Skip to main content
Log in

Distribution of metabolic activity (cytochrome oxidase) and immunoreactivity to calcium-binding proteins in the turtle brainstem auditory nuclei

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

Abstract

Using histochemical and immunohistochemical techniques, distribution of activity of oxidative mitochondrial enzyme cytochrome oxidase (CO) and calcium-binding proteins-immunoreactivity was studied in the spiral ganglion and auditory nuclei of brainstem in two turtle species. Calbindin-, parvalbumin-and calretinin-immunoreactivity in neurons and neuropil of cochlear, supraolivary complexes, the lateral lemniscal nucleus and neuropil of spiral ganglion is shown to coincide topographically with high activity of CO. Similarity of the studied metabolic and neuro-chemical characteristics of these auditory centers in reptiles, birds and mammals suggests some general principles of their organization in amniotes, despite phylogenetic differences and peculiarities of auditory system in different species.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Manley, G.A. and Clark, J.A., An Outline of the Evolution of Vertebrate Hearing, Evolution of the Vertebrate Auditory System, New York, Springer, 2004, pp. 1–26.

    Google Scholar 

  2. Grothe, B., Carr, C.E., Cassaday, J.H., Fritzsch, B., and Kцppl, C., The Evolution of Central Pathways and Their Neural Processing Patterns, Evolution of the Vertebrate Auditory System, New York: Springer, 2004, pp. 289–359.

    Google Scholar 

  3. Brauth, S.E., Investigation of Central Auditory Nuclei in the Budgerigar with Cytochrome Oxidase Histochemistry, Brain Res., 1990, vol. 508, pp. 142–146.

    Article  PubMed  CAS  Google Scholar 

  4. Deszo, A., Schwarz, D.W., and Schwarz, I.E., A Survey of Auditory Brainstem Nuclei in the Chicken (Gallus domesticus) with Cytochrome Oxidase Histochemistry, J. Otolaryngol., 1993, vol. 22, pp. 385–391.

    Google Scholar 

  5. Gonzalez-Limai, F. and Jones, D., Quantitative Mapping of Cytochrome Oxidase in the Central Auditory System of the Gerbil: A Study with Calibrated Activity Standards and Metal-Intensified Histochemistry, Brain Res., 1994, vol. 660, pp. 34–49.

    Article  Google Scholar 

  6. Belekhova, M.G., Kenigfest, N.B., Karamyan, O.A., and Vesselkin, N.P., Distribution of Calcium-Binding Proteins in the Central and Peripheral Parts of Mesencephalic Auditory Center (Torus semicircularis) of Turtles, Dokl. RAN, 2004, vol. 399, pp. 558–562.

    Google Scholar 

  7. Belekhova, M.G., Kenigfest, N.B., Chudinova, T.V., and Vesselkin, N.P., Metabolic Activity of the Central and Peripheral Parts of Reptilian Mesencephalic Auditory Center, Dokl. RAN, 2006, vol. 411, pp. 563–566.

    Google Scholar 

  8. Wong-Riley, M.T.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  PubMed  CAS  Google Scholar 

  9. Miller, M.R. and Kasahara, M., The Cochlear Nuclei of Some Turtles, J. Comp. Neurol., 1979, vol. 185, pp. 221–236.

    Article  PubMed  CAS  Google Scholar 

  10. ten Donkelaar, H.J., Reptiles, The Central Nervous System of Vertebrates, vol. 2, Berlin: Springer, 1998, pp. 1315–1524.

    Google Scholar 

  11. Kihlenbeck, H., The Central Nervous System of Vertebrates, vol. 4, pt. 2, Spinal Cord and Deuterencephalon, Basel: Karger, 1975.

    Google Scholar 

  12. Kappers Ariens, C.U., Huber, G.C., and Crosby, E.C., The Comparative Anatomy of the Nervous System of Vertebrates Including Man, vol. 1, New York: Hafner, 1960.

    Google Scholar 

  13. Belekhova, M.G., Zharskaja, V.D., Khachunts, A.S., Gaidaenko, G.V., and Tumanova, N.L., Connections of the Mesencephalic, Thalamic and Telencephalic Auditory Centers in Turtles. Some Structural Basis for Audiosomatic Interrelations, J. Hirnforsch., 1985, vol. 22, pp. 127–152.

    Google Scholar 

  14. Künzle, H., Projections from the Cochlear Nuclear Complex to Rhombencephalic Auditory Centers and Torus semicircularis in the Turtle, Brain Res., 1986, vol. 379, pp. 307–319.

    Article  PubMed  Google Scholar 

  15. Barsova, L.I., Bogoslovskaya, L.S., and Vasiliev, B.D., Slukhovye tsentry prodolgovatogo mozga nazemnykh pozvonochnykh (The Auditory Centers of Medulla of Terrestrial Vertebrates), Moscow, 1985.

  16. Foster, R.E. and Hall, W.C., The Organization of Central Auditory Pathways in a Reptile Iguana iguana, J. Comp. Neurol., 1978, vol. 178, pp. 783–832.

    Article  PubMed  CAS  Google Scholar 

  17. ten Donkelaar, H.J., Bangma, G.C., Barbas-Henry, H.A., and Boervan-Huizen, R., and Wolters, J.G., The Brainstem in a Lizard, Varanus exanthematicus, Adv. Anat. Embryol. Cell Biol., 1987, vol. 107, pp. 1–168.

    PubMed  Google Scholar 

  18. Hackney, C.M., Mahendrasingam, S., Jones, E.M., and Feltiplace, R., The Distribution of Calcium Buffering Proteins in the Turtle Cochlea, J. Neurosci., 2003, vol. 23, pp. 4577–4589.

    PubMed  CAS  Google Scholar 

  19. Partata, W.A., Krepsky, A.M., Xavier, L.L., Marques, M., and Achaval, M., Distribution of Glycogen Phosphorylase and Cytochrome Oxidase in the Central Nervous System of the Turtle Trachemys dorbigni, Comp. Biochem. Physiol. pt. A, 1999, vol. 124, pp. 113–122.

    Article  CAS  Google Scholar 

  20. Braun, K., Schleich, H., Schachner, M., and Heizmann, C.W., Distribution of Parvalbumin, Cytochrome Oxidase and 14C-2-Deoxyglucose Uptake in the Brain of the Zebra Finch. I. Auditory and Vocal Motor Systems, Cell Tiss. Res., 1985, vol. 240, pp. 101–115.

    Article  CAS  Google Scholar 

  21. Takahashi, T.T., Carr, C.E., Breche, N., and Konishi, M., Calcium-Binding Protein-Like Immunoreactivity Labels the Terminal Field of Nucleus laminaris of the Barn Owl, J. Neurosci., 1987, vol. 7, pp. 1843–1856.

    PubMed  CAS  Google Scholar 

  22. Braun, K., Calcium-Binding Proteins in Avian and Mammalian Central Nervous System: Localization, Development and Possible Functions, Progr. Histochem. Cytochem., 1990, vol. 21, pp. 1–62.

    CAS  Google Scholar 

  23. Hyde, G.E. and Durham, D., Cytochrome Oxidase Response to Cochlear Removal in Chicken Auditory Brainstem, J. Comp. Neurol., 1990, vol. 297, pp. 329–339.

    Article  PubMed  CAS  Google Scholar 

  24. Heizman, C.W. and Braun, K., Calcium-Binding Proteins: Molecular and Functional Aspects, The Role of Calcium in Biological Systems, Roca Raton, FL: CRC, 1990, pp. 21–65.

    Google Scholar 

  25. Zettel, M.L., Carr, C.E., and O’Neill, W.E., Calbindin-Like Immunoreactivity in the Central Auditory System in Mustached Bat, Pteronotus parnelli, J. Comp. Neurol., 1991, vol. 313, pp. 1–16.

    Article  PubMed  CAS  Google Scholar 

  26. Braun, K. and Pipienstock, A., Parvalbumin-Immunoreactive Neurons in the Subcortical Auditory Pathway of the Mongolian Gerbil (Meriones unguiculatus), Acta Histochem. Cytochem, 1993, vol. 26, pp. 543–554.

    Google Scholar 

  27. Vater, M. and Braun, K., Parvalbumin, Calbindin-D 28k and Calretinin Immunoreactivity in the Ascending Auditory Pathway of the Horseshoe Bats, J. Neurol., 1994, vol. 341, pp. 534–538.

    CAS  Google Scholar 

  28. Frizina, R.D., Zettel, M.L., Kelley, P.E., and Walton, J.P., Distribution of Calbindin D-28k Immunoreactivity in the Cochlear Nucleus of the Young Adult Chinchilla, Hear. Res., 1995, vol. 85, pp. 53–68.

    Article  Google Scholar 

  29. Krasnoshchekova, E.I., Rumyantseva, I.A., and Kulikov, G.A., Comparative Histochemical Study of Cytochrome Oxydase Activity in Somatosensory and Auditory Centers of Normal Rat Brain and after Exposure to Microwave Electromagnetic Field, Zh. Evol. Biokhim. Fiziol., 1995, vol. 31, pp. 573–583.

    PubMed  CAS  Google Scholar 

  30. Spatz, W.B. and Lohle, E., Calcium-Binding Proteins in the Spiral Ganglion of the Monkey, Callithrix jacchus, Hear. Res., 1995, vol. 86, pp. 89–99.

    Article  PubMed  CAS  Google Scholar 

  31. Caicedo, A., D’Aldin, C., Puel, J.L., and Eybalan, M., Distribution of Calcium-Binding Protein Immunoreactivities in the Guinea Pig Auditory Brainstem, Anat. Embryol. (Berlin), 1996, vol. 194, pp. 465–487.

    CAS  Google Scholar 

  32. Lohman, C. and Friauf, E., Distribution of the Calcium-Binding Proteins Parvalbumin and Calretinin in the Auditory Brainstem of Adult and Developing Rats, J. Comp. Neurol., 1996, vol. 367, pp. 90–109.

    Article  Google Scholar 

  33. Spatz, W.B., Differences between Guinea Pig and Rat in the Dorsal Cochlear Nucleus: Expression of Calcium-Binding Proteins by Cartwheel and Purkinje-Like Calls, Hear. Res., 1997, vol. 107, pp. 136–146.

    Article  PubMed  CAS  Google Scholar 

  34. Spatz, W.B., Purkinje-Like Cells in the Cochlear Nucleus of the Common Tree Shrew (Tupaia glis) Identified by Calbindin Immunohistochemistry, Brain Res., 2003, vol. 983, pp. 230–232.

    Article  PubMed  CAS  Google Scholar 

  35. Henkel, C.K. and Bruno-Bechtold, J.K., Calcium-Binding Proteins and GABA Reveal Spatial Segregation of Cell Types within the Developing Lateral Superior Olivary Nucleus of the Ferret, Microsc. Res. Techn., 1998, vol. 41, pp. 234–245.

    Article  CAS  Google Scholar 

  36. Tucci, D., Cant, N.B., and Durham, D., Conductive Hearing Loss Results in Changes in Cytochrome Oxidase Activity in Gerbil Auditory System, J. Assoc. Res. Otolaryngol., 2002, vol. 3, pp. 54–67.

    Article  Google Scholar 

  37. Smittkamp, S.E., Park, D.L., Gird, D.A., and Durham, D., Effects of Age and Cochlear Damage on the Metabolic Activity in the Avian Cochlear Nucleus, Hear. Res., 2003, vol. 175, pp. 101–111.

    Article  PubMed  CAS  Google Scholar 

  38. Por, A., Poscai, K., Rusznak, Z., and Szucs, G., Presence and Distribution of Three Calcium-Binding Proteins in Projection Neurons of the Adult Rat Cochlear Nucleus, Brain Res., 2005, vol. 1039, pp. 63–74.

    Article  PubMed  CAS  Google Scholar 

  39. Braun, K., Scheich, H., Heizmann, C.W., and Hunziker, M., Parvalbumin and Calbindin-D 28 K 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 

  40. Kelley, P.E., Frizina, R.D., Zettel, M.L., and Walton, J.P., Differential Calbindin-Like Immunoreactivity in the Brainstem Auditory System of the Chinchilla, J. Comp. Neurol., 1992, vol. 320, pp. 196–212.

    Article  PubMed  CAS  Google Scholar 

  41. Jones, E.G., Chemically Defined Parallel Pathways in the Monkey Auditory System, Ann. N. Y. Acad. Sci., 2003, vol. 999, pp. 218–233.

    Article  PubMed  CAS  Google Scholar 

  42. Scofield, B.R. and Cant, N.B., Organization of the Superior Olivary Complex in the Guinea Pig. I. Cytoarchitecture, Cytochrome Oxidase Histochemistry, and Dendritic Morphology, J. Comp. Neurol., 1991, vol. 314, pp. 645–670.

    Article  Google Scholar 

  43. Karmy, G., Carr, P.A., Yamamoto, T., Chan, S.H., and Nagi, J.I., Cytochrome Oxidase Immunohistochemistry in Rat Brain and Dorsal Root Ganglia: Visualization of Enzyme in Neuronal Perikarya and Parvalbumine-Positive Neurons, Neurosci., 1991, vol. 40, pp. 825–839.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. G. Belekhova.

Additional information

Original Russian Text © M. G. Belekhova, T. V. Chudinova, N. B. Kenigfest, and E. I. Krasnoshchekova, 2008, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2008, Vol. 44, No. 3, pp. 302–310.

The paper is dedicated to 100 anniversary of Artashes Ivanovich Karamyan who headed for many years the comparative physiological direction of Russian evolutionary neurobiology and advocated necessary of the multidisciplinary and systemic approach in studies of brain evolution.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Belekhova, M.G., Chudinova, T.V., Kenigfest, N.B. et al. Distribution of metabolic activity (cytochrome oxidase) and immunoreactivity to calcium-binding proteins in the turtle brainstem auditory nuclei. J Evol Biochem Phys 44, 354–364 (2008). https://doi.org/10.1134/S0022093008030125

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0022093008030125

Key words

Navigation