Calcium-Binding Proteins and Cytochrome Oxidase Activity in the Pigeon Entopallium: A Comparative Analysis of Interspecies Variability as Related to the Discussion on Avian Entopallium Homology

  • M. G. Belekhova
  • D. S. Vasilyev
  • N. B. Kenigfest
  • T. V. Chudinova
Morphological Basics for Evolution of Functions


We report the results of our studies of the distribution patterns of calcium-binding proteins (parvalbumin, PV, and calbindin, CB) and metabolic activity (cytochrome oxidase, CO) in the pigeon entopallium—the telencephalic projection field of the tectofugal visual system. These characteristics were comparatively analyzed in different avian species in the light of the recent revision of entopallial projections’ nomenclature (Krützfeldt and Wild, 2005). We demonstrate that in the pigeon neuropil both high PV immunoreactivity and CO activity as well as lower CB immunoreactivity are confined to the core region of the entopallium (E). The latter contains cells immunoreactive (ir) to PV and CB and having a heterogenous repertoire: small/medium-sized granular and large multipolar cells. They overlap in E and partly colocalize within the same cell, but differ in the internal (Ei) and external (Ex) portions by distribution density and labeling intensity. CO activity was identified in both cellular morphotypes. Sparse PV- and CB-ir cells were found in the perientopallium (Ep). The interspecies variability of PV and CB immunoreactivity, described in the avian entopallium by other authors, indicates its dependence on the adaptive functional specialization which underlies selective expression of these calcium-binding proteins. The above as well as the pertinent literature data are discussed in the wake of the current discussion on homology of the avian entopallium, supporting the idea of the existence in sauropsid amniotes of the ancestral precursor of the mammalian extrastriate visual cortex.


pigeon tectofugal visual system entopallium parvalbumin calbindin cytochrome oxidase birds entopallium homology 


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  1. 1.
    Braun, K., Scheich, H., Schachner, M., and Heizmann, C.W., Distribution of parvalbumin, cytochrome oxidase activity and [14C] 2-deoxyglucose uptake in the brain zebra finch II. Visual system, Cell Tissue Res., 1985, vol. 240, pp. 117–127.Google Scholar
  2. 2.
    Heizmann, C.W. and Braun, K., Calcium-binding proteins: molecular and functional aspects, The Role of Calcium in Biological Systems, Roca Raton, FL, 1990, pp. 21–65.Google Scholar
  3. 3.
    Johnson, J.K. and Casagrande, V.A., Distribution of calcium-binding proteins within the parallel visual pathways of a primate (Galago crassicaudatus), J. Comp. Neurol., 1995, vol. 356, pp. 238–260.CrossRefPubMedGoogle Scholar
  4. 4.
    Jones, E.G., Viewpoint: the core and matrix of thalamic organization, Neurosci., 1998, vol. 85, pp. 331–345.CrossRefGoogle Scholar
  5. 5.
    Husband, S.A. and Shimizu, T., Anatomical evidence for parallel processing within an avian collothalamic visual pathway, Abstr. Neurosci. Soc., 1999, vol. 23, p.172.Google Scholar
  6. 6.
    Soares, J.G.M., Botelho, E.P., and Gattas, R., Distribution of calbindin, parvalbumin and calretinin in the lateral geniculate nucleus and superior colliculus in Cebus apella monkeys, J. Chem. Neuroanat., 2001, vol. 22, pp. 139–146.CrossRefPubMedGoogle Scholar
  7. 7.
    Marin, G., Letelier, J.C., Henny, P., Sentis, E., Farfan, G., Fredes, F., Pohl, N., and Karten, H.J., Spatial organization of the pigeon tectorotundal pathway: an interdigitating topographic arrangement, J. Comp. Neurol., 2003, vol. 458, pp. 361–380.CrossRefPubMedGoogle Scholar
  8. 8.
    Heyers, D., Manns, M., Luksch, H., Gunturkun, O., and Mouritsen, H., Calcium-binding proteins label functional streams of the visual system in a songbid, Brain Res. Bull., 2008, vol. 75, pp. 324–335.CrossRefGoogle Scholar
  9. 9.
    Chudinova, T.V., Kenigfest, N.B., and Belekhova, M.G., Components of the pigeon tectothalamic visual pathway in the pigeon, revealed with aid of study of cytochrome oxidase and immunoreactivity to calcium-binding proteins, Zh. Evol. Biokhim. Fiziol., 2010, vol. 46, pp. 522–529.PubMedGoogle Scholar
  10. 10.
    Kenigfest, N.B. and Belekhova, M.G., Neurons visual thalamic centers of turtles, projecting upon the telencephalon, express different types of calcium-binding proteins: a combined immunohistochemical and tracer study, Zh. Evol. Biokhim. Fiziol., 2015, vol. 51, pp. 449–458.PubMedGoogle Scholar
  11. 11.
    Belekhova, M.G., Chudinova, T.V., Rio, J.-P., Tostivint, H., Vesselkin, N.P., and Kenigfest, N.B., Distribution of calcium-binding proteins in the visual thalamic nuclei and related pretectal and mesencephalic nuclei in pigeons. Phylogenetic and functional determinating factors, Brain Res., 2016, vol. 1631, pp. 165–193.CrossRefPubMedGoogle Scholar
  12. 12.
    Patton, T.B., An anatomical investigating of higher visual structures in the pigeon (Columba livia), PhD Diss., 2010.Google Scholar
  13. 13.
    Belekhova, M.G., Kenigfest, N.B., and Chudinova, T.V., Activity of cytochrome oxidase in centers of tectofugal and thalamofugal channels of the vi sual system of pigeon Columba livia, Zh. Evol. Biokhim. Fiziol., 2011, vol. 47, pp. 73–84.Google Scholar
  14. 14.
    Belekhova, M.G., Kenigfest, N.B., Chudinova, T.V., and Vesselkin, N.P., Homologous thalamic nuclei of the tectofugal visual system in reptiles and birds exhibit different immunoreactivity to calcium-binding proteins, Dokl. Akad. Nauk, 2012, vol. 445, pp. 221–225.Google Scholar
  15. 15.
    Manns, M., Freund, N., and Gunturkun, O., Development of the diencephalic relay structures of the visual thalamofugal system in pigeons, Brain Res. Bull., 2008, vol. 66, pp. 424–427.CrossRefGoogle Scholar
  16. 16.
    Karten, H.J. and Hodos, W., Telencephalic projections of the nucleus rotundus in the pigeon (Columba livia), J. Comp. Neurol., 1970, vol. 140, pp. 35–52.CrossRefPubMedGoogle Scholar
  17. 17.
    Benovitz, L.J. and Karten, J.H., The organization of the tectofugal visual pathway in the pigeon: anterograde transport study, J. Comp. Neurol., 1976, vol. 167, pp. 503–520.CrossRefGoogle Scholar
  18. 18.
    Watanabe, M., Ito, H., and Ikushima, M., Cytoarchitecture and ultrastructure of the avian ectostriatum: afferent terminals from the dorsal telencephalon and some nuclei in the thalamus, J. Comp. Neurol., 1985, vol. 236, pp. 241–257.CrossRefPubMedGoogle Scholar
  19. 19.
    Karten, H. J. and Shimizu, T., The origins of neocortex: connections and lamination as distinct events in evolution, J. Cogn. Neurosci., 1989, vol. 1, pp. 291–301.CrossRefPubMedGoogle Scholar
  20. 20.
    Husband, S. and Shimizu, T., Efferent projections of the ectostriatum in the pigeon (Columba livia), J. Comp. Neurol., 1999, vol. 406, pp. 329–345.CrossRefPubMedGoogle Scholar
  21. 21.
    Butler, A.B. and Hodos, W., Comparative Vertebrate Neuroanatomy. Evolution and Adaptation, 2nd ed., Hoboken, New Jersey, 2005.CrossRefGoogle Scholar
  22. 22.
    Shimizu, T., Patton, T.B., and Husband, S.A., Avian visual behavior and the organization of the telencephalon, Brain Behav. Evol., 2010, vol. 75, pp. 204–217.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Krutzfeldt, N.O. and Wild, M., Definition and connections of the entopallium in the pigeon (Columba livia), J. Comp. Neurol., 2005, vol. 490, pp. 40–56.CrossRefPubMedGoogle Scholar
  24. 24.
    Wong-Riley, M.T., Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry, Brain Res., 1979, vol. 171, pp. 11–28.CrossRefPubMedGoogle Scholar
  25. 25.
    Reiner, A., Yamamoto, K., and Karten, H.J., Organization and evolution of the avian forebrain, Anat. Rec., 2005, vol. 287, pp. 1080–1102.CrossRefGoogle Scholar
  26. 26.
    Hellmann, B., Waldman, C., and Gunturkun, O., Cytochrome oxidase activity reveals parcellation of the ectostriatum, Neuroreport, 1995, vol. 6, pp. 881–886.CrossRefPubMedGoogle Scholar
  27. 27.
    Theiss, C., Hellmann, B., and Gunturkun, O., The differential distribution of AMPA-receptor subunits in the tectofugal system of the pigeon, Brain Res., 1998, vol. 785, pp. 114–128.CrossRefPubMedGoogle Scholar
  28. 28.
    Krutzfeldt, N.O. and Wild, M., Definition and connections of the entopallium in the zebra finch (Taeniopygia guttata), J. Comp. Neurol., 2004, vol. 468, pp. 452–465.CrossRefPubMedGoogle Scholar
  29. 29.
    Fredes, F., Tapia, S., Letelier, J.C., Marin, G., and Mpodozis, J., Topographic arrangement of the rotundo-entopallial projection in the pigeon (Columba livia), J. Comp. Neurol., 2010, vol. 518, pp. 4342–4361.CrossRefPubMedGoogle Scholar
  30. 30.
    Suarez, J., Davila, J.C., Real, M.A., and Guirado, S., Distribution of GABA, calbindin and nitric oxide synthase in the developing chick entopallium, Brain Res. Bull., 2005, vol. 66, pp. 441–444.CrossRefPubMedGoogle Scholar
  31. 31.
    Roth, J., Baetens, D., Norman, A.W., and Garcia-Segura, L.M., Specific neurons in chick central nervous system stained with antibody against chick intestinal vitamin D-dependent calcium binding protein, Brain. Res., 1981, vol. 222, pp. 452–457.CrossRefPubMedGoogle Scholar
  32. 32.
    Tömböl, T., Maqloczky, Z., Stewart, M.G., and Csillag, A., The structure of chicken ectostriatum. I. Golgi study, J. Hirnforsch., 1988, vol. 29, pp. 525–546.PubMedGoogle Scholar
  33. 33.
    Tömböl, T., Edegi, G., and Nemeth, A., EM study on Phaseolus vulgaris lectin labelled terminals of rotunda fibers on GABA immunogold stained structures in chicken ectostriatum central, J. Hirnforsch., 1993, vol. 34, pp. 517–537.PubMedGoogle Scholar
  34. 34.
    Csillag, A., Bourne, R.C., Patel, S.N., Stewart, M.G., and Tömböl, T., Localization of GABA-like immunoreactivity in the ectostriatum of domestic chicks: GABA immunohistochemistry combined with Golgi impregnation, J. Neurocytol., 1989, vol. 18, pp. 369–379.CrossRefPubMedGoogle Scholar
  35. 35.
    Csillag, A., Large GABA cells of chick ectostriatum: anatomical evidence suggesting a double GABAergic disinhibitory mechanisms. An electron microscopic study, J. Neurocytol., 1991, vol. 20, pp. 518–528.CrossRefPubMedGoogle Scholar
  36. 36.
    Luksch, H., Cox, K., and Karten, H.J., Bottlebrush dendritic endings and large dendritic fields: motion-detecting neurons in the tectofugal pathway, J. Comp. Neurol., 1998, vol. 396, pp. 399–414.CrossRefPubMedGoogle Scholar
  37. 37.
    Hellmann, B. and Gunturkun, O., Structural organization of parallel information processing within the tectofugal visual system of the pigeon, J. Comp. Neurol., 2001, vol. 429, pp. 94–112.CrossRefPubMedGoogle Scholar
  38. 38.
    Laverghetta, A.V. and Shimizu, T., Organization of the ectostriatum based on afferent connections in the zebra finch (Taeniopygia guttata), Brain Res., 2003, vol. 963, pp. 101–112.CrossRefPubMedGoogle Scholar
  39. 39.
    Nguyen, A.P., Spetch, M.L., Crowder, N.A., Winship, I.R., and Wylie, D.R., A dissociation of motion and spatial-pattern vision in the avian telencephalon: implication for the evolution of “visual streams”, J. Neurosci., 2004, vol. 24, pp. 4962–4970.CrossRefPubMedGoogle Scholar
  40. 40.
    Wang, Y., Jang, S., and Frost, B., Visual processing in pigeon nucleus rotundus: luminance, color, motion, and looming subdivisions, Vis. Res., 1993, vol. 10, pp. 21–30.Google Scholar
  41. 41.
    Laverghetta, A.V. and Shimizu, T., Visual discrimination in the pigeon (Columba livia): effects of selective lesions of the nucleus rotundus, Neuroreport, 1999, vol. 10, pp. 981–985.CrossRefPubMedGoogle Scholar
  42. 42.
    Cook, R.G., Patton, T.B., and Shimizu, T., Functional segregation of the entopallium in pigeons, Philosophy, 2013, vol. 130, pp. 59–86.PubMedPubMedCentralGoogle Scholar
  43. 43.
    Bischof, H.J., Eckmeier, D., Keary, N., Lowel, S., Mayer, U., and Michael, N., Multiple visual representation in the visual Wulst of a laterally eyed bird, the zebra finch (Taeniopygia guttata), PLoS One, 2016, vol. 11. eO 154927. doi 10.137Google Scholar
  44. 44.
    Karten, H.J., The organization of the avian telencephalon and some speculations on the phylogeny of the amniote telencephalon, Ann. N.Y. Acad. Sci., 1969, vol. 167, pp. 164–179.CrossRefGoogle Scholar
  45. 45.
    Scarf, D., Stuart, M., Johnston, M., and Colombo, M., Visual response properties of neurons in four areas of the avian pallium, J. Comp. Physiol. A, 2016, vol. 202, pp. 235–245.CrossRefGoogle Scholar
  46. 46.
    Alpar, A. and Tömböl, T., Efferent connections of the ectostriatal core. An anterograde tracer study, Ann. Anat., 2000, vol. 182, pp. 101–110.CrossRefPubMedGoogle Scholar
  47. 47.
    Ahumada-Gallequillos, P., Fernandez, M., Marin, G., Letelier, J.C., and Mpodozis, J., Anatomical organization of the dorsal ventricular ridge 9n the chick (Gallus domesticus): layers and columns in the avian pallium, J. Comp. Neurol., 2015, vol. 523, pp. 2618–2636.CrossRefGoogle Scholar
  48. 48.
    Butler, A.B., Reiner, A., and Karten, H.J., Evolution of amniote pallium and origins of mammalian neocortex, Ann. N.Y. Acad. Sci., 2011, vol. 1225, pp. 14–27.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Dugas-Ford, J., Powell, J.J., and Ragsdale, C.W., Cell-type homologies and the origin of the neocortex, PNAS, 2012, vol. 109, pp. 16974–16979.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Atoji, Y. and Karin, M.R., Expression of the neocortical marker, RORβ, in the entopallium and field L2 of adult chicken, Neurosci. Lett., 2012, vol. 521, pp. 119–124.CrossRefPubMedGoogle Scholar
  51. 51.
    Reiner, A., You are who you talk with—a commentary on Dugas-Ford et al., PNAS, 2012, Brain Behav. Evol., 2013, vol. 81, pp. 146–149.CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Karten, H.J., Neocortical evolution: neocortical circuits arise independently of lamination, Curr. Biol., 2013, vol. 23, pp. R12–R15.CrossRefPubMedGoogle Scholar
  53. 53.
    Jarvis, E.D., Yu, J., Rivas, M.V., Horita, H., Feenders, G., and Whitney, O., et al., Global view of the functional molecular organization of the avian cerebrum: mirror images and functional columns, J. Comp. Neurol., 2013, vol. 521, pp. 3614–3665.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Karten, H.J., Vertebrate brains and evolutionary connectomics: on the origins of mammalian “neocortex”, Phil. Trans. R. Soc. B, 2015, vol. 370. doi: 10.1098/rstb.2015.0060Google Scholar
  55. 55.
    Dugas-Ford, J. and Ragsdale, C.W., Levels of homology and problem of neocortex, Ann. Rev. Neurosci., 2015, vol. 38, pp. 351–368.CrossRefPubMedGoogle Scholar
  56. 56.
    Wild, M. and Krutzfeldt, N.O.E., Neocortical-like organization of avian auditory “cortex”, Brain Behav. Evol., 2010, vol. 76, pp. 89–92.CrossRefPubMedGoogle Scholar
  57. 57.
    Bourne, J.A., Waarner, C.E., Upton, D.J., and Rosa, M.G.P., Chemoarchitecture of the middle temporal visual area in the marmoset monkey (Callithrix jacchus): laminar distribution of calcium-binding proteins (calbindin, parvalbunin), J. Comp. Neurol., 2007, vol. 500, pp. 832–849.CrossRefPubMedGoogle Scholar
  58. 58.
    Wong, P. and Kaas, J.H., Architectonic subdivisions of neocortex in the gray squirrel (Sciurus carolinensis), Anat. Rec., 2008, vol. 291, pp. 1301–1033.CrossRefGoogle Scholar
  59. 59.
    Wong, P. and Kaas, J.H., Architectonic subdivisions of neocortex in the galago (Otolemur garnetti), Anat. Rec., 2010, vol. 293, pp. 1033–1089.CrossRefGoogle Scholar
  60. 60.
    Kim, H.G., Gu, Y.N., Lee, K.P., Kim, C.W., Lee, J.W., Jeong, T.., and Jeon, C.J., Immunocytochemical localization of the calcium-binding proteins calbindin D 28k, calretinin and parvalbumin in bat visual cortex, Histol. Histopathol., 2016, vol. 31, pp. 317–327.PubMedGoogle Scholar
  61. 61.
    Hof, P.R., Glezer, T.T., Conde, F., Flagg, R.A., Rubin, M.B., Nimchinsky, E.A., Vogt Weweisenhorn, D.M., Cellular distribution of the calciumbinding proteins parvalbumin, calbindin and calretinin in the neocortex of mammals, J. Chem. Neuroanat., 1999, vol. 16, pp. 77–116.CrossRefPubMedGoogle Scholar
  62. 62.
    Kaas, J.H., Neocortex in early mammals and its subsequent variations, Ann. NY Acad. Sci., 2011.Google Scholar
  63. 63.
    Stacho, M., Ströckens, F., Xiao, Q., and Gunturkun, O., Functional organization of telencephalic visual association fields in pigeons, Behav. Brain Res., 2016, vol. 303, pp. 93–102.CrossRefPubMedGoogle Scholar
  64. 64.
    Puelles, L., Thoughts on the development, structure and evolution of the mammalian and avian telencephalon, Phil. Trans. R. Soc. Lond. B, 2001, vol. 356, pp. 1583–1598.CrossRefGoogle Scholar
  65. 65.
    Guirado, S., Real, M.A., and Davila, J.C., The ascending tectofugal visual system in amniotes: new insight, Brain Res. Bul., 2005, vol. 66, pp. 290–296.CrossRefGoogle Scholar
  66. 66.
    Striedter, G.F., Principles of Brain Evolution, Irvine, 2005, p.357.Google Scholar
  67. 67.
    Reiner, A.J., A hypothesis as to the organization of cerebral cortex in the common amniote ancestor of modern reptiles and mammals, Novarts Found. Symp., 2000, vol. 228, pp. 83–102.Google Scholar
  68. 68.
    Jarvis, C.D., Avian brains and a new understanding of vertebrate brain evolution, 2005, vol. 6, pp. 151–159.Google Scholar
  69. 69.
    Wada, K., Chen, C.-C., and Jarvis, E.J., Molecular profiling reveals insight into avian brain organization and functional columnar commonalities with mammals, Brain Evolution by Design, 2017, pp. 273–285.CrossRefGoogle Scholar
  70. 70.
    Butler, A.B. and Molnar, Z., Development and evolution of the collopallium in amniotes: a new hypothesis of field homology, Brain Res. Bull., 2002, vol. 57, pp. 475–479.CrossRefPubMedGoogle Scholar
  71. 71.
    Molnar, Z. and Butler, A.B., Neuronal changes during forebrain evolution in amniotes: an evolutionary developmental perspective, Progr. Brain Res., 2002, vol. 136, pp. 1–38.CrossRefGoogle Scholar
  72. 72.
    Chen, C.C., Winkler, C.M., Pfenning, A.R., and Jarvis, E.D., Molecular profiling of the developing avian telencephalon; regional timing and brain subdivision continuities, J. Comp. Neurol., 2013, vol. 521, pp. 3666–3701.CrossRefPubMedGoogle Scholar
  73. 73.
    Nomura, T., Murakami, J., Cotho, H., and Ono, K., Reconstruction of ancestral brains: exploring the evolutionary process of encephalization in amhiotes, Neurosci. Res., 2014, vol. 86, pp. 25–36.CrossRefPubMedGoogle Scholar
  74. 74.
    Nomura, T. and Hirata, T., The neocortex homologues in nonmammalian amniotes: bridging the hierarchical concepts of homology through comparative neurogenesis, Chapter in Evolution of Nervous System, Springer, 2017, pp. 195–204.CrossRefGoogle Scholar
  75. 75.
    Yamashita, W. and Nomura, T., The neocortex and dorsal ventricular ridge: functional convergence and underlying developmental mechanisms, Chapter in Bran Evolution and Design, 2017, Springer, pp. 291–309.CrossRefGoogle Scholar

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© Pleiades Publishing, Ltd. 2018

Authors and Affiliations

  • M. G. Belekhova
    • 1
  • D. S. Vasilyev
    • 1
  • N. B. Kenigfest
    • 1
  • T. V. Chudinova
    • 1
  1. 1.Sechenov Institute of Evolutionary Physiology and BiochemistryRussian Academy of SciencesSt. PetersburgRussia

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