Synaptic development in the rabbit superior colliculus and visual cortex

Mathers, Lawrence H.; Mercer, K. Lynne; Marshall, Patricia

doi:10.1007/bf00235559

Cited by 34 publications

(9 citation statements)

References 40 publications

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“…Synaptogenesis entails the formation of presynaptic boutons containing synaptic vesicles and specialization of pre-and postsynaptic membranes, which results in the establishment of a synaptic junction between the pre-and postsynaptic structures. Developmental changes within pre-and postsynaptic structures are well documented in previous studies undertaken on different parts of the visual system of rat (Blue and Parnavelas, 1983a,b;Dyson and Jones, 1980;Lund and Lund, 1972) and other species (Cooper and Rakic, 1983;Cragg, 1975;Mathers et al, 1978;Winfield, 1981Winfield, , 1983) and seem to be universal for nervous tissue. Our electron-microscope observations confirm that the overall pattern of synaptic development is also occurring in the SGS.…”

Section: Morphogenesis Of Synaptic Structuresmentioning

confidence: 59%

Synaptogenesis in the stratum griseum superficiale of the rat superior colliculus

Warton

McCart

1989

Synapse

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The time course of synaptogenesis in the visual part of the superior colliculus (SC) of pigmented rats has been studied. The number of synaptic profiles per unit area and volume of neuropil in the stratum griseum superficiale (SGS) was estimated in seven groups of animals at ages 3, 9, 15, 21, 30, 49 and 85 days after birth. At 3 days only 1.5 +/- 0.06 synaptic contacts per unit area and 5.5 +/- 0.18 per unit volume were found. Most of them were immature contacts between growing processes. The density of synaptic contacts increased slowly during the first week. By day 9, 4.1 +/- 0.25 and 13.4 +/- 0.66 synaptic contacts were counted per unit of area and volume, respectively. A rapid synaptic proliferation occurred during the next 3 weeks and there were 7.7 +/- 0.27 and 25.5 +/- 1.04 synaptic contacts per unit area and volume at 15 days, 21.1 +/- 1.70 and 86.4 +/- 5.11 at 21 days, and 25.9 +/- 1.20 and 96.7 +/- 3.48 at 30 days. At the same time, the synaptic population gradually acquired more mature morphological characteristics: the pre- and postsynaptic structures became more specialized, the number of synaptic vesicles within presynaptic structures increased, and the synaptic junctional apposition became defined. After 30 days, a decrease in the density of synaptic profiles was recorded: 23.9 +/- 0.44 and 79.8 +/- 1.43 per unit area and volume of neuropil at 49 days and 13.4 +/- 0.53 and 49.7 +/- 2.40 at 85 days, respectively. Thus, after the phase of synaptic proliferation, a significant reduction of synaptic density occurred in the SGS neuropil until it was stabilized at the adult level by the third month of life. Considering the data available on the development of the retinal and visual cortical projections to the SC, the process of synaptic elimination, which takes place after the first postnatal month, does not appear to be directly connected with segregation of these particular projections.

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Section: Morphogenesis Of Synaptic Structuresmentioning

confidence: 59%

Synaptogenesis in the stratum griseum superficiale of the rat superior colliculus

Warton

McCart

1989

Synapse

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“…Synaptic development, in particular in the cerebral cortex, has been extensively studied in a wide variety of species (rat: Aghajanian and Bloom, 1967;Blue and Parnavelas, 1983;rabbit: Vrensen et al, 1977;Mathers et al, 1978;cat: O'Kusky, 1985;tree shrew: Ungersbock et al, 1991;marmoset: Missler et al, 1993;macaque: O'Kusky and Colonnier, 1982;Bourgeois and Rakic, 1993;rhesus monkey: Zecevic et al, 1989;Bourgeois et al, 1994;and man: Huttenlocher and de Courten, 1987). As a general rule, the rate of synapse formation was shown to be low in the beginning, then to sharply increase during a period of maximal synaptic production, and finally to fall again to low levels.…”

Section: Changes In the Overall Population Of Synapses In The Rat Sommentioning

confidence: 99%

“…A particularly well studied example of such a developmental mechanism is the overproduction and subsequent elimination of synapses, which is observed in a variety of species like cat (O'Kusky, 1985), marmoset (Missler et al, 1993), macaque (O'Kusky and Colonnier, 1982;Bourgeois and Rakic, 19931, rhesus monkey (Zecevic et al, 1989;Bourgeois et al, 1994), and man (Huttenlocher and de Courten, 1987). Nevertheless, this mechanism is by no means ubiquitous, and in other species, such as rat (Aghajanian and Bloom, 1967;Blue and Parnavelas, 1983), rabbit (Vrensen et al, 1977;Mathers et al, 1978), and tree shrew (Ungersbock et al, 1991), no overproduction of synapses has been observed and synaptic numbers were shown to increase gradually until adult values are reached. It is, however, important to remember that numerous synaptic populations exist in the cerebral cortex as defined by their source, molecular content, target specificity, etc.…”

mentioning

confidence: 93%

Quantitative aspects of synaptogenesis in the rat barrel field cortex with special reference to GABA circuitry

Micheva¹,

Beaulieu²

1996

J. Comp. Neurol.

257

136

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The postnatal establishment of cortical connectivity was studied by estimating the number (numerical density, synapse-to-neuron ratio, and total number) of the overall synaptic population and its distribution into gamma-aminobutyric acid (GABA)-immunopositive and GABA-immunonegative synaptic contacts in the developing rat somatosensory cortex. These numerical data were obtained using the unbiased disector method in combination with GABA postembedding immunocytochemistry. The numerical density of both synaptic populations was low in the early postnatal period (postnatal days 5 and 10, P5, P10) after which it abruptly increased between P10 and P15 to approach adult values. However, since cortical volume continues to increase after this age, the number of synapses per neuron and the total number of synapses reached adult values only by P30. There was no evidence of overproduction of either GABA or non-GABA synapses. Direct comparison between the two synaptic populations revealed a similar developmental pattern with the exception of the period around P20 when the production of GABA synapses slowed down. Thus, while the formation of non-GABA synapses proceeded in a continuous manner throughout the first month of life, GABA synapse production was accomplished in two consecutive waves. We suggest that the second delayed wave of GABA synapse formation is related to the great developmental plasticity of the cortical inhibitory system.

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“…The arrows at right indicate molecular weights of 100,000 ; 50,000 ; 25,000; and 15,000 . the number of multiple synapses (taken to be of retinal origin) in the superior colliculus increase sharply, reaching 85-90% of their adult level by 21 d after birth (11). Furthermore, the total protein-associated radioactivity rapidly transported into the superior colliculus increases sharply at -21 d after birth, indicating that growth of new axons into the superior colliculus or maturation of axons already in the superior colliculus continues through the period that GAP-43 is transported at elevated FIGURE 4 Induction of GAP-43 during hypoglossal nerve regeneration in rabbits .…”

Section: Rapidly Transported Proteins In Axotomized Adult Pns and Cnsmentioning

confidence: 99%

Axonally transported proteins associated with axon growth in rabbit central and peripheral nervous systems

Skene¹,

Willard²

1981

The Journal of Cell Biology

568

160

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In an effort to determine whether the "growth state" and the "mature state" of a neuron are differentiated by different programs of gene expression, we have compared the rapidly transported (group I) proteins in growing and nongrowing axons in rabbits . We observed two polypeptides (GAP-23 and GAP-43) which were of particular interest because of their apparent association with axon growth . GAP-43 was rapidly transported in the central nervous system (CNS) (retinal ganglion cell) axons of neonatal animals, but its relative amount declined precipitously with subsequent development. It could not be reinduced by axotomy of the adult optic nerves, which do not regenerate ; however, it was induced after axotomy of an adult peripheral nervous system nerve (the hypoglossal nerve, which does regenerate) which transported only very low levels of GAP-43 before axotomy. The second polypeptide, GAP-23 followed the same pattern of growth-associated transport, except that it was transported at significant levels in uninjured adult hypoglossal nerves and not further induced by axotomy. These observations are consistent with the "GAP hypothesis" that the neuronal growth state can be defined as an altered program of gene expression exemplified in part by the expression of GAP genes whose products are involved in critical growth-specific functions. When interpreted in terms of the GAP hypothesis, they lead to the following conclusions: (a) the growth state can be subdivided into a "synaptogenic state" characterized by the transport of GAP-23 but not GAP-43, and an "axon elongation state" requiring both GAPS; (b) with respect to the expression of GAP genes, regeneration involves a recapitulation of a neonatal state of the neuron ; and (c) the failure of mammalian CNS neurons to express the GAP genes may underly the failure of CNS axons to regenerate after axon injury .Certain rapidly transported proteins (which we have designated "growth-associated polypeptides" [GAPs]) are specifically induced during the regeneration of amphibian retinal ganglion cell axons (17). In the preceding paper we proposed that the GAPs are proteins involved in key functions related to axon growth and that their induction is a critical event in axon regeneration. The mammalian nervous system provides a particularly interesting and important system in which to further evaluate this hypothesis, because it is possible to distinguish between metabolic changes resulting from axon injury itself and those directly related to axon growth : mature neurons of the mammalian peripheral nervous system (PNS) (e.g., the hypoglossal and vagus nerves) retain the ability to regenerate their axons after injury, while those of the central nervous system (CNS) (e.g., the optic nerve and spinal cord) generally do not . The failure of CNS regeneration is an important clinical problem and in the past has been explained in terms of models emphasizing either extrinsic or intrinsic factors . A particularly durable extrinsic model has been that regenerating CNS axons are ph...

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Synaptic development in the rabbit superior colliculus and visual cortex

Cited by 34 publications

References 40 publications

Synaptogenesis in the stratum griseum superficiale of the rat superior colliculus

Synaptogenesis in the stratum griseum superficiale of the rat superior colliculus

Quantitative aspects of synaptogenesis in the rat barrel field cortex with special reference to GABA circuitry

Axonally transported proteins associated with axon growth in rabbit central and peripheral nervous systems

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