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Distribution of calcium-binding proteins parvalbumin and calbindin in the thalamic auditory center in pigeons

  • Morphological Basics for Evolution of Functions
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Abstract

Distribution of calcium-binding proteins (CaBPr) parvalbumin (PV) and calbindin (CB) in the thalamic auditory center (nucleus ovoidalis, Ov) was studied in the pigeon (Columba livia). Two parts of Ov were distinguished on the basis of their cytoarchitectonics and distribution of PV and CB immunoreactivity. The central lemniscal region (core, nCe) contains both dense PV-ir neuropil and PV-ir neurons overlapped with scant CB-ir neuropil and weaker stained CB-ir neurons. The peripheral extralemniscal region (belt), consisting of peri/paraovoidal nuclei (Ovl, Ovm, SPO), contains only CB-ir neuropil and strongly stained CB-ir neurons morphologically differing from CB-ir neurons in the nCe. A comparative analysis of our data on the distribution of PV and CB immunoreactivity in the thalamic auditory relay center in pigeons and related literature data obtained on other avian, reptilian and mammalian species indicates high evolutionary conservatism of its extralemniscal region across all sauropside amniotеs and mammals in contrast to plasticity of its central lemniscal region due to adaptive, ecologically dependent transformations during the evolution.

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Abbreviations

CaBPr:

calcium-binding proteins

CB:

calbindin

CO:

cytochrome oxidase

DMP:

nucleus dorsomedialis posterior

ir:

immunoreactive

MGB:

corpus geniculatus medialis

MLD:

nucleus mesencephalicus lateralis, pars dorsalis

L:

telencephalic auditory field

L2:

central lamina of Field L

L1, L3:

peripheral laminae of Field L

nCe:

nucleus centralis Ov

Ov:

nucleus ovoidalis

Ovl:

nucleus lateralis Ov

Ovm:

nucleus medialis Ov

PV:

parvalbumin

Rot:

nucleus rotundus

SPO:

nucleus semilunaris paraovoidalis

SRt:

nucleus subrotundus

tOv:

tractus ovoidalis

References

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

    Article  CAS  Google Scholar 

  2. Grothe, B., Carr, C.E., Casseday, J.H., Fritzsch, B., and Köppl, C., The evolution of central pathways and their neural processing patterns, Evolution of the Vertebrate Auditory System, New York, 2004, pp. 289–359.

    Chapter  Google Scholar 

  3. Braun, K., Scheich, H., Schachner, M., and Heizmann, C.W., Distribution of parvalbumin, cytochrome oxidase activity and 14 C-2-desoxyglucose uptake of the zebra finch. I. Auditory and vocal motor systems, Cell Tissue Res., 1985, vol. 240, pp. 101–115.

    CAS  Google Scholar 

  4. Heizmann, C.W. and Braun, K., Calcium binding proteins. Molecular and functional aspects, The Role of Calcium in Biological Systems, Roca Raton, 1990, pp. 21–65.

    Google Scholar 

  5. Celio, M.R., Calbindin D-28k and parvalbumin in the rat nervous system, Neurosci., 1990, vol. 35, pp. 375–475.

    Article  CAS  Google Scholar 

  6. Vater, M. and Braun, K., Parvalbumin, calbindin D-28k and calretinin immunoreactivity in the ascending auditory pathway of horseshoe bats, J. Comp. Neurol., 1994, vol. 341, pp. 534–558.

    CAS  PubMed  Google Scholar 

  7. Zeng, S.J., Lin, Y.T., Yang, L., Zhang, X.W., and Zuo, M.X., Comparative analysis of neuronogenesis between core and shell regions in the chick (Gallus gallus domesticus), Brain Res., 2008, vol. 1216, pp. 24–37.

    Article  CAS  PubMed  Google Scholar 

  8. Belekhova, M.G., Chudinova, T.V., Repérant, J., Ward, R., Bruno, J.B., Vesselkin, N.P., and Kenigfest, N.B., Core-and-belt organisation of the mesencephalic and forebrain auditory centres in turtles: expression of calcium-binding proteins and metabolic activity, Brain Res., 2010, vol. 13, pp. 84–102.

    Article  Google Scholar 

  9. Yan, K., Tang, Y.-Z., and Carr, C.E., Calciumbinding protein immunoreactiviry characterizes the auditory system of Gekko gecko, J. Comp. Neurol., 2010, vol. 518, pp. 3409–3426.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Belekhova, M.G., Chudinova, T.V., Kenigfest, N.B., and Krasnoshchekova, E.I., Distribution of metabolic activity (cytochrome oxidase) and immunoreactivity to calcium-binding proteins in the turtle brainstem auditory nuclei, Zh. Evol. Biokhim. Fiziol., 2008, vol. 44, pp. 302–310.

    CAS  PubMed  Google Scholar 

  11. Belekhova, M.G., Kenigfest, N.B., Chudinova, T.V., and Vesselkin, N.P., Distribution of calcium-binding proteins parvalbumin and calbindin in the pigeon mesencephalic auditory center, Dokl. RAN, 2016, vol. 466, pp. 361–365.

    Google Scholar 

  12. Chudinova, T.V., Belekhova, M.G., Tostivint, E., Rio, J.-P., Ward, R., and Kenigfest, N.B., Differences in CB- and PV-chemospecificity in the centres of the ascending auditory pathway of turtles revealed by double immunofluorescence labeling, Brain Res., 2012, vol. 1473, pp. 87–103.

    Article  CAS  PubMed  Google Scholar 

  13. Braun, K., Scheich, H., Heizmann, C.W., and Hunziker, W., Parvalbumin and calbindin-D-28k immunoreactivity as developmental markers of auditory and vocal motor nuclei of the zebra finch, Neurosci., 1991, vol. 40, pp. 853–869.

    Article  CAS  Google Scholar 

  14. Pinaud, R., Saldanha, C.J., Wynne, R.D., Lovell, P.V., and Mello, C.V., The excitatory thalamo-“ cortical” projection within the song control system of zebra finches is formed by calbindin-expressing neurons, J. Comp. Neurol., 2007, vol. 504, pp. 601–618.

    Article  PubMed  Google Scholar 

  15. 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 

  16. Belekhova, M.G., Kenigfest, N.B., Minakova, M.N., Rio, J.-P., and Repérant, J., Calciumbinding proteins in the turtle thalamus. An analysis in the light of hypothesis of the “core–matrix” thalamic organization in relation to the problem of homology of thalamic nuclei among amniotes, Zh. Evol. Biokhim. Fiziol., 2003, vol. 39, pp. 504–523.

    CAS  PubMed  Google Scholar 

  17. Belekhova, M.G., Chudinova, T.V., Rio, J.-P., Tostivint, H., Vesselkin, N.P., and Kenigfest, N.B., Distribution of calcium-binding proteins in visual thalamic nuclei and related pretectal, mesencephalic nuclei in pigeons. Phylogenetic and functional determinating factors, Brain Res., 2016, vol. 1631, pp. 165–193.

    CAS  Google Scholar 

  18. Karten, H.J., The ascending auditory pathway in the pigeon (Columba livia). II. Telencephalic projections of the nucleus ovoidalis thalami, Brain Res., 1968, vol. 11, pp. 134–163.

    Article  CAS  PubMed  Google Scholar 

  19. Durand, S.E., Tepper, J.M., and Cheng, M.F., The shell region of the nucleus ovoidalis: a subdivision of avian auditory thalamus, J. Comp. Neurol., 1992, vol. 323, pp. 495–518.

    Article  CAS  PubMed  Google Scholar 

  20. Wild, J.M., Karten, H.J., and Frost, B.J., Connections of the auditory forebrain in the pigeon (Columba livia), J. Comp. Neurol., 1993, vol. 337, pp. 32–62.

    Article  CAS  PubMed  Google Scholar 

  21. Cheng, M.F. and Zuo, M.X., Proposed pathway for vocal self-stimulation: met-enkephalinergic projections linking the midbrain vocal nucleus, auditory responsive thalamic regions and neurosecretory hypothalamus, J. Neurobiol., 1994, vol. 25, pp. 361–379.

    CAS  PubMed  Google Scholar 

  22. Vates, G.E., Broome, B.M., Mello, C.V., and Nottebohm, F., Auditory pathways of caudal telencephalon and their relation to the song system of adult male zebra finch, J. Comp. Neurol., 1996, vol. 366, pp. 613–642.

    Article  CAS  PubMed  Google Scholar 

  23. Cheng, M.F. and Peng, J.P., Reciprocal call between the auditory thalamus and the hypothalamus: an antidromic study, Neuroreport, 1997, vol. 8, pp. 653–658.

    Article  CAS  PubMed  Google Scholar 

  24. Lanuza, E., Davies, D.C., Landete, J.M., Novejarque, A., and Martinez-Garcia, F., Distribution of CGRP-like immunoreactivity in the chick and quail brain, J. Comp. Neurol., 2000, vol. 421, pp. 515–532.

    Article  CAS  PubMed  Google Scholar 

  25. Zeng, S., Zhang, X., Peng, W., and Zuo, M.X., Immunohistochemistry and neural connectivity of the Ov shell in song-bird and their evolutionary implications, J. Comp. Neurol., 2004, vol. 470, pp. 192–209.

    Article  PubMed  Google Scholar 

  26. Brauth, S.E., McHale, C.M., Brasher, C.A., and Dooling, R.J., Auditory pathways in the budgerigar. I. Thalamo-telencephalic projections, Brain Behav. Evol., 1987, vol. 30, pp. 174–199.

    Article  CAS  PubMed  Google Scholar 

  27. Proctor, L. and Konishi, M., Representation of sound localization cues in the auditory thalamus of the barn owl, Proc. Nat. Acad. Sci. USA, 1997, vol. 94, pp. 10421–10425.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Medina, L. and Reiner, A., The efferent projections of the dorsal and ventral pallidal parts of the pigeon basal ganglia, studied with biotynilated dextran amine, Neuroscience, 1987, vol. 81, pp. 773–802.

    Google Scholar 

  29. Brauth, S.E., Investigation of central auditory nuclei in the budgerigar with cytochrome oxidase histochemistry, Brain Res., 1990, vol. 508, pp. 142–146.

    Article  CAS  PubMed  Google Scholar 

  30. Belekhova, M.G., Chudinova, T.V., and Kenigfest, N.B., Metabolic activity of pigeon thalamic and telencephalic auditory centers, Zh. Evol. Biokhim. Fiziol., 2009, vol. 45, pp. 512–517.

    Google Scholar 

  31. Brauth, S.E., Liang, W, and Hall, W.S., Contactcall driven and tone-driven zenk expression in the nucleus ovoidalis of the budgerigar (Melopsittacus undulatus), Neuroreport, 2006, vol. 17, pp. 1407–1410.

    Article  PubMed  Google Scholar 

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Correspondence to M. G. Belekhova.

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Original Russian Text © M.G. Belekhovа, T.V. Chudinova, N.B. Kenigfest, 2016, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2016, Vol. 52, No. 6, pp. 429—435.

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Belekhova, M.G., Chudinova, T.V. & Kenigfest, N.B. Distribution of calcium-binding proteins parvalbumin and calbindin in the thalamic auditory center in pigeons. J Evol Biochem Phys 52, 482–489 (2016). https://doi.org/10.1134/S1234567816060070

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  • DOI: https://doi.org/10.1134/S1234567816060070

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