Skip to main content
SpringerLink
Log in

Distribution of calcium-binding proteins parvalbumin and calbindin in the pigeon telencephalic auditory center

  • Morphological Basics for Evolution of Functions
  • Published:
Journal of Evolutionary Biochemistry and Physiology Aims and scope Submit manuscript

Abstract

Immunoreactivity for calcium-binding proteins parvalbumin (PV) and calbindin (CB) was studied in the pigeon (Columba livia) telencephalic auditory center. All its regions displayed overlapping distribution patterns of PV and CB immunoreactivity, although in the central (L2) vs. peripheral (L1, L3, CMM) layers they were dissimilar. L2 and the inner L1 sublayer (L1i) were distinguished by a higher immunoreactivity of neuropil for both proteins and the presence (in L2) of numerous small densely packed granular-type cells: heavily stained PV-ir and, as a rule, poorly stained CB-ir neurons. In Lli, the number of neurons and the density of neuropil immunoreactive to both proteins decreased. The outer L1 sublayer (L1e) as well as L3 and CMM were characterized by a generally lesser density and irregular distribution of immunoreactive neuropil and a heterogenous repertoire of PV-ir and CB-ir neurons referring to diverse morphological types, with an increased number of large multipolar cells. The differences in PV and CB immunoreactivity among different regions of the pigeon telencephalic auditory center revealed the similarity of the latter to the laminar auditory cortex in mammals.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

СаВРr:

calcium-binding proteins

СВ:

calbindin

CLM:

mesopallium caudolaterale

CMM:

mesopallium caudomediale

СО:

cytochrome oxidase

DA:

tractus dorsoarcopallialis

ir:

immunoreactive

MGB:

corpus geniculatum mediale

MLD:

nucleus mesencephalicus lateralis, pars dorsalis

L:

telencephalic auditory field

L2:

L central layer

Lam:

lamina mesopallialis

L1, L3:

L peripheral layers

L1е:

L1 outer sublayer

L1i:

L1 inner sublayer

nCe:

nucleus centralis Ov

NCM:

nidopallium caudomediale

Ov:

nucleus ovoidalis

Ovl:

nucleus lateralis Ov

Ovm:

nucleus medialis Ov

PV:

parvalbumin

SPO:

nucleus semilunaris parovoidalis

References

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

    Google Scholar 

  2. Belekhova, M.G., Chudinova, T.V., and Kenigfest, N.B, Distribution of calcium-binding proteins parvalbumin and calbindin in the thalamic auditory center in pigeons, J. Evol. Biochem. Physiol., 2016, vol. 52, pp. 482–489.

    Article  CAS  Google Scholar 

  3. 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 

  4. 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 

  5. 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 

  6. 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 

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

    Article  CAS  Google Scholar 

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

    Google Scholar 

  9. 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 

  10. 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 

  11. 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 

  12. 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 

  13. 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 

  14. Elliott, T.M. and Theunissen, F.E, The Avian Auditory Pallium. Auditory Cortex, Springer, New York and oth., 2011, pp. 429–443.

    Google Scholar 

  15. Wang, Y., Brzozowska-Precht, H.J., and Karten, H.J, Laminar and column auditory cortex in avian brain, PNAS, 2010, vol. 107, pp. 12676–12681.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Prather, J.F, Auditory signal processing in communication: perception and performance of vocal sounds, Hearing Res., 2013, vol. 305, pp. 144–155.

    Article  Google Scholar 

  17. Karten, H.J, The organization of the avian telencephalon and some speculations on the phylogeny of the amniote telencephalon, Ann. NY Acad. Sci., 1969, vol. 167, pp. 164–179.

    Article  Google Scholar 

  18. Karten, H.J, Vertebrate brains and evolutionary connections: on the origins of the mammalian “neocortex”, Phil. Trans. Roy. Soc. B., 2015, vol. 370.0060.

    Google Scholar 

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

    Article  Google Scholar 

  20. Jarvis, E.D., Güntürkü n, O., Bruce, L.L., Csillag, A., Karten, H.J., Kuenzel, W., Medina, L., et al., Avian brains and a new understanding of vertebrate brain evolution, Nat. Rev. Neurosci., 2005, vol. 6, pp. 151–159.

    Article  CAS  PubMed  Google Scholar 

  21. Wild, J.M. and Krutzfeldt, N.O.E, Neocorticallike organization of avian auditory cortex, Brain Behav. Evol., 2010, vol. 76, pp. 89–92.

    Article  PubMed  Google Scholar 

  22. Butler, A.N., Reiner, A., and Karten, H.J, Evolution of amniote pallium and the origins of mammalian neocortex, Ann. N.Y. Acad. Sci., 2011, vol. 1225, pp. 14–27.

    Article  PubMed  PubMed Central  Google Scholar 

  23. 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 

  24. Reiner, A, You are who you talk with—a commentary on Dougas-Ford et al., PNAS, 2012, Brain Behav. Evol., 2013, vol. 81, pp. 146–149.

    PubMed  Google Scholar 

  25. Bruce, L.L., Kornblum, H.I., and Seroogy, K.B, Comparison of thalamic populations in mammals and birds: expression of ErbB4 mRNA, Brain Res. Bull., 2002, vol. 57, pp. 455–461.

    Article  CAS  PubMed  Google Scholar 

  26. Puelles, L, Thoughts on the development, structure and evolution of the mammalian and avian telencephalic pallium, Phil. Trans. Roy. Soc. B, 2001, vol. 356, pp. 1583–1598.

    CAS  Google Scholar 

  27. Striedter, G.F., Principles of Brain Evolution, University of California Press, Irvine, 2005.

    Google Scholar 

  28. De Venecia, R.K., Smelser, C.B., and McMullen, N.T, Parvalbumin is expressed in a reciprocal circuit linking the medial geniculate body and auditory neocortex in the rabbit, J. Comp. Neurol., 1998, vol. 400, pp. 349–362.

    Article  PubMed  Google Scholar 

  29. Cruikshank, S.J., Killackey, H.P., and Metherate, R, Parvalbumin and calbindin are differently distributed within primary and secondary subdivisions of the mouse auditory forebrain, Neurosci., 2000, vol. 105, pp. 553–569.

    Article  Google Scholar 

  30. Chiry, O., Tardif, E., Magistretti, P.J., and Clarke, S, Patterns of calcium-binding proteins support parallel and hierarchical organization of human auditory areas, Eur. J. Neurosci., 2003, vol. 17, pp. 397–410.

    Article  PubMed  Google Scholar 

  31. Desegent, S., Boire, D., and Ptito, M, Distribution of calcium binding proteins in visual and auditory cortices of hamster, Exp. Brain Res., 2005, vol. 163, pp. 159–172.

    Article  Google Scholar 

  32. Wong, P. and Kaas, J.H, Architectonic subdivisions of neocortex in Galago (Otolemur garnetti), Anat. Rec., 2010, vol. 293, pp. 1033–1069.

    Article  Google Scholar 

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

    Google Scholar 

  34. Fortune, E.S. and Margoliash, D, Cytoarchitectonic organization and morphology of cells of the field L complex in male zebra finches (Taenopigia guttata), J. Comp. Neurol., 1992, vol. 325, pp. 388–404.

    Article  CAS  PubMed  Google Scholar 

  35. Saini, K.D. and Leppelsack, H.J, Cell types of the auditory neostriatum of the starling (Sturnus vulgaris), J. Comp. Neurol., 1981, vol. 198, pp. 209–229.

    Article  CAS  PubMed  Google Scholar 

  36. 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 

  37. Bosman, C.A. and Aboitiz, F, Functional constraints in the evolution of brain circuits, Front. Neurosci., 2015, vol. 9, p. 303.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Calabrese, A. and Woolley, S.M.N, Coding principles of the canonical cortical microcircuits in tha avian brain, Proc. Natl. Acad. Sci. USA, 2015, vol. 112, pp. 3517–3522.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Harris, K.D, Cortical computation in mammals and birds, Proc. Natl. Acad. Sci., 2015, vol. 112, pp. 3184–3185.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Atoji, Y. and Karim, M.R, Expreßsion of the neocortical marker RORß in the entopallium and Field L2 of adult chicken, Neurosci. Lett., 2012, vol. 521, pp. 119–124.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  42. Pinaud, R. and Terleph, T.A., A songbird forebrain area potentially involved in auditory discrimination and memory formation, J. Biosci., 2008, vol. 33, pp. 145–155.

    Article  PubMed  Google Scholar 

  43. Meliza, C.D. and Margoliash, D, Emergence of selectivity and tolerance in the avian auditory cortex, J. Neurosci., 2012, vol. 32, pp. 15158–15168.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Krutzfeldt, N.O. and Wild, M, Definition and novel connections of the entopallium in the pigeon (Columba livia), J. Comp. Neurol., 2005, vol. 490, pp. 40–56.

    Article  PubMed  Google Scholar 

  45. Hof, P.R., Glezer, T.T., Conde, F., Flagg, R.A., Rubin, M.B., Nimchinsky, E.A., and Weisenhorn, D.M, Cellular distribution of the calcium-binding proteins parvalbumin, calbindin, and calretinin in the neocortex of mammals: phylogenetic and developmental patterns, J. Chem. Neuroanat., 1999, vol. 16, pp. 77–116.

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Sechenov Institute of Evolutionary Physiology and Biochemistry, Russian Academy of Sciences, St. Petersburg, Russia

    N. B. Kenigfest, M. G. Belekhova & T. V. Chudinova

  2. Muséum National d’Histoire Naturelle USM-0501, Paris, France

    N. B. Kenigfest

Authors
  1. N. B. Kenigfest
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. G. Belekhova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. T. V. Chudinova
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to N. B. Kenigfest.

Additional information

Original Russian Text © N.B. Kenigfest, M.G. Belekhova, T.V. Chudinova, 2017, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2017, Vol. 53, No. 2, pp. 127—135.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kenigfest, N.B., Belekhova, M.G. & Chudinova, T.V. Distribution of calcium-binding proteins parvalbumin and calbindin in the pigeon telencephalic auditory center. J Evol Biochem Phys 53, 143–152 (2017). https://doi.org/10.1134/S1234567817020070

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1234567817020070

Key words

Search

Navigation