Abstract
The immunoreactivity patterns of gamma-aminobutyric acid (GABA), choline acetyltransferase (ChAT), calcium-binding protein (CaBPr) and the histochemical pattern of cytochrome oxidase (CO) activity were studied in the isthmic complex of visual nuclei of turtles (Testudo horsfieldi, Emys orbicularis). Magnocellular nucleus (IMc) was shown to contain mainly the intensely labeled GABA- and parvalbumin (PV)-immunoreactive and CO-positive neurons as well as the variable both in number and degree of immunorecativity (-ir) ChAT-, calbindin (CB)-, and calretinin (CR)-ir neurons. Local tracer injection into the optic tectum revealed in IMc the GABAir neurons co-localizing the retrograde label. The most characteristic feature of the parvocellular nucleus (IPc) was the presence of the intensely labeled ChAT-ir neurons, dense GABA-ir and CO-active terminal fields, as well as GABA- and CaBPr-ir neurons variable in number and degree of immunoreactivity. The data obtained further corroborate the identity revision of the reptilian isthmic complex of visual nuclei we have undertaken previously. A fundamental similarity of the IMc and IPc isthmic nuclei in turtles and birds suggests their homology and similar participation in selective processing of visual information flow. A comparison with lower vertebrates confirms the evolutionary conservatism of the visual isthmic complex among vertebrates and its progressive differentiation in the process of evolution.
Similar content being viewed by others
Abbreviations
- BDA:
-
biotinylated dextran amine
- Cb:
-
cerebellum
- CB:
-
calbindin
- ChAT:
-
choline acetyltransferase
- CO:
-
cytochrome oxidase
- CR:
-
calretinin
- GABA:
-
gamma-aminobutyric acid
- HRP:
-
horseradish peroxidase
- IMc:
-
nucleus isthmi, pars magnocellularis
- IPc:
-
nucleus isthmi, pars parvocellularis
- IPcr:
-
rostral area of IPc
- IPcc:
-
caudal area of IPc
- PV:
-
parvalbumin
- Sm:
-
mean square of neuronal cell bodies
- TeO:
-
tectum opticum
- Ts:
-
torus semicircularis
- v:
-
ventricle
- X:
-
nucleus X
- IV:
-
nervus trochlearis
References
Wang, Y., Major, D.E., and Karten, H.J., Mor phology and connections of nucleus isthmi pars magnocellularis in chicks (Gallus gallus), J. Comp. Neurol., 2004, vol. 469, pp. 275–297.
Marin, G., Salas, C., Sentis, E., Rojas, X., Letelier, J.C., and Mpodozis, J., A cholinergic gating mechanisms controlled by competitive interactions in the optic tectum of the pigeon, J. Neurosci, 2007, vol. 27, pp. 8112–8121.
Marin, G.J., Duran, E., Morales, C., Gonzalez-Cabrera, C., Sentis, E., Mpodozis, J., and Letelier, J.C., Attention capture? Synchronized feedback signals from the isthmi boost retinal signals to higher visual areas, J. Neurosci., 2012, vol. 32, pp. 1110–1122.
Faunes, M., Fernandez, S., Guttierez-Ibanez, A.N., Iwaniuk, A.N., Wylie, D.R., Mpodozis, J., Karten, H.J., and Marin, G., Laminar segregation of GABAergic neurons in the avian nucleus pars magnocellularis: a retrograde tracer and comparative study, J. Comp. Neurol., 2013, vol. 521, pp. 1721–1742.
Mysore, S.P. and Knudsen, E.I., A shared inhibitory circuits for both exogenous and endogenous control stimulus selection, Nat. Neurosci., 2013, vol. 16, pp. 473–478.
Marin, O., Smeets, W.J.A.J., and Gonzalez, A., Distributon of choline acetyltransferase immunoreactivity in the brain of anuran (Rana perezi, Xenopus laevis) and urodele (Pleurodeles walti) amphibians, J. Comp. Neurol., 1997, vol. 382, pp. 499–534.
Wang, S.R., The nucleus isthmi and dual modulation of the receptive field of tectal neurons in non-mammals, Brain Res. Brain Res. Rev., 2003, vol. 41, pp. 13–25.
Clemente, D., Porters, A., Weruaga, E., Alonso, J.R., Arenzana, F.R., Aijon, J., and Arevalo, R., Cholinergic elements in the zebra fish central nervous system: histochemical and immunohistochemical analysis, J. Comp. Neurol., 2004, vol. 474, pp. 75–107.
Buler, A.B. and Hodos, W., Comparative Vertebrate Neuroanatomy. Evolution and Adaptation, 2nd ed., Hoboken, New Jersey (USA), 2005.
Dudkin, E. and Gruberg, E., Evolution of nucleus isthmi, Encyclopedia of Neuroscience, Springer Verlag, Berlin, Heidelberg, 2009, vol. 9, pp. 1258–1262.
Lopez, J.M., Domingues, L., Morona, R., Northcutt, G.R., and Gonzalez, A., Organization of the cholinergic systems in the brain of two lungfishes, Protopterus dolloi and Neoceratodus forsteri, Brain Structure and Function, 2011, vol. 217, pp. 549–576.
Kappers, A., Huber, G.C., and Crosby, E.C., The Comparative Anatomy of the Nervous System of Vertebrates, Iincluding Man, New York, 1936, vol. 2.
Cruce, W.L.R. and Nieuwenhuys, R., The cell mass in the brain stem of the turtle Testudo hermanni; a topographical and topological analysis, J. Comp. Neurol., 1974, vol. 153, pp. 277–306.
Foster, R.E. and Hall, W.C., The connections and laminar organization of the optic tectum in a reptile (Iguana iguana), J. Comp. Neurol., 1975, vol. 163, pp. 397–426.
Ten Donkelaar, H. J. and Nieuwenhuys, R., The brainstem, Biology of the Reptilien, vol. 10, Neurology B. London: Academic, 1979, pp. 133–200.
Powers, A.S. and Reiner, A., A stereotaxic atlas of the forebrain and midbrain of the eastern painted turtle (Chrysemys picta picta), J. Hirnforsch., 1980, vol. 21, pp. 125–159.
Künzle, H. and Schnyder, H., The isthmus-tegmentum complex in the turtle and rat: a comparative analysis of its interconnections with the optic tectum, Exp. Brain Res., 1984, vol. 56, pp. 509–522.
Sereno, M.I., Tectoreticular pathways in the turtle, Pseudemys scripta. I. Morphology of tectoreticular axons, J. Comp. Neurol., 1985, vol. 233, pp. 48–90.
Sereno, M.I. and Ulinski, P.S., Caudal topographic nucleus isthmi and the rostral nontopographic nucleus isthmi in the turtle Pseudemys scripta, J. Comp. Neurol., 1987, vol. 261, pp. 319–346.
Powers, A.S. and Reiner, A., The distribution of cholinergic neurons in the central nervous system of turtles, Brain Behav. Evol., 1993, vol. 41, pp. 269–348.
Veenman, C.L. and Reiner, A., The distribution of GABA-containing pericarya, fibers and terminals in the forebrain and midbrain of pigeons, with particular reference to the basal ganglia and its projection targets, J. Comp. Neurol., 1994, vol. 339, pp. 209–250.
Medina, L. and Reiner, A., Distribution of choline acetyltransferase immunoreactivity in the pigeon brain, J. Comp. Neurol., 1994, vol. 340, pp. 1–41.
Tömbol, T. and Nemeth, A., GABA-immunohistological observations, at the electron microscopical level, of the neurons of isthmic nuclei in chicken, Gallus domesticos, Cell Tissue Res., 1998, vol. 291, pp. 255–266.
Wang, Y., Luksch, H., Brecha, N.C., and Karten, H.J., Columnar projections from cholinergic nucleus isthmi to the optic tectum in chicks (Gallus gallus): a possible substrate for synchronizing tectal channels, J. Comp. Neurol., 2006, vol. 494, pp. 7–35.
Sun, Z., Wang, H.B., Laverghetta, A., Yamamoto, K., and Reiner, A., The distribution and cellular localization of glutamic acid decarboxilase-65 (GAD-65) mRNA in the forebrain and midbrain of domestic chick, J. Chem. Neuroanat., 2005, vol. 29, pp. 265–281.
Wylie, D.R.W., Gutierrez-Ibanez, C., Pakan, J.M.P., and Iwaniuk, A.N., The optic tectum of birds: mapping our way to understanding visual processing, Canad. J. Psychol., 2009, vol. 63, pp. 328–338.
Knudsen, E.I., Control from below: the role of a midbrain network in spatial attention, Eur. J. Neurosci., 2011, vol. 33, pp. 1961–1972.
Belekhova, M.G., Kenigfest, N.B., Minakova, M.N., Rio, J.-P., and Reperant, J., Calciumbinding proteins in turtle thalamus: the analysis in the light of the “core-matrix” thalamus organization hypothesis as related to the problem of thalamic nuclei homology among amniotes, Zh. Evol. Biokhim. Fiziol., 2003, vol. 39, pp. 504–523.
Belekhova, M.G., Kenigfest, N.B., Gapanovich, S.O., Rio, J.-P., and Reperant, J., Neurochemical organization of turtle thalamus, Zh. Evol. Biokhim. Fiziol., 2006, vol. 42, pp. 509–525.
Kenigfest, N., Belekhova, M., Reperant, J., Rio, J.-P., Ward, R., and Vesselkin, N., The turtle thalamic anterior entopeduncular nucleus shares connectional and neurochemical characteristics with the mammalian thalamic reticular nucleus, J. Chem. Neuroanat., 2005, vol. 30, pp. 129–143.
Belekhova, M., Chudinova, T.V., Kenigfest, N.B., and Krasnoschekova, E.I., The level of metabolic activity (cytochrome oxidase) as an indicator of functional activity of the reptilian tectofugal and thalamofugal visual pathways, Zh. Evol. Biokhim. Fiziol., 2007, vol. 43, pp. 87–98.
Saha, D., Morton, D., Ariel, M., and Wessel, R., Response properties of visual neurons in the turtle nucleus isthmi, J. Comp. Physiol. A. Neuroethol. Sens. Neural Behav. Physiol., 2011, vol. 197, pp. 153–165.
Desan, P.H., Gruberg, E.R., and Eckenstein, F., A cholinergic prpjection from the nucleus isthmi to the optic tectum in turtle and frog, Soc. Neurosci. Abstr., 1984, vol. 10, p. 575.
Medina, L. and Smeets, W.A.J.A., Distribution of choline acetyltransferase immunoreactivity in the brain of lizards (Gekko gecko, Galottia galotti), Brain Behav. Evol., 1992, vol. 40, pp. 157–181.
Wang, S.R., Yan, K., Wang, Y.-T., Jiang, S.-Y., and Wang, X.-S., Neuroanatomy and electrophysiology of the lacertilian nucleus isthmi, Brain Res., 1983, vol. 275, pp. 355–360.
Granda, R.H. and Crossland, W.J., GABA-like immunoreactivity of neurons in the chicken diencephalon and mesencephalon, J. Comp. Neurol., 1989, vol. 287, pp. 455–469.
Sorenson, E.M., Parkinson, D., Dahl, J.L., and Chiapelli, V.A., Immunohistochemical localization of choline acetyltransferase in the chicken mesencephalon, J. Comp. Neurol., 1989, vol. 281, pp. 641–657.
Hunt, S.P., Streit, P., Künzle, H., and Cuenod, M., Characterization of the pigeon isthmotectal pathway by selective uptake and retrograde movement of radioactive compounds and by Golgi-like horseradish peroxidase labeling, Brain Res., 1977, vol. 129, pp. 197–212.
Wang, S.R., Wu, G.Y., and Felix, D., Avian Imctectal projection is mediated by acetylcholine and glutamate, Neuroreport, 1995, vol. 6, pp. 757–760.
George, S.A., Wu, G.-Y., Li, W.-C., and Wang, S.R., Dual action of isthmic input to tectal neurons in a reptile Gekko gecko, Vis. Neurosci., 1999, vol. 16, pp. 889–893.
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.
Partata, W.A., Krepsky, A.M.R., Xavier, L.L., Marques, M., and Achaval, M., Distribution of glycogen phosphorilase and cytochrome oxidase in the central nervous system in the turtle Trachemys dorbigni, Comp. Biochem. Physiol. Part A, 1999, vol. 124, pp. 113–122.
Belekhova, M.G., Kenigfest, N.B., and Chudinova, T.V., Cytochrome oxidase activity in the pigeon tectofugal and thalamofugal visual pathways, Zh. Evol. Biokhim. Fiziol., 2011, vol. 47, pp. 73–84.
Helleman, B., Manns, M., and Gunturkun, O., Nucleus isthmi, pars semilunaris as a key component of the tectofugal visual system in pigeons, J. Comp. Neurol., 2001, vol. 436, pp. 153–166.
Gruberg, E.B. and Udin, S.B., Topographic projections between the nucleus isthmi and the tectum of the frog Rana pipiens, J. Comp. Neurol., 1978, vol. 179, pp. 487–500.
Grobstein, P. and Comer, C., The nucleus isthmi as an intertectal relay for the ipsilateral oculotectal projection in the frog Rana pipiens, J. Comp. Neurol., 1983, vol. 217, pp. 54–74.
Perez, S.E., Yanez, J., Marin, O., Anadon, R., Gonzalez, A., and Rodrigues-Moldes, I., Distribution of choline acetyltransferase (ChAT) im munoreactivity in the brain of adult trout and tract-tracing observations on the connections of the nuclei of the isthmus, J. Comp. Neurol., 2000, vol. 428, pp. 450–474.
Pombal, M.A., Marin, O., and Gonzalez, A., Distribution of choline acetyltransferase-immunoreactive structures in the lamprey brain, J. Comp. Neurol., 2001, vol. 431, pp. 105–126.
Lopez, J.M., Periado, J., Morona, R., Northcutt, R.G., and Gonzalez, A., Neuroanatomical organization of the cholinergic system in the central nervous system of a basal actinopterygian fish, the senegal bichir Polypterus senegalus, J. Comp. Neurol., 2013, vol. 521, pp. 24–49.
Zottoli, S.J., Rhodes, K.J., Corrodi, J.G., and Mufson, E.J., Putative cholinergic projections from the nucleus isthmi and the nucleus reticularis mesencephali in the optic tectum in the gold fish (Carassius auratus), J. Comp. Neurol., 1988, vol. 273, pp. 385–398.
Li, Z., and Fite, K.V., Distribution of GABA-like immunoreactive neurons and fibers in the central visual nuclei and retina of frog, Rana pipiens, Vis. Neurosci., 1998, vol. 15, pp. 995–1006.
Li, Z. and Fite, K.V., GABAergic visual pathways in the frog Rana pipiens, Vision. Res., 2001, vol. 18, pp. 457–464.
Pollak, E., Lazar, G., Gabriel, R., and Wang, S.R., Localization and source of gamma aminobutyric acid in the isthmic nucleus of the frog Rana esculenta, Brain Res. Bull., 1999, vol. 48, pp. 343–350.
Rybicka, K.K. and Udin, S.B., Connections of contralaterally projecting isthmotectal axons and GABA-immunoreactive neurons in Xenopus tectum: an ultrastructural study, Vis. Neurosci., 2005, vol. 22, pp. 305–315.
Author information
Authors and Affiliations
Corresponding author
Additional information
Original Russian Text © M.G. Belekhova, N.B. Kenigfest, 2014, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2014, Vol. 50, No. 5, pp. 381–391.
Rights and permissions
About this article
Cite this article
Belekhova, M.G., Kenigfest, N.B. Turtle isthmic complex of visual nuclei: Immunohistochemistry of gamma-aminobutyric acid, choline acetyltransferase, calcium-binding proteins and histochemistry of cytochrome oxidase activity. J Evol Biochem Phys 50, 435–447 (2014). https://doi.org/10.1134/S0022093014050081
Received:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S0022093014050081