Abstract
Parvalbumin and calbindin D28k immunoreactivities were examined in the neocortex of the rat during postnatal development. Parvalbumin-immunoreactive nonpyramidal neurons first appear in layer V and later in layers VI and IV, and then in II and III. Immunoreactive terminals forming baskets surrounding unlabelled somata appear about 2 days later. The first parvalbumin-immunoreactive neurons appear in the retrosplenial and cingulate cortices, and the rostral region of the primary somatosensory cortex at postnatal days 8 or 9 (P8–P9). These regions are followed by the primary visual, primary auditory and motor cortices at P11. Parvalbumin immunoreactivity appears last in the secondary areas of the sensory regions and association cortices. Adult patterns are reached at the end of the 3rd week. Calbindin D28K-immunoreactive nonpyramidal neurons are found at birth in all cortical layers excepting the molecular layer. The intensity of the immunoreaction increases during the first 8 or 11 days of postnatal life, first in the inner and later in the upper cortical layers, following, therefore, an “inside-out” gradient. Heavily-labelled calbindin D28K-immunoreactive nonpyramidal cells dramatically decrease in number from P11 to P15 due mainly to a decrease of the multipolar subtypes. This suggests that two populations of calbindin D28k-immunoreactive nonpyramidal neurons are produced in the neocortex during postnatal development: one population of neurons transitorily expresses calbindin D28k immunoreactivity; the other population is composed of neurons that are permanently calbindin D28k immunoreactive. In addition to heavily labelled nonpyramidal cells, a band of weakly labelled pyramid-like neurons progressively appears in layers II and III throughout the cerebral cortex, beginning in layer IV in the somatosensory cortex by the end of the 2st week. Adult patterns are reached at the end of the 3rd week. These results indicate that parvalbumin and calbindin D28k immunoreactivities in the cerebral neocortx follow different characteristic patterns during postnatal development. The appearance of parvalbumin immunoreactivity correlates with the appearance of the related functional activity in the different cortical regions, and, probably, with the appearance of inhibitory activity in the neocortex. On the other hand, the early appearance of calbindin D28k immunoreactivity in the neocortex may be related to the early appearance of calbindin immunoreactivity in many other brain regions, and suggests another, as yet unknown, role for this calcium-binding protein during development of the cerebral cortex.
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References
Bähr S, Wolff JR (1985) Postnatal development of axosomatic synapses in the rat visual cortex: morphogenesis and quantitative evaluation. J Comp Neurol 233:405–420
Baimbridge KG, Miller JJ (1982) Immunohistochemical localization of calcium-binding protein in the cerebellum, hippocampal formation and olfactory bulb of the rat. Brain Res 245:223–229
Baimbridge KG, Miller JJ, Parkes CO (1982) Calcium-binding protein distribution in the rat brain. Brain Res 239:519–525
Baimbridge KG, Celio MR, Rogers JH (1992) Calcium-binding proteins in the nervous system. TINS 15:303–308
Bergmann I, Nitsch R, Frotscher M (1991) Area-specific morphological and neurochemical maturation of non-pyramidal neurons in the rat hippocampus as revealed by parvalbumin immunocytochemistry. Anat Embryol 184:403–409
Braun K, Scheich H, Schachner M, Heizmann CW (1985a) Distribution of parvalbumin, cytochrome C oxidase activity and [14C]-2-deocyglucose uptake in the brain of the zebra finch. I. Auditory and vocal motor systems. Cell Tissue Res 240:101–115
Braun K, Scheich H, Schachner M, Heizmann CW (1985b) Distribution of parvalbumin, cytochrome C oxidase activity and [14C]-2-deoxyglucose uptake in the brain of the zebra finch. II. Visual system. Cell Tissue Res 240:117–127
Brederode JFM van, Mulligan KA, Hendrickson AE (1990) Calcium-binding proteins as markers for subpopulations of GABA-ergic neurons in monkey striate cortex. J Comp Neurol 298:1–22
Brederode JFM van, Helliesen MK, Hendrickson AE (1991) Distribution of the calcium-binding proteins and calbindin D-28k in the somatosensory cortex of the rat. Neuroscience 44:157–171
Celio MR (1984) Parvalbumin as a marker of fast firing neurons. Neurosci Lett [Suppl 18]:S332
Celio MR (1986) GABA neurons contain the calcium-binding protein parvalbumin. Science 232:995–997
Celio MR (1990) Calbindin D-28K and parvalbumin in the rat nervous system. Neuroscience 35:375–475
Celio MR, Heizmann CW (1981) Calcium-binding protein parvalbumin as a neuronal marker. Nature 293:300–302
Celio MR, Baier W, Schärer PA, DeViragh PA, Gerday C (1988) Monoclonal antibodies directed against the calcium-binding protein parvalbumin. Cell Calcium 9:81–86
Chronwall B, Wolff JR (1980) Prenatal and postnatal development of GABA-accumulating cells in the occipital neocortex of the rat. J Comp Neurol 190:187–208
Cobas A, Fairén A, Alvarez-Bolado G, Sánchez MP (1991) Prenatal development of the intrinsic neurons of the rat neocortex: a comparative study of the distribution of GABA-immunoreactive cells and the GABA receptor. Neuroscience 40:375–397
DeFelipe J, Jones EG (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. Eur J Neurosci 4:46–60
Del Rio JA, Soriano E, Ferrer I (1992) The development of GABA-immunoreactivity in the neocortex of the mouse. J Comp Neurol 326:501–526
Demeulemeester H, Orban GA, Brandon C, Vanderhaeghen JJ (1988) Heterogeneity of GABAergic cells in the cat visual cortex. J Neurosci 8:988–1000
Demeulemeester H, Vandesande F, Orban GA, Heizmann CW, Pochet R (1989) Calbindin D-28K and parvalbumin immunoreactivity is confined to two separate neuronal subpopulations in the cat visual cortex, whereas partial co-existence is shown in the dorsal geniculate nucleus. Neurosci Lett 99:6–11
Demeulemeester H, Arckness L, Vandesande F, Orban GA, Heizmann W, Pochet R (1991) Calcium binding proteins and neuropeptides as molecular markers of GABAergic interneurons in the cat visual cortex. Exp Brain Res 84:538–544
Ellk's JH, Richards DE, Rogers JH (1991) Calretinin and calbindin in the retina of the developing chick. Cell Tissue Res 264:197–208
Enderlin S, Norman AW, Celio MR (1987) Ontogeny of the calcium binding protein calbindin D-28K in the rat nervous system. Anat Embryol 177:15–28
Ferrer I, Bernet E, Soriano E, Del Rio JA, Fonseca M (1990) Naturally occurring cell death in the cerebral cortex of the rat and removal of dead cells by transitory phagocytes. Neuroscience 39:451–458
Ferrer I, Soriano E, Del Rio JA, Alcántara S, Auladell C (1992) Cell death and removal in the cerebral cortex during development. Prog Neurobiol 39:1–43
Fox K (1992) A critical period for experience-dependent synaptic plasticity in rat barrel cortex. J Neurosci 12:1826–1838
Frassoni C, Bentivoglio M, Spreafico R, Sánchez MP, Puelles L, Fairén A (1991) Postnatal development of calbindin and parvalbumin immunoreactivity in the thalamus of the rat. Dev Brain Res 58:243–249
García-Segura LM, Baetens D, Roth J, Norman AW, Orci L (1984) Immunohistochemical mapping of calcium-bindin protein in the rat central nervous system. Brain Res 296:75–86
Heizmann CW (1984) Parvalbumin, an intracellular calcium-binding protein: distribution, properties and possible roles in mammalian cells. Experientia 40:910–921
Heizmann CW, Berchtold MW (1987) Expression of parvalbumin and other Ca2+ binding proteins in normal and tumor cells: a topical review. Cell Calcium 8:1–41
Heizmann CW, Braun K (1992) Changes in Ca2+-binding proteins in human neurodegenerative disorders. TINS 15:259–264
Heizmann CW, Hunzinker W (1990) Intracellular calcium-binding molecules. In: Bronner F (ed) Intracellular calcium regulation. Liss, New York, pp 211–248
Hendrickson AE, Van Brederode JFM, Mulligan KA, Celio MR (1991) Development of calcium-binding proteins parvalbumin and calbindin in monkey striate cortex. J Comp Neurol 307:626–646
Hendry SHC, Jones EG (1991) GABA neuronal subpopulations in cat primary auditory cortex: co-localization with calcium-binding proteins. Brain Res 543:45–55
Hendry SH, Jones EG, Emson DC, Lawson DE, Heizmann CW, Streit P (1989) Two classes of cortical GABA neurons defined by differential calcium-binding protein immunoreactivities. Exp Brain Res 76:467–472
Kosaka T, Heizmann CW (1989) Selective staining of a population of parvalbumin-containing GABAergic neurons in the cerebral cortex by lectins with specific affinity for terminal N-acetylgalactosamine. Brain Res 483:158–163
Kosaka T, Katsumaru H, Hama K, Wu JY, Heizmann CW (1987) GABAergic neurons containing the CA2+ binding proteins parvalbumin in the rat hippocampus and dentate gyrus. Brain Res 419:119–130
Kriegstein AR, Suppes T, Prince DA (1987) Cellular and synaptic physiology and epileptogenesis of developing rat neocortical neurons in vitro. Dev Brain Res 34:161–171
Lang U, Frotscher M (1990) Postnatal development of non-pyramidal neurons in the rat hippocampus (areas CA1 and CA3): a combined Golgi-electron microscope study. Anat Embryol 181:533–545
Luhmann HJ, Prince DA (1988) Postnatal development of GABAergic inhibition in rat neocortex. Soc Neurosci Abstr 14:189
Luhmann HJ, Prince DA (1991) Postnatal maturation of the GA-BAergic system in the rat neocortex. J Neurophysiol 65:247–263
Lund RD, Mustari MJ (1977) Development of geniculocortical pathways in rats. J Comp Neurol 173:289–306
Miller MW (1986) Maturation of rat visual cortex. III Postnatal morphogenesis and synaptogenesis of local-circuit neurons. Dev Brain Res 25:271–285
Miller MW (1988) Development of projection and local circuit neurons in neocortex. In: Peters A, Jones EG (eds) Cerebral cortex, vol 7. Plenum Press, New York, pp 133–175
Miller RJ (1991) The control of neuronal Ca2+ homeostasis. Progr Neurobiol 37:255–285
Morino-Wannier P, Fujita SC, Jones EG (1992) GABAergic neuronal populations in monkey primary auditory cortex defined by co-localized calcium-binding proteins and surface antigens. Exp Brain Res 88:422–432
Nicolelis MAL, Lin CS, Chapin JK (1991) Ontogeny of corticocortical connections of the rat somatosensory cortex. Somatos Mot Res 8:193–200
Nitsch R, Bergmann I, Küppers K, Mueller G, Frotscher M (1990) Late appearance of parvalbumin-immunoreactivity in the development of GABAergic neurons in the rat hippocampus. Neurosci Lett 118:147–150
Paxinos G, Törk I, Tecott LH, Valentine KL (1991) Atlas of the developing rat brain. Academic Press, San Diego New York Boston London Sydney Tokyo Toronto
Persechini A, Moncrief ND, Kretsinger RH (1989) The EF-hand family of calcium-modulated proteins. TINS 11:462–467
Puelles L, Sánchez MP, Spreafico R, Fairén A (1992) Prenatal development of calbindin immunoreactivity in the dorsal thalamus of the rat. Neuroscience 46:135–147
Sánchez MP, Frassoni C, Alvarez-Bolado G, Spreafico R, Fairén A (1992) Distribution of calbindin and parvalbumin in the developing cortex and its primordium in rat: an immunohistochemical study. J Neurocytol 21:717–736
Seto-Ohshima A, Aoki E, Semba R, Emson PC, Heizmann CW (1990) Appearance of parvalbumin-specific immunoreactivity in the cerebral cortex and hippocampus of the developing rat and gerbil brain. Histochemistry 94:579–589
Solbach S, Celio MR (1991) Ontogeny of the calcium-binding protein parvalbumin in the rat nervous system. Anat Embryol 184:103–124
Soriano E, Del Rio JA, Ferrer I, Auladell C, De Lecea L, Alcántara S, (1992) Late appearance of parvalbumin-immunoreactive neurons in the rodent cerebral cortex does not follow an “inside-out” sequence. Neurosci Lett 142:147–150
Stichel CC, Singer W, Heizmann CW, Norman AW (1987) Immunohistochemical localization of calcium-binding proteins, parvalbumin and calbindin D-28k, in the adult and developing visual cortex of cats: a light and electron microscopic study. J Comp Neurol 262:563–577
Swann JW, Brady RJ, Martin DL (1989) Postnatal development of GABA-mediated synaptic inhibition in rat hippocampus. Neuroscience 28:551–561
Tinner R, Oertle M, Heizmann CW, Bosshard HR (1990) Ca2+-binding site of carp parvalbumin recognized by monoclonal antibody. Cell Calcium 11:19–23
Vogt BA (1985) Cingulate cortex. In: Peters A, Jones EG (eds) Cerebral cortex, vol 4. Association and auditory cortex. Plenum Press, New York London, pp 89–149
Wise SP, Jones EG (1976) The organization and postnatal development of the commissural projection to the somatic sensory cortex of the rat. J Comp Neurol 168:313–344
Wise SP, Jones EG (1978) Developmental studies of thalamocortical and commissural connections in the rat somatic sensory cortex. J Comp Neurol 178:187–208
Zilles K (1985) The cortex of the rat. Springer, Berlin Heidelberg New York Tokyo
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Alcántara, S., Ferrer, I. & Soriano, E. Postnatal development of parvalbumin and calbindin D28K immunoreactivities in the cerebral cortex of the rat. Anat Embryol 188, 63–73 (1993). https://doi.org/10.1007/BF00191452
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DOI: https://doi.org/10.1007/BF00191452