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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

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Abstract

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.

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References

  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.

    CAS  Google Scholar 

  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. 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.

    Article  CAS  PubMed  Google Scholar 

  4. Jones, E.G., Viewpoint: the core and matrix of thalamic organization, Neurosci., 1998, vol. 85, pp. 331–345.

    Article  CAS  Google Scholar 

  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. 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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  12. Patton, T.B., An anatomical investigating of higher visual structures in the pigeon (Columba livia), PhD Diss., 2010.

    Google Scholar 

  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. 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. 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.

    Article  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  21. Butler, A.B. and Hodos, W., Comparative Vertebrate Neuroanatomy. Evolution and Adaptation, 2nd ed., Hoboken, New Jersey, 2005.

    Book  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  25. Reiner, A., Yamamoto, K., and Karten, H.J., Organization and evolution of the avian forebrain, Anat. Rec., 2005, vol. 287, pp. 1080–1102.

    Article  Google Scholar 

  26. Hellmann, B., Waldman, C., and Gunturkun, O., Cytochrome oxidase activity reveals parcellation of the ectostriatum, Neuroreport, 1995, vol. 6, pp. 881–886.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    CAS  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  42. Cook, R.G., Patton, T.B., and Shimizu, T., Functional segregation of the entopallium in pigeons, Philosophy, 2013, vol. 130, pp. 59–86.

    PubMed  PubMed Central  Google Scholar 

  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 10.137

    Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  Google Scholar 

  46. Alpar, A. and Tömböl, T., Efferent connections of the ectostriatal core. An anterograde tracer study, Ann. Anat., 2000, vol. 182, pp. 101–110.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Karten, H.J., Neocortical evolution: neocortical circuits arise independently of lamination, Curr. Biol., 2013, vol. 23, pp. R12–R15.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  PubMed  PubMed Central  Google Scholar 

  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.2015.0060

  55. Dugas-Ford, J. and Ragsdale, C.W., Levels of homology and problem of neocortex, Ann. Rev. Neurosci., 2015, vol. 38, pp. 351–368.

    Article  CAS  PubMed  Google Scholar 

  56. Wild, M. and Krutzfeldt, N.O.E., Neocortical-like organization of avian auditory “cortex”, Brain Behav. Evol., 2010, vol. 76, pp. 89–92.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  59. Wong, P. and Kaas, J.H., Architectonic subdivisions of neocortex in the galago (Otolemur garnetti), Anat. Rec., 2010, vol. 293, pp. 1033–1089.

    Article  Google Scholar 

  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.

    CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  62. Kaas, J.H., Neocortex in early mammals and its subsequent variations, Ann. NY Acad. Sci., 2011.

    Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  Google Scholar 

  66. Striedter, G.F., Principles of Brain Evolution, Irvine, 2005, p.357.

    Google Scholar 

  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.

    CAS  Google Scholar 

  68. Jarvis, C.D., Avian brains and a new understanding of vertebrate brain evolution, 2005, vol. 6, pp. 151–159.

    CAS  Google Scholar 

  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.

    Chapter  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Chapter  Google Scholar 

  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.

    Chapter  Google Scholar 

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Correspondence to M. G. Belekhova.

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Original Russian Text © M.G. Belekhova, D.S. Vasilyev, N.B. Kenigfest, T.V. Chudinova, 2018, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2018, Vol. 54, No. 1, pp. 60—72.

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Belekhova, M.G., Vasilyev, D.S., Kenigfest, N.B. et al. 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. J Evol Biochem Phys 54, 68–82 (2018). https://doi.org/10.1134/S0022093018010088

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