Hostname: page-component-848d4c4894-x24gv Total loading time: 0 Render date: 2024-06-11T14:36:06.340Z Has data issue: false hasContentIssue false
  • English
  • Français

Projection status of calbindin- and parvalbumin-immunoreactive neurons in the superficial layers of the rat's superior colliculus

Published online by Cambridge University Press:  02 June 2009

Richard D. Lane ,
Dawn M. Allan ,
Carol A. Bennett-Clarke ,
David L. Howell  and
Robert W. Rhoades
Richard D. Lane
Affiliation:
Department of Anatomy and Neurobiology, Medical College of Ohio, Toledo
Dawn M. Allan
Affiliation:
Department of Anatomy and Neurobiology, Medical College of Ohio, Toledo
Carol A. Bennett-Clarke
Affiliation:
Department of Anatomy and Neurobiology, Medical College of Ohio, Toledo
David L. Howell
Affiliation:
Department of Anatomy and Neurobiology, Medical College of Ohio, Toledo
Robert W. Rhoades
Affiliation:
Department of Anatomy and Neurobiology, Medical College of Ohio, Toledo
Get access Rights & Permissions [Opens in a new window]

Abstract

Immunocytochemistry and retrograde labeling were used to define the thalamic projections of calbindin- and parvalbumin-containing cells in superficial layers of the rat's superior colliculus (SC). Quantitative analysis revealed that 90.8 ± 2.2% (mean ± standard deviation) of the calbindin-immunoreactive neurons in the stratum griseum superficiale (SGS) projected to the dorsal lateral geniculate nucleus (LGNd) and that 91.3 ± 4.3% of calbindin-immunoreactive neurons in the stratum opticum (SO) projected to the lateral posterior nucleus (LP). In contrast, only 17.3 ± 2.5% of parvalbumin-immunoreactive neurons in the SGS were found to project to the LGNd and 16.5 ± 3.1% of the parvalbumin-immunoreactive SO cells were retrogradely labeled after LP injections. Few of the parvalbumin-immunoreactive neurons in either the SGS (7.2 ± 2.5%) or the SO (9.2 ± 2.5%) were GABA positive. The retrograde-labeling results suggest that parvalbumin-immunoreactive neurons in the rat's SO and SGS may either be primarily interneurons or have descending projections, while calbindin-containing cells are primarily thalamic projection neurons. These results are consistent with data from other rodents, but almost exactly the opposite of data that have been reported for the cat for these same populations of SC projection neurons. Such interspecies differences raise questions regarding the functional importance of expressing one calcium-binding protein versus another in a specific neuronal population.

Keywords

Superior colliculusLateral geniculate nucleusLateral posterior nucleus
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 2 , March 1997 , pp. 277 - 286
Copyright
Copyright © Cambridge University Press 1997

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Behan, M, Jourdain, A. & Bray, G.M (1992). Calcium-binding protein (calbindin D28k) immunoreactivity in the hamster superior colliculus: Ultrastructure and lack of colocalization with GABA. Experimental Brain Research 89, 115–124.CrossRefGoogle ScholarPubMed
Bennett-Clarke, C.A., Chiaia, N.L., Jacquin, M.F. & Rhoades, R.W. (1992). Parvalbumin and calbindin immunocytochemistry reveal functionally distinct cell groups and vibrissa-related patterns in the trigeminal brainstem complex of the adult rat. Journal of Comparative Neurology 320, 323–338.CrossRefGoogle ScholarPubMed
Caldwell, R.B. & Mize, R.R. (1981). Superior colliculus neurons which project to the cat lateral posterior nucleus have varying morphologies. Journal of Comparative Neurology 203, 53–66.CrossRefGoogle Scholar
Celio, M.R. (1986). Parvalbumin in most gamma-aminobutyric acid containing neurons of the rat cerebral cortex. Science 231, 995–997.CrossRefGoogle ScholarPubMed
Celio, M.R. (1990). Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35, 375–475.CrossRefGoogle ScholarPubMed
Chard, P.S., Bleakman, D., Christakos, S., Fullmer, C.S. & Miller, R.J. (1993). Calcium buffering properties of calbindin D28k and parvalbumin in rat sensory neurones. Journal of Physiology 472, 341–357.CrossRefGoogle ScholarPubMed
DeFelipe, J. & Jones, E.G. (1992). High-resolution light and electron-microscopic immunocytochemistry of colocalized GABA and calbindin D-28k in somata and double bouquet cell axons of monkey somatosensory cortex. European Journal of Neuroscience 4, 46–60.CrossRefGoogle ScholarPubMed
Freund, T.F., Buzsaki, G., Leon, A., Baimbridge, K.G. & Somogyi, P. (1990). Relationship of neuronal vulnerability and calcium binding protein immunoreactivity in ischemia. Experimental Brain Research 83, 55–66.CrossRefGoogle ScholarPubMed
Gerfen, C.R., Baimbridge, K.G. & Miller, J.J. (1985). The neostriatal mosaic: Compartmental distribution of calcium-binding protein and parvalbumin in the basal ganglia of the rat monkey. Proceedings of the National Academy of Sciences of the U.S.A. 82, 8780–8784.CrossRefGoogle Scholar
Gonzales, C, Lin, R.C.-S. & Chesselet, M.-F. (1992). Relative sparing of GABAergic interneurons in the striatum of gerbils with ischemia-induced lesions. Neuroscience Letters 135, 53–58.CrossRefGoogle ScholarPubMed
Harrell, J.V., Caldwell, R.B. & Mize, R.R. (1982). The superior col-liculus neurons which project to the dorsal and ventral lateral geniculate nuclei in the cat. Experimental Brain Research 46, 234–242.CrossRefGoogle Scholar
Hendry, S.H., Jones, E.G., Emson, P.C., Lawson, D.E., Heizmann, C.W. & Streit, P. (1989). Two classes of cortical GABA neurons defined by differential calcium-binding protein immunoreactivities. Experimental Brain Research 76, 467–472.CrossRefGoogle ScholarPubMed
Huerta, M.F. & Harting, J.K. (1984). The mammalian superior collic-ulus: Studies of its morphology and connections. In Comparative Neu rology of the Optic Tectum, ed. Vaneges, H., pp. 687–725. New York: Plenum.CrossRefGoogle Scholar
Illing, R.-B., Vogt, D.M. & Spatz, W.B. (1990). Parvalbumin in rat superior colliculus. Neuroscience Letters 120, 197–200.CrossRefGoogle ScholarPubMed
Jones, E.G. & Hendry, S.H.C. (1989). Differential calcium-binding protein immunoreactivity distinguishes classes of relay neurons in monkey thalamic nuclei. European Journal Neuroscience 1, 222–246.CrossRefGoogle ScholarPubMed
Kawaguchi, Y. (1995). Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. Journal of Neuroscience 15, 2638–2655.CrossRefGoogle ScholarPubMed
Kawaguchi, Y, Katsumaru, H., Kosaka, T, Heizmann, C.W. & Hama, K. (1987). Fast spiking cells in rat hippocampus (CAI region) contain the calcium-binding protein parvalbumin. Brain Research 416, 369–374.CrossRefGoogle Scholar
Kawaguchi, Y. & Kubota, Y (1993). Correlation of physiological sub-groupings of nonpyramidal cells with parvalbumin- and calbindinD28k-immunoreactive neurons in layer V of rat frontal cortex. Journal of Neurophysiology 70, 387–396.CrossRefGoogle Scholar
Kawaguchi, Y., Wilson, C.J. & Emson, P.C. (1989). Intracellular recording of identified neostriatal patch and matrix spiny cells in a slice preparation preserving cortical inputs. Journal of Neurophysiology 62, 1052–1068.CrossRefGoogle Scholar
Kawaguchi, Y., Wilson, C.J., Augood, S.J. & Emson, P.C. (1995). Striatal interneurons: chemical, physiological and morphological characterization. Trends in Neuroscience 18, 527–535.CrossRefGoogle ScholarPubMed
Kawamura, S., Fukushima, N., Hattori, S. & Kudo, M. (1980). Laminar segregation of cells of origin of ascending projections from the superficial layers of the superior colliculus in the cat. Brain Research 184, 486–490.CrossRefGoogle ScholarPubMed
Kohr, G., Lambert, C.E. & Mody, I. (1991). Calbindin-D28K (CaBP) levels and calcium currents in acutely dissociated epileptic neurons. Experimental Brain Research 85, 543–551.CrossRefGoogle ScholarPubMed
Lane, R.D., Bennett-Clarke, C.A., Allan, D.M. & Mooney, R.D. (1993). Immunochemical heterogeneity in the tecto-LP pathway of the rat. Journal of Comparative Neurology 333, 210–222.CrossRefGoogle ScholarPubMed
Leifer, D. & Kowall, N.W. (1993). Immunohistochemical patterns of selective cellular vulnerability in human cerebral ischemia. Journal of Neurological Sciences 119, 217–228.CrossRefGoogle ScholarPubMed
Leranth, C. & Ribak, C.E. (1991). Calcium-binding proteins are concentrated in the CA2 field of the monkey hippocampus: A possible key to this regions's resistance to epileptic damage. Experimental Brain Research 85, 129–136.CrossRefGoogle Scholar
Mattson, M.P., Rychlik, C.C., Chu, C. & Christakos, S. (1991). Evidence for calcium-reducing and excitoprotective roles for the calcium-binding protein calbindin D28k in cultured hippocampal neurones. Neuron 6, 41–51.CrossRefGoogle Scholar
Mize, R.R., Jeon, C.-J., Butler, C.D., Luo, Q. & Emson, P.C. (1991a). The calcium-binding protein calbindin-D 28K reveals subpopulations of projection and interneurons in the cat superior colliculus. Journal of Comparative Neurology 307, 417–436.CrossRefGoogle ScholarPubMed
Mize, R.R., Jeon, C.-J, Luo, Q. & Nabors, B. (1991b). Parvalbumin antibodies label projection neurons in the cat superior colliculus. Investigations in Ophthalmology and Visual Sciences (Suppl.) 32, 1036.Google Scholar
Mize, R.R., Luo, Q., Butler, G., Jeon, C.-J. & Nabors, B. (1992). The calcium-binding proteins parvalbumin and calbindin-D 28K form complementary patterns in the cat superior colliculus. Journal of Comparative Neurology 320, 243–256.CrossRefGoogle ScholarPubMed
Nabors, L.B. & Mize, R.R. (1991). A unique neuronal organization in the cat pretectum revealed by antibodies to the calcium-binding protein calbindin-D 28K. Journal of Neuroscience 11, 2460–2476.CrossRefGoogle Scholar
Nitsch, C, Scorn, A., Sommacal, A. & Kalt, G. (1989). GABAergic hippocampal neurons resistant to ischemia-induced neuronal death contain the Ca2+-binding protein parvalbumin. Neuroscience Letters 105, 263–268.CrossRefGoogle ScholarPubMed
Paxinos, G. & Watson, C. (1982). The Rat Brain in Stereotaxic Coordinates. Sydney, Australia: Academic Press.Google Scholar
Rausell, E., Bae, C.S., Vinuela, A., Huntley, G.W. & Jones, E.G. (1992). Calbindin and parvalbumin cells in monkey VPL thalamic nucleus: distribution, laminar cortical projections, and relations to spinothalamic terminations. Journal of Neuroscience 12, 4088–4111.CrossRefGoogle ScholarPubMed
Schmidt-Kastner, R., Meller, D. & Eysel, U.T. (1992). Immunohisto-chemical changes of neuronal calcium-binding proteins parvalbumin and calbindin-D-28k following unilateral deafferentation in the rat visual system. Experimental Neurology 117, 230–246.CrossRefGoogle Scholar
Sloviter, R.S., Sollas, A.L., Barbaro, N.M. & Laxer, K.D. (1991). Calcium-binding protein (calbindin-D28K) and parvalbumin immuno-cytochemistry in the normal and epileptic human hippocampus. Journal of Comparative Neurology 308, 381–396.CrossRefGoogle Scholar
Spreafico, R., Kirk, C, Franceschetti, S. & Avanzini, G. (1980). Brain stem projections to the pulvinar-lateralis posterior complex of the cat. Experimental Brain Research 40, 209–220.CrossRefGoogle Scholar
Sugita, S., Otani, K., Tokunaga, A. & Terasawa, K. (1983). Laminar origin of the tecto-thalamic projections in the albino rat. Neuroscience Utters 43, 143–147.CrossRefGoogle ScholarPubMed
Tortosa, A. & Ferrer, I. (1993). Parvalbumin immunoreactivity in the hippocampus of the gerbil after transient forebrain ischaemia: A qualitative and quantitative sequential study. Neuroscience 55, 33–43.CrossRefGoogle ScholarPubMed