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 overlap** 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.
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
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Elliott, T.M. and Theunissen, F.E, The Avian Auditory Pallium. Auditory Cortex, Springer, New York and oth., 2011, pp. 429–443.
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.
Prather, J.F, Auditory signal processing in communication: perception and performance of vocal sounds, Hearing Res., 2013, vol. 305, pp. 144–155.
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.
Karten, H.J, Vertebrate brains and evolutionary connections: on the origins of the mammalian “neocortex”, Phil. Trans. Roy. Soc. B., 2015, vol. 370.0060.
Reiner, A., Yamamoto, K., and Karten, H.J, Organization and evolution of the avian brain, Anat. Rec., 2005, vol. 287 A, pp. 1080–1102.
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.
Wild, J.M. and Krutzfeldt, N.O.E, Neocorticallike organization of avian auditory cortex, Brain Behav. Evol., 2010, vol. 76, pp. 89–92.
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.
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.
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.
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.
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.
Striedter, G.F., Principles of Brain Evolution, University of California Press, Irvine, 2005.
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.
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.
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.
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.
Wong, P. and Kaas, J.H, Architectonic subdivisions of neocortex in Galago (Otolemur garnetti), Anat. Rec., 2010, vol. 293, pp. 1033–1069.
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.
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.
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.
Brauth, S.E, Investigation of central auditory nuclei in the budgerigar with cytochrome oxidase histochemistry, Brain Res., 1990, vol. 508, pp. 142–146.
Bosman, C.A. and Aboitiz, F, Functional constraints in the evolution of brain circuits, Front. Neurosci., 2015, vol. 9, p. 303.
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.
Harris, K.D, Cortical computation in mammals and birds, Proc. Natl. Acad. Sci., 2015, vol. 112, pp. 3184–3185.
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.
Jones, E.G, Viewpoint: the core and matrix of thalamic organization, Neurosci., 1998, vol. 85, pp. 331–345.
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.
Meliza, C.D. and Margoliash, D, Emergence of selectivity and tolerance in the avian auditory cortex, J. Neurosci., 2012, vol. 32, pp. 15158–15168.
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.
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.
Author information
Authors and Affiliations
Corresponding author
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
About this article
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
Received:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1234567817020070