A quantitative electron microscopic study of synaptogenesis in the dentate gyrus of the rat

Crain, Barbara J.; Cotman, Carl W.; Taylor, Dwan A.; Lynch, Gary

doi:10.1016/0006-8993(73)90088-7

Cited by 343 publications

(125 citation statements)

References 14 publications

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“…While the hippocampus and prefrontal cortex do not appear to be functional neonatally, the olfactory bulb has a uniquely important role in neonatal learning, and CORT may have direct effects on olfactory bulb odor processing (Crain, Cotman, Taylor, & Lynch, 1973;Fanselow & Rudy, 1998;Sananes & Campbell, 1989;Stanton, 2000;Sullivan et al, 2000;reviews Hofer & Sullivan, 2001;Sullivan, in press). Specifically, during neonatal learning, olfactory bulb norepinephrine (NE) from the locus coeruleus (LC) is necessary for learning.…”

Section: Discussionmentioning

confidence: 99%

Corticosterone Influences on Mammalian Neonatal Sensitive-Period Learning.

Moriceau

Sullivan

2004

Behavioral Neuroscience

104

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Infant rats exhibit sensitive-period odor learning characterized by olfactory bulb neural changes and odor preference acquisitions critical for survival. This sensitive period is coincident with low endogenous corticosterone (CORT) levels and stress hyporesponsivity. The authors hypothesized that low corticosterone levels modulate sensitive-period learning. They assessed the effects of manipulating CORT levels by increasing and removing CORT during (Postnatal Day 8) and after (Postnatal Day 12) the sensitive period. Results show that (a) exogenous CORT prematurely ends sensitive-period odor-shock-induced preferences; (b) adrenalectomy developmentally extends the sensitive period as indicated by odor-shock-induced odor-preference learning in older pups, whereas CORT replacement can reinstate fear learning; and (c) CORT manipulation modulates olfactory bulb correlates of sensitive-period odor learning in a manner consistent with behavior.Sensitive periods for enhanced learning have been documented in a wide range of species. For example, language acquisition in humans is more easily learned prior to puberty, the ewe has a few hours postpartum when she may bond with her lamb, and imprinting in avian species occurs during the first few hours posthatching. However, sensitive periods can also involve suppression of other types of learning that could interfere with attachment and learning about the mother, such as fear conditioning, inhibitory conditioning, and passive avoidance

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Section: Discussionmentioning

confidence: 99%

Corticosterone Influences on Mammalian Neonatal Sensitive-Period Learning.

Moriceau

Sullivan

2004

Behavioral Neuroscience

104

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“…The dentate gyrus is immature at birth, and only 5%0 of its ultimate population of synapses appear to have formed at 11 days (32). Such marked developmental immaturity could be imagined to pose few constraints on synaptic reorganization and, hence, on functional compensation after trauma.…”

Section: Discussionmentioning

confidence: 99%

Synaptic Rearrangement in the Dentate Gyrus: Histochemical Evidence of Adjustments after Lesions in Immature and Adult Rats

Cotman¹,

Matthews²,

Taylor³

et al. 1973

Proc. Natl. Acad. Sci. U.S.A.

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147

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In immature animals, ablation of the entorhinal cortex elicited a rapid intensification of acetylcholinesterase (EC 3.1.1.7) staining in the outer one-quarter of the molecular layer of the dentate gyrus. Subsequent lesions of the septum eliminated this acetylcholinesterase intensification. Electron-microscopic histochemical analysis demonstrated a 30-fold increase in the number of acetylcholinesterase-positive synaptic endings in the intensification zone. The acetylcholinesterase augmentation thus appears attributable, in part at least, to an increase in the number of acetylcholinesterase-rich synaptic endings established by septo-hippocampal fibers. Observations in a comparative study -of immature and adult rats point to the animal's developmental state as a major determinant of differences in these lesion-induced neuronal adjustments.Both the anatomical and functional effects of brain injury are generally attributed solely to the loss of damaged or ablated neurons. Findings in recent experiments indicate that this view of the effects of brain lesions needs to be reexamined. Under some conditions, axons from intact neurons grow into areas vacated by the axons of damaged neurons and form new synapses that reoccupy the vacated synaptic territories (1-9).If such capacity for neural reorganization is a general property of brain tissue, these findings have several important implications for understanding the consequences of brain damage. First, in efforts to explain the physiological and behavioral effects of brain lesions it may become necessary to consider not only the net loss of neurons caused by the lesion, but also a possible secondary effect: the formation of new connections by intact neurons. Second, the reorganization of neuronal circuitry after brain damage could explain the frequently observed, but poorly understood, phenomenon of partial recovery of function after brain damage. Third, these findings have demonstrated that neuronal organization is much more dynamic than was heretofore realized; in fact, it has already been suggested that synaptic rearrangements are continuously taking place in the brain even under normal conditions (10). Thus, the induction of reactive synaptogenesis by a brain lesion provides a method of investigating what might well be one of the bases of functional plasticity in normal animals.We examined changes in the organization of the synapse population in the dentate gyrus of the rat's hippocampal formation after lesions that selectively destroy the massive Abbreviation: AChE, acetylcholinesterase. afferent system originating in the entorhinal cortex. In studies of synaptic reorganization, the dentate gyrus offers several advantages: (a) its normal synaptic organization is simple and well defined; (b) it is suitable for electrophysiological recording (11) so that the functional significance of any known structural changes eventually may be assessed; (c) the afferents of the dentate gyrus are accessible to experimental manipulation (e.g., surgical lesion); and (d) the syst...

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“…Electron microscopy of brain tissue that has been selectively stained with phosphotungstic acid for visualization of synapses has demonstrated that the number of synapses in various regions of the rat brain increases markedly between 1 and 4 weeks postnatally (13)(14)(15)(16). Synaptic vesicles have been shown to increase with a time course similar to that for synaptic membranes (16).…”

Section: Methodsmentioning

confidence: 99%

Ontogeny of synaptic phosphoproteins in brain.

Lohmann¹,

Ueda²,

Greengard³

1978

Proc. Natl. Acad. Sci. U.S.A.

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The ontogeny of two endogenous substrates for cyclic AMP-dependent protein kinase (ATP:protein phosphotransferase; EC 2.7.1.37) has been studied in rat and guinea pig cerebrum. These endogenous substrates, referred to as proteins Ia and Ib, have been shown in other studies to be specific to nervous tissue and to be enriched in the synaptic membrane and synaptic vesicle fractions of adult brain. In the present study, proteins Ia and lb were shown to increase markedly during the time of major synaptogenesis in rat cerebrum and guinea pig cerebrum, in which the morphological development of synapses is predominantly postuatal and prenatal, respectively. Similar results were obtained either by measuring endogenous phosphorylation of proteins Ia and lb in the synaptic membrane fraction or by measuring phosphorylation of extracted proteins Ta and lb with added protein inase. Phosphorylation of synaptic membrane proteins has been proposed as a mechanism for mediation or modulation of synaptic transmission (1). Synaptic 10 sec at 300, and the reaction was terminated by the addition of 50 Ml of a "sodium dodecyl sulfate (NaDodSO4)-stop solution," containing 6% NaDodSO4, 6% 2-mercaptoethanol, 15% glycerol, and a small amount of bromphenol blue, in 0.2 M Tris-HCI (pH 6.7). This mixture was boiled for 3 min, and aliquots (50 Al) were subjected to NaDodSO4/polyacrylamide slab gel electrophoresis, as described (3). In order to improve the resolution of proteins Ia and Tb, we modified the NaDodSO4/ polyacrylamide gels from those formerly described (3) so that they contained 6% acrylamide/0. 16% N,N'-methylenebisacrylamide in the separation gel and 3% acrylamide/0.08% N,N'-methylenebisacrylamide in the stacking gel. To improve resolution of these proteins further, we used longer (17 cm) separation gels.Extraction of Protein I. Rat or guinea pig cerebra were homogenized in 9 vol of ice-cold distilled water at 900 rpm in a glass-Teflon homogenizer. The homogenates were centrifuged at 150,000 X g for 30 min to obtain the total particulate fraction. The pellets, which contained virtually all of the protein I present in the homogenates, were resuspended in the original volume of ice-cold distilled water by homogenization at 900 rpm. For extraction of protein I, aliquots (2 ml) of the resuspended membranes were adjusted to pH 3.0 with 0.1 M HC1 and centrifuged at 50,000 X g for 15 min. (Essentially identical amounts of protein I were obtained with pH values ranging from 2.5 to 3.2.) The supernatant, containing the extracted protein I, was removed, neutralized by the addition of 600 Ml of 0.5 M sodium phosphate buffer (pH 6.0), and centrifuged again at 50,000 X g for 15 min. [ Values of pHThe costs of publication of this article were defrayed in part by the payment of page charges This article must therefore be hereby marked "advertisement" in accordance with 18 U. S. C. §1734 solely to indicate this fact. 4037Abbreviations: Hepes, 4-(2-hydroxyethyl)1-piperazineethanesulfonic acid; iBuMeXan, 3-isobutyl-1-methylxanthine; NaDo...

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A quantitative electron microscopic study of synaptogenesis in the dentate gyrus of the rat

Cited by 343 publications

References 14 publications

Corticosterone Influences on Mammalian Neonatal Sensitive-Period Learning.

Corticosterone Influences on Mammalian Neonatal Sensitive-Period Learning.

Synaptic Rearrangement in the Dentate Gyrus: Histochemical Evidence of Adjustments after Lesions in Immature and Adult Rats

Ontogeny of synaptic phosphoproteins in brain.

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