. Butler AB, Hodos W (1996) Comparative Vertebrate Neuroanatomy. New York: Wiley-Liss.
  10. Changizi MA (2001) Principles underlying mammalian neocortical scaling. Biol Cybern 84:207–215.
  11. Christidis L, Schodde R, Shaw DD, Maynes SF (1991) Relationships among the Australo-Papuan parrots, lorikeets and cockatoos (Aves: Psittaciformes). Condor 93:302–317.
  12. Day LB, Westcott DA, Olster DH (2005) Evolution of bower complexity and cerebellum size in bowerbirds. Brain Behav Evol 66:62–72.
  13. Deaner RO, Nunn CL, van Schaik CP (2000) Comparative tests of primate cognition: different scaling methods produce different results. Brain Behav Evol 55:44–52.
  14. Desmond JE, Fiez JA (1998) Neuroimaging studies of the cerebellum: language, learning and memory. Trends Cogn Sci 2:355–362.
  15. Ebinger P (1995) Domestication and plasticity of brain organization in mallards (Anas platyrhynchos). Brain Behav Evol 45:286–300.
  16. Ebinger P, Röhrs M (1995) Volumetric analysis of brain structures, especially of the visual system in wild and domestic turkeys (Meleagris gallopavo). J Brain Res 36:219–228.
  17. Faraway JJ (2005) Linear Models with R. Boca Raton FL: Chapman & Hall/CRC Press.
  18. Garland T Jr, Dickerman AW, Janis CM, Jones JA (1993) Phylogenetic analysis of covarianceby computer simulation. Syst Biol 42:265–292.
    External Resources
  19. Garland T Jr, Harvey PH, Ives AR (1992) Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst Biol 41:18–32.
    External Resources
  20. Gould SJ, Lewontin RC (1979) The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist program. Proc R Soc Lond B 205:581–598.
  21. Harrison KH, Hof PR, Wang SS-H (2002) Scaling laws in the mammalian neocortex: Does form provide clues to function? J Neurocytol 31:289–298.
  22. Harvey PH, Pagel MD (1991) The Comparative Method in Evolutionary Biology. Oxford UK: Oxford University Press.
  23. Hofman M (1985) Size and shape of the cerebral cortex in mammals. I. The cortical surface. Brain Behav Evol 27:28–40.
  24. Hutcheon JM, Kirsch JAW, Garland T Jr (2002) A comparative analysis of brain size in relation to foraging ecology and phylogeny in the Chiroptera. Brain Behav Evol 60:165–180.
  25. Imamizu H, Kuroda T, Miyauchi S, Yoshioka T, Kawato M (2003) Modular organization of internal models of tools in the human cerebellum. Proc Nat Acad Sci USA 100:5461–5466.
  26. Irwin RE (1996) The phylogenetic content of avian courtship display and song evolution. In: Phylogenies and the Comparative Method in Animal Behavior (Martin EP, ed), pp 234–252. Oxford UK: Oxford University Press.
  27. Ito M (1984) The Cerebellum and Neural Control. New York: Raven.
  28. Iwaniuk AN, Hurd PL (2005) A multivariate analysis of cerebrotypes in birds. Brain Behav Evol 65:215–230.
  29. Iwaniuk AN, Nelson JE (2002) Can endocranial volume be used as an estimate of brain size in birds? Can J Zool 80:16–23.
    External Resources
  30. Iwaniuk AN, Nelson JE (2003) Developmental differences are correlated with relative brain size in birds: A comparative analysis. Can J Zool 81:1913–1928.
    External Resources
  31. Iwaniuk AN, Clayton DH, Wylie DRW (2006a) Echolocation, vocal learning, auditory localization and the evolution of the avian inferior colliculus (MLd). Behav Brain Res 167:305–317.
  32. 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 65:40–59.
  33. Iwaniuk AN, Hurd PL, Wylie DRW (2006b) The comparative morphology of the cerebellum in caprimulgiform birds: evolutionary and functional implications.Brain Behav Evol 67:53–68.
  34. Johnson KP, McKinney F, Wilson R, Sorenson MD (2000) The evolution of postcopulatory displays in dabbling ducks (Anatini): a phylogenetic perspective. Anim Behav 59:953–963.
  35. Kalisinska E (2005) Anseriform brain and its parts versus taxonomic and ecological categories. Brain Behav Evol 65:244–261.
  36. Kennedy M, Spencer HG, Gray RD (1996) Hop, step and gape: Do the social displays of the Pelecaniformes reflect phylogeny? Anim Behav 51:273–291.
  37. 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 11:38–54.
  38. Klyachko VA, Stevens CF (2003) Connectivity optimization and the positioning of cortical areas. Proc Nat Acad Sci USA 100:7937–7941.
  39. Kretschmann H-J, Wingert F (1969) Biometrische Analyse der Volumina des Striatum einer ontogenetischen Reihe von Albinomäusen. Z Anat Entwicklungsgesch 128:85–108.
  40. Larsell O (1967) The Comparative Anatomy and Histology of the Cerebellum from Myxinoids through Birds. Minneapolis MN: University of Minnesota Press.
  41. Lefebvre L, Nicolakakis N, Boire D (2002) Tools and brains in birds. Behaviour 139:939–973.
  42. Lefevbre L, Reader SM, Sol D (2004) Brains, innovations and evolution in birds and primates. Brain Behav Evol 63:233–246.
  43. Legge S (2004) Kookaburra: King of the Bush. Collingwood: CSIRO Publishing.
  44. Matochik JA, Reems CN, Wenzel BM (1991) A brain atlas of the northern fulmar (Fulmarus glacialis) in stereotaxic coordinates. Brain Behav Evol 37:215–244.
  45. Monroe BL Jr, Sibley CG (1997) A World Checklist of Birds. New Haven CT: Yale University Press.
  46. Paulin MG (1993) The role of the cerebellum in motor control and perception. Brain Behav Evol 41:39–50.
  47. Pearson R, Pearson L (1976) The Vertebrate Brain. London: Academic Press.
  48. Pellis SM, Iwaniuk AN (2002) Brain system size and adult-adult play in primates: a comparative analysis of the roles of the non-visual neocortex and the amygdala. Behav Brain Res 134:31–39.
  49. Portmann A (1946) Études sur la cérébralisation chez les oiseaux. I. Alauda 14:2–20.
  50. Portmann A (1947) Études sur la cérébralisation chez les oiseaux. II. Les indices intra-cérébraux. Alauda 15:1–15.
  51. Price JJ, Lanyon SM (2002) Reconstructing the evolution of complex bird song in the oropendolas. Evolution 56:1514–1529.
  52. R Core Development Team (2004) R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.
  53. 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 37:125–143.
  54. Rilling JK, Insel TR (1999) The primate neocortex in comparative perspective using magnetic resonance imaging. J Hum Evol 37:191–223.
  55. Rodríguez F, Durán E, Gómez A, Ocaña FM, Ðvarez E, Jiménez-Moya F, Broglio C, Salas C (2005) Cognitive and emotional functions of the teleost fish cerebellum. Brain Res Bull 66:365–370.
  56. Senglaub K (1963) Das Kleinhirn der Vögel in Beziehung zu phylogenetischer Stellung, Lebensweise und Körpergrösse. Z Wiss Zool 169:1–63.
  57. Sherry DF, Vaccarino AL, Buckenham K, Herz RS (1989) The hippocampal complex of food-storing birds. Brain Behav Evol 34:308–317.
  58. Sibley CG, Ahlquist JE (1990) Phylogeny and Classification of Birds. New Haven CT: Yale University Press.
  59. Sol D, Lefebvre L, Rodriguez-Teijeiro JD (2005) Brain size, innovative propensity and migratory behaviour in temperate Palaearctic birds. Proc R Soc Lond B 272:1433–1441.
    External Resources
  60. Starck JM (1989) Zeitmuster der Ontogenesen bei nestflüchtenden und nesthockenden Vögeln. Cour Forschunginst Senckenb No. 114.
  61. Striedter GF (2004) Principles of Brain Evolution. Sunderland MA: Sinauer Associates.
  62. Sultan F (2002) Analysis of mammalian brain architecture. Nature 415:133–134.
  63. Sultan F (2005) Why some bird brains are larger than others. Curr Biol 15:R649–R650.
  64. Timmermans S, Lefebvre L, Boire D, Basu P (2000) Relative size of the hyperstriatum ventrale is the best predictor of feeding innovation rate in birds. Brain Behav Evol 56:196–203.
  65. Van Essen DC (1997) A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 385:313–318.
  66. Voogd J, Glickstein M (1998) The anatomy of the cerebellum. Trends Neurosci 21:370–375.
  67. Ward BC, Nordeen EJ, Nordeen KW (2001) Anatomical and ontogenetic factors producing variation in HVc neuron number in zebra finches. Brain Res 904:318–326.
  68. Weaver AN (2005) Reciprocal evolution of the cerebellum and neocortex in fossil humans. Proc Nat Acad Sci USA 102:3576–3580.
  69. Zilles K, Armstrong E, Moser KH, Schleicher A, Stephan H (1989) Gyrification in the cerebral cortex of primates. Brain Behav Evol 34:143–150.

Article / Publication Details

First-Page Preview
Abstract of Original Paper

Received: October 27, 2005
Accepted: March 15, 2006
Published online: June 14, 2006
Issue release date: June 2006

Number of Print Pages: 18
Number of Figures: 6
Number of Tables: 5

ISSN: 0006-8977 (Print)
eISSN: 1421-9743 (Online)

For additional information: https://www.karger.com/BBE


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