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Postnatal development of zinc-containing cells and neuropil in the visual cortex of the mouse

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Summary

The postnatal development of zinc-containing synaptic boutons and their cells of origin in the visual cortex of a pigmented mouse is described. Two phases can be distinguished. During the early phase zinc-containing neuropil is first apparent by postnatal day 3. By day 7 a light, but distinct neuropil staining sketches the primary and secondary visual cortices. The primary visual area contains light precipitate in layers V and VI as well as the monocular portion of layer II/III. The secondary visual areas contain slightly denser precipitate in layers II/III through VI. The transition to the second phase is marked by a large increase in precipitate density by day 11. Thereafter, the intensity of the neuropil staining increases to day 28, first in layer II/III and then in layer V, as the adult pattern of neuropil staining gradually develops. In the primary visual cortex precipitate is dense in layers II/III and V, moderate in layer VI, and sparse in layers I and IV. In the secondary visual areas the precipitate is dense in layers II/III and V and moderate in the lower portion of layer I and in layers IV and VI. Cells of origin of zinc-containing boutons are visible by the end of the second postnatal week in layer II/III of the secondary visual cortex. By 21 days of age the pattern of staining in the mature mouse is established, and cells in layers II/III and VI are labeled in both the primary and secondary visual cortices. The developmental sequence of zinc-containing cells and neuropil does not preclude an involvement of zinc in the postnatal regulation of NMDA receptor function.

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References

  • Albanese A, Albanese E, Brusco A, Saavedra JP (1983) A quantitative study of visual cortex synapses during the postnatal development of dark-reared rats. J Neurobiol 14:1–8

    Google Scholar 

  • Angevine JB Jr, Sidman RL (1961) Autoradiographic study of cell migration during histogenesis of cerebral cortex in mouse. Nature 192:766–768

    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, Brocher S, Singer W (1991) Mechanisms of use-dependent synaptic plasticity in slices of rat visual cortex. In: Meldrum BS, Moroni F, Simon RP, Woods JH (eds) Excitatory amino acids. Raven Press, New York, pp 495–501

    Google Scholar 

  • Balkema GW, Dräger UC (1991) Impaired visual thresholds in hypopigmented animals. Visual Neuroscience 6:577–585

    Google Scholar 

  • Bayer SA (1990) Development of the lateral and medial limbic cortices in the rat in relation to cortical phylogeny. Exp Neurol 107:118–131

    Google Scholar 

  • Bennett-Clarke CA, Chiaia NL, Crissman RS, Rhoades RW (1991) The source of transient serotoninergic input to the developing visual and somatosensory cortices in rat. Neuroscience 43:163–183

    Google Scholar 

  • Blue ME, Parnavelas JG (1983a) The formation and maturation of synapses in the visual cortex of the rat. I. Qualitative analysis. J Neurocytol 12:599–616

    Google Scholar 

  • Blue ME, Parnavelas JG (1983b) The formation and maturation of synapses in the visual cortex of the rat. II. Quantitative analysis. J Neurocytol 12:697–712

    Google Scholar 

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

    Google Scholar 

  • Boje KM, Skolnick P (1992) Ontogeny of glycine-enhanced [3H]MK-801 binding to N-methyl-d-aspartate receptor-coupled ion channels. Dev Brain Res 65:51–56

    Google Scholar 

  • Burkhalter A (1989) Intrinsic connections of rat primary visual cortex: laminar organization of axonal projections. J Comp Neurol 279:171–186

    Google Scholar 

  • Caviness VS JR (1975) Architectonic map of neocortex of the normal mouse. J Comp Neurol 164:247–264

    Google Scholar 

  • Coogan TA, Burkhalter A (1988) Sequential development of connections between striate and extrastriate visual cortical areas in the rat. J Comp Neurol 278:242–252

    Google Scholar 

  • Danscher G (1981) Histochemical demonstration of heavy metals. Histochemistry 71:1–16

    Google Scholar 

  • Danscher G (1982) Exogenous selenium in the brain. Histochemistry 76:281–293

    Google Scholar 

  • Dinopoulos A, Eadie LA, Dori I, Parnavelas JG (1989) The development of basal forebrain projections to the rat visual cortex. Exp Brain Res 76:563–571

    Google Scholar 

  • Dräger UC (1975) Receptive fields of single cells and topography in mouse visual cortex. J Comp Neurol 160:269–290

    Google Scholar 

  • Dyson SE, Jones DG (1980) Quantitation of terminal parameters and their interrelationships in maturing central synapses: a perspective for experimental studies. Brain Res 183:43–59

    Google Scholar 

  • Erdo SL, Wolff JR (1990a) Postnatal development of the excitatory amino acid system in visual cortex of the rat. Changes in ligand binding to NMDA, quisqualate and kainate receptors. Int J Dev Neurosci 8:199–204

    Google Scholar 

  • Erdo SL, Wolff JR (1990b) Postnatal development of the excitatory amino acid system in visual cortex of the rat. Changes in uptake and levels of aspartate and glutamate. Int J Dev Neurosci 8:205–208

    Google Scholar 

  • Friedman B, Price JL (1984) Fiber systems in the olfactory bulb and cortex: a study in adult and developing rats, using the Timm method with the light and electron microscope. J Comp Neurol 223:88–109

    Google Scholar 

  • Garrett B, Geneser FA, Slomianka L (1991) Distribution of acetylcholinesterase and zinc in the visual cortex of the mouse. Anat Embryol 184:461–468

    Google Scholar 

  • Garrett B, Sorensen JC, Slomianka L (1992) Fluoro-Gold tracing of zinc-containing afferent connections in the mouse visual cortices. Anat Embryol 185:451–459

    Google Scholar 

  • Geneser-Jensen FA, Blackstad TW (1971) Distribution of acetylcholinesterase in the hippocampal region of the guinea pig. I. Entorhinal area, parasubiculum, and presubiculum. Z Zellforsch Mikrosk Anat 114:460–481

    Google Scholar 

  • Gilbert CD, Wiesel TN (1983) Clustered intrinsic connections in cat visual cortex. J Neurosci 3:1116–1133

    Google Scholar 

  • Hicks RR, Huerta MF (1991) Differential thalamic connectivity of rostral and caudal parts of cortical area Fr2 in rats. Brain Res 568:325–329

    Google Scholar 

  • Jones KA, Baughman RW (1988) NMDA-and non-NMDA-receptor components of excitatory synaptic potentials recorded from cells in layer V of rat visual cortex. J Neurosci 8:3522–3534

    Google Scholar 

  • Jones KA, Baughman RW (1991) Both NMDA and non-NMDA subtypes of glutamate receptors are concentrated at synapses on cerebral cortical neurons in culture. Neuron 7:593–603

    Google Scholar 

  • Kato N, Artola A, Singer W (1991) Developmental changes in the susceptibility to long-term potentiation of neurones in rat visual cortex slices. Dev Brain Res 60:43–50

    Google Scholar 

  • Kimura F, Nishigori A, Shirokawa T, Tsumoto T (1980) Longterm potentiation and N-methyl-d-aspartate receptors in the visual cortex of young rats. J Physiol (Lond) 414:125–144

    Google Scholar 

  • Krettek JE, Price JL (1977) The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat. J Comp Neurol 171:157–192

    Google Scholar 

  • Kvale I, Fosse VM, Fonnum F (1983) Development of neurotransmitter parameters in lateral geniculate body, superior colliculus and visual cortex of the albino rat. Dev Brain Res 7:137–145

    Google Scholar 

  • Luhmann HJ, Prince DA (1991) Postnatal maturation of the GA-BAergic system in rat neocortex. J Neurophysiol 65:247–263

    Google Scholar 

  • Martinez-Gujarro FJ, Soriano E, Del Rio JA, Lopez-Garcia C (1991) Zinc-positive boutons in the cerebral cortex of lizards show glutamate immunoreactivity. J Neurocytol 20:834–843

    Google Scholar 

  • McDonald JK, Speciale SG, Parnavelas JG (1987) The laminar distribution of glutamate decarboxylase and choline acetyltransferase in the adult and developing visual cortex of the rat. Neuroscience 21:825–832

    Google Scholar 

  • Olavarria J, Mignano LR, Van Sluyters RC (1982) Pattern of extrastriate visual areas connecting reciprocally with striate cortex in the mouse. Exp Neurol 78:775–779

    Google Scholar 

  • Parnavelas JG, Cavanagh ME (1988) Transient expression of neurotransmitters in the developing neocortex. TINS 11:92–93

    Google Scholar 

  • Parnavelas JG, Sullivan K, Lieberman AR, Webster KB (1977) Neurons and their synaptic organization in the visual cortex of the rat. Cell Tissue Res 183:499–517

    Google Scholar 

  • Perkins AT IV, Teyler TJ (1988) A critical period for long-term potentiation in the developing rat visual cortex. Brain Res 439:222–229

    Google Scholar 

  • Peters S, Koh J, Choi DW (1987) Zinc selectively blocks the action of N-methyl-d-aspartate on cortical neurons. Science 236:589–593

    Google Scholar 

  • Schadè JP, Pascoe EG (1964) Maturational changes in cerebral cortex. III. Effects of methionine sulfoximine on electrical parameters and dendritic organisation of cortical neurons. In: Himwich WA, Himwich HE (eds) The developing brain. Progr in Brain Res, vol 9. Elsevier, Amsterdam, pp 132–154

    Google Scholar 

  • Sidman RL, Angevine Jr JB, Pierce ET (1971) Atlas of the mouse brain and spinal cord. Harvard University Press, Cambridge, Mass, USA

    Google Scholar 

  • Slomianka L (1992) Neurons of origin of zinc-containing pathways and the distribution of zinc-containing boutons in the hippocampal region of the rat. Neuroscience 48:325–352

    Google Scholar 

  • Slomianka L, Danscher G, Frederickson CJ (1990) Labeling of the neurons of origin of zinc-containing pathways by intraperitoneal injections of sodium selenite. Neuroscience 38:843–854

    Google Scholar 

  • Sukekawa K (1988) Interconnections of the visual cortex with the frontal cortex in the rat. J Hirnforsch 29:83–93

    Google Scholar 

  • Teyler TJ, Perkins AT IV, Harris KM (1989) The development of long-term potentiation in hippocampus and neocortex. Neuropsychologia 27:31–39

    Google Scholar 

  • Teyler T, Aroniadou V, Berry RL, Borroni A, DiScenna P, Grover L, Lambert N (1990) LTP in neocortex. Seminars Neurosci 2:365–379

    Google Scholar 

  • Tsumoto T (1990) Long-term potentiation and depression in the cerebral neocortex. Jpn J Physiol 40:573–593

    Google Scholar 

  • Vaudano E, Legg CR, Glickstein M (1991) Afferent and efferent connections of temporal association cortex in the rat: a horseradish peroxidase study. Eur J Neurosci 3:317–330

    Google Scholar 

  • Wagor E, Mangini NJ, Pearlman AL (1980) Retinotopic organization of striate and extrastriate visual cortex in the mouse. J Comp Neurol 193:187–202

    Google Scholar 

  • Wahlsten D (1982) Deficiency of corpus callosum varies with strain and supplier of the mice. Brain Res 239:329–347

    Google Scholar 

  • Westbrook GL, Mayer ML (1987) Micromolar concentrations of Zn2+ antagonize NMDA and GABA responses of hippocampal neurons. Nature 328:640–643

    Google Scholar 

  • Wolff JR, Böttcher H, Zetsche T, Oertel WH, Chronwall BM (1984) Development of GABAergic neurons in rat visual cortex as identified by glutamate decarboxylase-like immunoreactivity. Neurosci Lett 47:207–212

    Google Scholar 

  • Wong EHF, Kemp JA (1991) Sites of antagonism of the N-methyl-d-aspartate receptor channel complex. Annu Rev Pharmacol Toxicol 31:401–425

    Google Scholar 

  • Wree A, Zilles K, Schleicher A (1983) A quantitative approach to cytoarchitectonics. Anat Embryol 166:333–353

    Google Scholar 

  • Zilles K (1985) The Cortex of the Rat. Springer, Berlin

    Google Scholar 

  • Zilles K, Wree A, Dausch N-D (1990) Anatomy of the neocortex: neurochemical organization. In: Kolb B, Tees RC (eds) The cerebral cortex of the rat. MIT Press, Cambridge, Mass, pp 113–150

    Google Scholar 

  • Zimmer J, Laurberg S, Sunde N (1986) Non-cholinergic afferents determine the distribution of the cholinergic septohippocampal projection: a study of the AChE staining pattern in the rat fascia dentata and hippocampus after lesions, X-irradiation, and intracerebral grafting. Exp Brain Res 64:158–168

    Google Scholar 

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Garrett, B., Slomianka, L. Postnatal development of zinc-containing cells and neuropil in the visual cortex of the mouse. Anat Embryol 186, 487–496 (1992). https://doi.org/10.1007/BF00185462

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