Skip to main content
Log in

Immunocytochemical localization of calcineurin in the adult and developing primary visual cortex of cats

  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

An immunocytochemical method was used to localize calcineurin, a calcium-dependent calmodulinstimulated protein phosphatase, in the primary visual cortex of developing and adult cats. In the adult calcineurin immunoreactivity exhibits a laminar distribution with dense labeling in the upper half of layers II/III and two lightly labeled bands in lower layer IV and in layer VI. Most of the immunoreactive neurons are pyramidal in shape and appear to form a subpopulation of cortical neurons, but non-pyramidal neurons were also labeled, especially during early stages of postnatal development. The distribution pattern of calcineurin immunoreactivity showed developmental changes until at least 3 months of age. The number of calcineurin-positive cells abruptly increased at 3 weeks, and heavily labeled neurons appeared in a well-delineated band in layer IV between 3 and 5 weeks of age. At 6 to 10 weeks, neurons in layers II/III also became strongly immunoreactive. At this developmental stage intensely stained cells were thus distributed throughout layers II to IV. Thereafter, there was a marked decrease in the number of immunoreactive cells in layer IV and beyond 12 weeks the distribution pattern of calcineurin immunoreactivity became similar to that of adult animals. These changes of calcineurin expression show some relation with the inside-out pattern of cortical maturation and with the time course and the laminar selectivity of use-dependent malleability. Therefore, we suggest that calcineurin may be involved in processes of neuronal differentiation and experience-dependent plasticity.

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

  • Antonini A, Shatz CJ (1990) Relation between putative transmitter phenotypes and connectivity of subplate neurons during cerebral cortical development. Eur J Neurosci 2:744–761

    Google Scholar 

  • Artola A, Singer W (1987) Long-term potentiation and NMDA receptors in rat visual cortex. Nature 330:649–652

    Google Scholar 

  • Artola A, Singer W (1990) The involvement of N-methyl-d-aspartate receptors in induction and maintenance of long-term potentiation in rat visual cortex. Eur J Neurosci 2:254–269

    Google Scholar 

  • Artola A, Bröcher S, Singer W (1990) Different voltage-dependent thresholds for inducing long-term depression and long-term potentiation in slices of rat visual cortex. Nature 347:69–72

    Google Scholar 

  • Bode-Greuel KM, Singer W (1988) Developmental changes of the distribution of binding sites for organic calcium-channel blockers in cat visual cortex. Exp Brain Res 70:266–275

    Google Scholar 

  • Bode-Greuel KM, Singer W (1989) The development of N-methy-ld-aspartate receptor in cat visual cortex. Dev Brain Res 46:197–204

    Google Scholar 

  • Bode-Greuel KM, Singer W (1991) Developmental changes of calcium currents in the visual cortex of the cat. Exp Brain Res 84:311–318

    Google Scholar 

  • Bröcher S, Artola A, Singer W (1992) Intracellular injection of Ca2+ chelators blocks induction of long-term depression in rat visual cortex. Proc Natl Acad Sci USA 89:123–127

    Google Scholar 

  • Callaway EM, Katz LC (1990) Emergence and refinement of clustered horizontal connections in cat striate cortex. J Neurosci 10:1134–1153

    Google Scholar 

  • Chun JJM, Nakamura MJ, Shatz J (1987) Transient cells of the developing mammalian telencephalon are peptide immunoreactive neurons. Nature 325:617–620

    Google Scholar 

  • Cline HT, Debski EA, Constantine-Paton M (1987) N-Methyl-d-aspartate receptor antagonist desegregates eye-specific stripes. Proc Natl Acad Sci USA 84:4342–4345

    Google Scholar 

  • Collingridge GL, Singer W (1990) Excitatory amino acid receptors and synaptic plasticity. Trends Pharmacol Sci 11:290–296

    Google Scholar 

  • Connor JA, Wadman WJ, Hockberger PE, Wong RKS (1988) Sustained dendritic gradients of calcium induced by excitatory amino acids in CA1 hippocampal neurons. Science 240:649–653

    Google Scholar 

  • Constantine-Paton M, Cline HT, Debski E (1990) Patterned activity, synaptic convergence, and the NMDA receptor in developing visual pathways. Ann Rev Neurosci 13:129–154

    Google Scholar 

  • Dehay C, Bullier J, Kennedy H (1985) Transient projections from the fronto-parietal and temporal cortex to areas 17, 18 and 19 in the kitten. Exp Brain Res 57, 208–212

    Google Scholar 

  • Frégnac Y, Imbert M (1984) Development of neuronal selectivity in primary visual cortex of cat. Physiol Rev 64:325–434

    Google Scholar 

  • Garthwaite J (1989) NMDA receptors, neuronal development and neurodegeneration. In: Watkins JC, Collingridge GL (eds) The NMDA receptor. Oxford University Press, pp 187–205

  • Gilbert CD, Hirsch JA, Wiesel TN (1990) Lateral interactions in visual cortex. Cold Spring Harbor Symposium Quant Biol, vol LV. Cold Spring Harbor Laboratory Press, pp 663–677

  • Goto S, Yamamoto H, Fukunaga K, Iwasa T, Miyamoto E (1985) Dephosphorylation of microtubule-associated protein 2, tau factor, and tubulin by calcineurin. J Neurochem 45:276–283

    Google Scholar 

  • Goto S, Matsukado Y, Mihara Y, Inoue N, Miyamoto E (1986a) The distribution of calcineurin in the rat brain by light and electron microscopic immunohistochemistry and enzyme-immunoassay. Brain Res 397:161–172

    Google Scholar 

  • Goto S, Matsukado Y, Mihara Y, Inoue N, Miyamoto E (1986b) Calcineurin in human brain and its relation to extrapyramidal system. Immunohistochemical study on postmortem brains. Acta Neuropathol 72:150–156

    Google Scholar 

  • Goto S, Matsukado Y, Miyamoto E, Yamada M (1987) Morphological characterization of the rat striatal neurons expressing calcineurin immunoreactivity. Neuroscience 22:189–201

    Google Scholar 

  • Goto S, Matsukado Y, Uemura S Mihara Y, Inoue N, Ikeda J, Miyamoto E (1988) A comparative immunohistochemical study of calcineurin and S-100 protein in mammalian and avian brains. Exp Brain Res 69:645–650

    Google Scholar 

  • Gu Q, Bear MF, Singer W (1989) Blockade of NMDA-receptors prevents ocularity changes in kitten visual cortex after reversed monocular deprivation. Dev Brain Res 47:281–288

    Google Scholar 

  • Halpain S, Greengard P (1990) Activation of NMDA receptors induces rapid dephosphorylation of the cytoskeletal protein MAP2. Neuron 5:237–246

    Google Scholar 

  • Halpain S, Girault J-A, Greengard P (1990) Activation of NMDA receptors induces dephosphorylation of DARPP-32 in rat striatal slices. Nature 343:369–372

    Google Scholar 

  • Hemmings HC Jr, Greengard P, Tung HYL, Cohen P (1984) DARPP-32, a dopamine-regulated neuronal phosphoprotein, is a potent inhibitor of protein phosphatase-1. Nature 310:503–505

    Google Scholar 

  • Hsu SM, Raine L, Fanger H (1981) Use of avidin-biotin peroxidase complex (ABC) in immunoperoxidase techniques. J Histochem Cytochem 29:577–580

    CAS  PubMed  Google Scholar 

  • Innocenti GM (1981) Growth and reshaping of axons in the establishment of visual callosal connections. Science 212:824–826

    Google Scholar 

  • Kaas JH, Krubitzer LA, Chino YM, Langston AL, Polley EH, Blair N (1990) Reorganization of retinotopic maps in adult mammals after lesions of the retina. Science 248:229–231

    Google Scholar 

  • Klee CB, Cohen P (1988) The calmodulin-regulated protein phosphatase. In: Cohen P, Klee CB (eds) Molecular aspects of cellular regulation. Elsevier Biomedical Press, North Holland, pp 225–248

    Google Scholar 

  • Klee CB, Krinks MH, Manalan AS, Cohen P, Stewart AA (1983) Isolation and characterization of bovine brain calcineurin: a calmodulin-stimulated protein phosphatase. Methods Enzymol 102:227–244

    Google Scholar 

  • Kleinschmidt A, Bear MF, Singer W (1987) Blockade of “NMDA” receptors disrupts experience-dependent plasticity of kitten striate cortex. Science 238:355–358

    Google Scholar 

  • Kretsinger RH, Nockholds CE (1973) Carp muscle calcium-binding protein II, Structure determination and general description. J Biol Chem 248:3313–3326

    Google Scholar 

  • Liu Y, Storm DR (1989) Dephosphorylation of neuromodulin by calcineurin. J Biol Chem 264:12800–12804

    Google Scholar 

  • Löwel S, Singer W (1992) Selection of intrinsic horizontal connections in the visual cortex by correlated neuronal activity. Science 255:209–212

    Google Scholar 

  • Luhmann HJ, Martinez-Millan L, Singer W (1986) Development of horizontal intrinsic connections in cat striate cortex. Exp Brain Res 63:443–448

    Google Scholar 

  • Luhmann HJ, Singer W, Martinez-Millan L (1990) Horizontal interactions in cat striate cortex. I. Anatomical substrate and postnatal development. Eur J Neurosci 2:344–357

    Google Scholar 

  • Luskin MB, Shatz CJ (1985a) Neurogenesis of the cat's primary visual cortex. J Comp Neurol 242:611–631

    Google Scholar 

  • Luskin MB, Shatz CJ (1985b) Studies on the earliest generated cells of the cat's visual cortex: cogeneration of subplate and marginal zones. J Neurosci 5:1062–1075

    Google Scholar 

  • MacDermott AB, Mayer ML, Westbrook GL, Smith SJ, Barker JL (1986) NMDA-receptor activation increases cytoplasmic calcium concentration in cultured spinal cord neurones. Nature 321:519–522

    Google Scholar 

  • Matus A (1988) Microtubule-associated proteins: their potential role in determining neuronal morphology. Ann Rev Neurosci 11:29–44

    Google Scholar 

  • Mower GD, Caplan CJ, Christen WG, Duffy FH (1985) Dark rearing prolongs physiological but not anatomical plasticity of the cat visual cortex. J Comp Neurol 235:448–466

    Google Scholar 

  • Nicoll RA, Kauer JA, Malenka RC (1988) The current excitement in long-term potentiation. Neuron 1:97–103

    Google Scholar 

  • Pfenninger KH, Hyman C, Garofalo RS (1986) Protein phosphorylation in the nerve growth cone. Prog Brain Res 69:235–244

    Google Scholar 

  • Rakiç P (1977) Prenatal development of the visual system in the rhesus monkey. Philos Trans R Soc Lond [Biol] 278:245–260

    Google Scholar 

  • Rauschecker, JP (1991) Mechanisms of visual plasticity: Hebb synapses, NMDA receptors, and beyond. Physiol Reviews 71:587–615

    Google Scholar 

  • Shatz CJ, Luskin MB (1986) Relationship between the geniculo-cortical afferents and their cortical target cells during development of the cat's primary visual cortex. J Neurosci 6:3655–3668

    Google Scholar 

  • Shatz CJ, Ghosh A, McConnell SK, Allendoerfer KL, Friauf E, Antonini A (1990) Pioneer neurones and target selection in cerebral cortical development. Cold Spring Harbor Symposium Quant Biol, vol LV. Cold Spring Harbor Laboratory Press, pp 469–480

  • Shaw C, Needler MC, Cynader M (1984) Ontogenesis of muscarinic acetylcholine-binding sites in cat visual cortex: reversal of specific laminar distribution during critical period. Dev Brain Res 14:295–299

    Google Scholar 

  • Shaw C, Wilkinson M, Cynader M, Needler MC, Aoki C, Hall SE (1986) The laminar distributions and postnatal development of neurotransmitter and neuromodulator receptors in cat visual cortex. Brain Res Bull 16:661–671

    Google Scholar 

  • Singer W (1990) The formation of cooperative cell assemblies in the visual cortex. J Exp Biol 153:177–197

    Google Scholar 

  • Singer W, Tretter F, Yinon U (1982) Evidence for long-term functional plasticity in the visual cortex of adult cats. J Physiol 324:239–248

    Google Scholar 

  • Skene JHP (1989) Axonal growth-associated proteins. Ann Rev Neurosci 12:127–156

    Google Scholar 

  • Tsumoto T, Hagihara K, Sato H, Hata Y (1987) NMDA receptors in the visual cortex of young kittens are more effective than those of adult cats. Nature 327:513–514

    Google Scholar 

  • Wahle P, Meyer G (1987) Morphology and quantitative changes of transient NPY-ir neuronal populations during early postnatal development of the cat visual cortex. J Comp Neurol 261:165–192

    Google Scholar 

  • Wahle P, Meyer G, Wu JJ, Albus K (1987) Morphology and axon terminal pattern of glutamate decarboxylase-immunoreactive cell types in the white matter of cat occipital cortex during early postnatal development. Dev Brain Res 36:53–61

    Google Scholar 

  • Wiesel TN (1982) Postnatal development of the visual cortex and the influence of environment. Nature 299:583–588

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Goto, S., Singer, W. & Gu, Q. Immunocytochemical localization of calcineurin in the adult and developing primary visual cortex of cats. Exp Brain Res 96, 377–386 (1993). https://doi.org/10.1007/BF00234107

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00234107

Key words

Navigation