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PubMed1985

Postnatal development of axosomatic synapses in the rat visual cortex: morphogenesis and quantitative evaluation.

Postnatal development of axosomatic synapses was studied in the rat visual cortex in order to obtain experimental data that may explain how the unequal distribution of asymmetric and symmetric synapses evolves on the soma of cortical neurons. Three types of synaptic junctions were identified: asymmetric or type 1 synapses, with postsynaptic densities greater than or equal to 20 nm, symmetric type 2 synapses, and symmetric synapses with an intermediate structure. The third synapse type had a structure similar to that of type 1 synapses, although the postsynaptic densities were thinner than 20 nm. Type 1 synapses developed in three phases. In phase 1, the first postnatal week, there were many free postsynaptic thickenings and immature synapses whereby a higher degree of postsynaptic differentiation was visible in comparison to the presynaptic elements. During the following 10 days, phase 2, type 1 synapses containing thin postsynaptic densities and intermediate synapses temporarily increased in number. Intermediate synapses are interpreted as precursors of type 1 synapses that have relatively immature postsynaptic elements. Toward the end of synaptogenesis, phase 3, the free postsynaptic thickenings reappeared while type 1 synapses containing well developed postsynaptic elements prevailed. Throughout the whole postnatal period, the numerical density of axosomatic type 1 synapses remained very low and the ratio of asymmetric to symmetric synapses at the neuronal somata was inversely proportional to that at the dendrites. Also, there was a significant decrease in the numerical density of type 1 synapses between postnatal days (P) 17 and 30. Data normalized according to cortical growth suggest that this is probably due to a decrease in the number of axosomatic type 1 synapses. This corresponds to the observation that in layers III and V a few type 1 synapses were found on pyramid-like cells up to P10 which then disappeared in later stages. Axosomatic type 2 synapses appear to be formed by two different presynaptic processes. The first presynaptic type contains flocculent material with glycogen granules and resembles axonal growth cones. These junctions contain multiple adhesion patches, intermediate junctions, one or more active zones, narrow synaptic clefts, and small pleomorphic vesicles. All of these are structural features of adult type 2 synapses. The growth-cone-like presynaptic elements disappeared after about 3 weeks. The second presynaptic type is smaller in size and also forms contacts with a structure similar to adult type 2 synapses.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗
PubMed1976

A quantitative comparison of the formation of synapses in the rat superior cervical sympathetic ganglion by its own and by foreign nerve fibres.

The rat superior cervical sympathetic ganglion (SCG) has about 36,000 neurones in a volume of about 1 cu.mm. There are about 8.8 X 10(6) synapses, and 6000-9000 preganglionic axons. Section of the preganglionic chain causes a loss of 93% of the synapses. In the denervated SCG there are 0.6 X 10(6) remaining ('intrinsic') synapses, and a proportion of the synaptic sites are identifiable as vacated synaptic thickenings (3 X 10(6) per SCG, as compared with 0.5 X 10(6) in the normal intact SCG). After deducting the intrinsic synapses, this indicates that each preganglionic axon forms about 1100 (900-1400) synapses. After freezing the preganglionic chain, subsequent axonal regeneration restores synapse numbers to 85% of normal (7.5 X 10(6) synapses per SCG). After anastomotic repair by suture of the cut ends of the preganglionic chain (a necessary control for the foreign nerve anastomoses), the SCG contains only 60% of the normal complement of synapses (5.2 X 10(6) synapses per SCG). The results of this anastomosis are very variable. However, in individual ganglia the numbers of synapses are directly correlated with the numbers of axons which reach the SCG. After deducting the intrinsic synapses it can be calculated that each axon forms about 700 synapses. This is probably an underestimation of the numbers which would be achieved at longer survival times. After anastomosis of the vagal nerve into the denervated SCG there are about 4.4 X 10(6) synapses per SCG. Morphologically the majority have axon terminals with large dense cored vesicles, and it is likely that these belong to the axons of the parasympathetic preganglionic neurones in the dorsal motor nucleus of the vagus. A smaller population of axon terminals are devoid of large dense cored vesicles; their origin is unknown. The dorsal motor nucleus of the vagus has between 1000 and 2000 neurones. After deducting the intrinsic synapses, this indicates that each axon may form up to 1900-3800 synapses. To the extent that other, unidentified vagal fibres also contribute to the synapses found after this anastomosis, this figure is an overestimate. After anastomosis of the hypoglossal nerve into the denervated SCG, there are 1.5 X 10(6) synapses per SCG. A morphologically distinctive type of axon terminal is found, and it is argued that this may belong to a special category of skeletomotor neurones located in the caudoventral part of the hypoglossal nucleus and distinguished by pseudocholinesterase staining. There are about 600 of these neurones, which would indicate that they form about 1500 synapses per axon (after deducting the numbers of intrinsic synapses). The majority of the hypoglossal neurones do not form intraganglionic synapses; this suggests that although the possession of a cholinergic mechanism may be necessary for axons to be able to form ganglionic synapses, it is not in itself sufficient. For each of the types of anastomosis, the numbers of vacated thickenings are inversely proportional to the numbers of synapses...

Acetyltransferases↗
PubMed1991

Perforated and non-perforated synapses in rat neocortex: three-dimensional reconstructions.

Perforated and non-perforated synapses in the molecular layer of rat parietal cortex have been assessed morphologically and quantitatively using three-dimensional reconstructions of the postsynaptic terminal. Perforated synapses were analyzed at nine ages, ranging from 0.5 to 22 months of age, and non-perforated synapses at three ages--0.5, 12, and 22 months. Examination of the reconstructions shows that perforated synapses increase in size and complexity with increasing age. This increasing complexity is reflected in a break-up of the postsynaptic density, which is punctuated by larger, branched perforations. In the most extreme cases the result is the appearance of isolated islands of postsynaptic density separated by, and also surrounded by, a synaptic contact zone. Spinules are especially prominent at around 12 months of age in perforated synapses, and the overall negative curvature of the young junctions is replaced by positively curved junctions from 4 months onwards. The non-perforated synapses are relatively small and show few changes with increasing age. Using the measurement option in the reconstruction program, the following trends emerged. All parameters of perforated synapses increased in size with increasing age, whereas the corresponding parameters of non-perforated synapses remained relatively unchanged over this age range. In addition, the percentage of the synaptic contact zone surface area occupied by the postsynaptic density decreased with increasing age in perforated synapses, but increased in non-perforated synapses. The total postsynaptic density surface area of non-perforated synapses per unit volume of molecular layer was double that of perforated synapses at 0.5 months, but the situation was reversed at 12 months. This parameter was similar in the 2 populations at 22 months. This suggests that perforated synapses contribute more to the total surface area of the postsynaptic density in mid- to late-adulthood than do non-perforated synapses, despite non-perforated synapses outnumbering perforated by 2-3:1 at these ages. These data provide more specific evidence that perforated and non-perforated synapses constitute separate synaptic populations from early in development, and that perforated synapses are responsible for the maintenance of neuronal postsynaptic density surface area from mid-adulthood onwards.

Animals↗
PubMed1984

Development of synapses on pyramidal and multipolar non-pyramidal neurons in the visual cortex of rabbits. A combined Golgi-electron microscope study.

A combined Golgi-electron microscope method was used to study the ultrastructural maturation of synapses on identified pyramidal and multipolar non-pyramidal neurons in the visual cortex of young and adult rabbits. In samples of 10 (time of eye opening), 14, 20 day old and 7 month old animals, fully impregnated pyramidal neurons within the layers II-V and multipolar non-pyramidal neurons mainly located in lower layer III and layer IV was studied. We found that synapses in 10 and 14 day old animals were occasionally immature in appearance. They were characterized by either a poorly defined postsynaptic band or equal rims of pre- and postsynaptic electron-dense material and could therefore not be classified as Gray type I or II. The distinction between both types of synapses was easier at day 20 and in the adults when the postsynaptic band of the asymmetrical (type I) synapses had become remarkably thicker. In pyramidal neurons the cytoplasmic organelles increased in number during development. Although a few symmetrical synapses were present on dendritic spines of pyramidal neurons in 14 and 20 day old animals, all pyramidal neurons exhibited the same types of synapses on specific sites of their neuronal surface. They received exclusively type II synapses on their somata, type I synapses on their dendritic spines and both types of synapses on their dendritic shafts. However, in the adult animals the frequency of occurrence of type II synapses, especially on basal dendritic shafts, had increased. In some cases only type II and no type I synapses were present. A striking finding in all young and adult animals was that synapses at the borderline between somata and apical dendritic shafts as well as on dendritic spines were frequently complex or interrupted. The characteristic ultrastructural features of adult spine-free and sparsely spiny multipolar non-pyramidal neurons e.g. the many cytoplasmic organelles and type I and II synapses on somata and on dendrites were already present at day 10. After day 10 the number of organelles and synapses increased prominently and in adult animals the different types of synapses on dendrites were located at relatively short intervals of about 4 microns. In contrast with the dendritic shafts of pyramidal neurons many asymmetrical synapses were observed on dendritic shafts of the non-pyramidal neurons analysed in the adult animals. Furthermore, it appeared that the number of synapses on these non-pyramidal neurons is about twice that on pyramidal neurons in day 20 old animals and about four times in adult animals.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗
PubMed1976

Dendroaxonic synapses in the substantia gelatinosa glomeruli of the spinal trigeminal nucleus of the cat.

The glomeruli in the substantia gelatinosa layer of the spinal trigeminal nucleus of the cat contain three kinds of dendritic processes. One of these, the type 2 dendrite, contains large synaptic vesicles in its spine heads and in its shafts. The type 2 dendrite receivers axodendritic synapses from primary trigeminal afferent (C) axons and an occasional axodendritic synapse from small axonal (P) endings with small synaptic vesicles. The type 2 dendrites in turn form dendroaxonic synapses on the C endings. The dendroaxonic synapse and the axodendritic synapse of the C ending typically occur in reciprocal pairs. The axodendritic synapse usually lies in the depths of scalloped depressions in the surface of the C ending while the dendroaxonic synapse is found on the rim of the depression. Type 1 spines, i.e., dendritic spines receiving axodendritic synapses from the primary ending and lacking synaptic vesicles, also receive dendrodentritic synapses from type 2 dendrites. The type 2 dendrite with its large, rounded synaptic vesicles is considered to be excitatory at its dendroaxonic and dendrodendritic synapses. The type 2 dendrites course from glomerulus to glomerulus receiving their excitatory input through the axodendritic synapses of C axons. A type 2 dendrite, in response to C axon excitation would activate type 1 spines directly through their dendrodendritic synapses (C leads to 2 leads to 1) and indirectly by increasing transmitter release at the axodendritic synapses of the C axonal endings through their dendroaxonic synapses (2 leads to C leads to 1). The type 2 dendrites could serve two functions. First, they may prolong transmitter release from the axodendritic synapses of C axonal endings beyond the time of arrival of incoming potentials because of the reciprocal pairing of dendroaxonic and axodendritic synapses (C in equilibrium 2). Second, they may extend the spatial range of the excitatory output of active primary afferent axons to type 1 spines of glomeruli whose primary afferent axons may be inactive (C leads to 2 leads to 1).

Animals↗
PubMed2000

Differential mechanisms of transmission at three types of mossy fiber synapse.

The axons of the dentate gyrus granule cells, the so-called mossy fibers, innervate their inhibitory interneuron and pyramidal neuron targets via both anatomically and functionally specialized synapses. Mossy fiber synapses onto inhibitory interneurons were comprised of either calcium-permeable (CP) or calcium-impermeable (CI) AMPA receptors, whereas only calcium-impermeable AMPA receptors existed at CA3 principal neuron synapses. In response to brief trains of high-frequency stimuli (20 Hz), pyramidal neuron synapses invariably demonstrated short-term facilitation, whereas interneuron EPSCs demonstrated either short-term facilitation or depression. Facilitation at all CI AMPA synapses was voltage independent, whereas EPSCs at CP AMPA synapses showed greater facilitation at -20 than at -80 mV, consistent with a role for the postsynaptic unblock of polyamines. At pyramidal cell synapses, mossy fiber EPSCs possessed marked frequency-dependent facilitation (commencing at stimulation frequencies >0.1 Hz), whereas EPSCs at either type of interneuron synapse showed only moderate frequency-dependent facilitation or underwent depression. Presynaptic metabotropic glutamate receptors (mGluRs) decreased transmission at all three synapse types in a frequency-dependent manner. However, after block of presynaptic mGluRs, transmission at interneuron synapses still did not match the dynamic range of EPSCs at pyramidal neuron synapses. High-frequency stimulation of mossy fibers induced long-term potentiation (LTP), long-term depression (LTD), or no change at pyramidal neuron synapses, interneuron CP AMPA synapses, and CI AMPA synapses, respectively. Induction of LTP or LTD altered the short-term plasticity of transmission onto both pyramidal cells and interneuron CP AMPA synapses by a mechanism consistent with changes in release probability. These data reveal differential mechanisms of transmission at three classes of mossy fiber synapse made onto distinct targets.

Animals↗
PubMed1986

Protein-synthetic machinery at postsynaptic sites during synaptogenesis: a quantitative study of the association between polyribosomes and developing synapses.

Previous studies have revealed dramatic accumulations of polyribosomes under growing spine synapses, suggesting a critical role for protein synthesis at the postsynaptic site during synaptogenesis. The present study quantitatively analyzes the distribution of polyribosomes under synapses during developmental synaptogenesis in the rat's dentate gyrus. The middle molecular layer of the suprapyramidal blade of the dentate gyrus was examined electron-microscopically at 1, 4, 7, 10, 15, 20, and 28 d of age. At each age, we evaluated (1) synapse density (the number of synapses/100 micron2 of neuropil), (2) the width of the molecular layer, (3) the proportion of spine synapses with underlying polyribosomes, and (4) the number of polyribosome-containing synapses/1000 micron2 of neuropil. From the first two measures, an estimate was obtained of the total extent of synaptogenesis, taking into account both the increase in synapse density and the increase in total area of neuropil. At 1 d of age, very few synapses were found in the molecular layer of the dentate gyrus, and those that were present were quite immature in appearance. Synapse density increased about 140-fold between 1 and 28 d of age, from an average of 0.36 synapses/100 micron2 at 1 d of age to 49 synapses/100 micron2 at 28 d of age. An inverse relationship was found between synapse density and the proportion of synapses with polyribosomes. Between 1 and 7 d of age, about 60% of the spine synapses had one or more polyribosomes under the spine base. Thereafter, the proportion of spines with polyribosomes decreased as synapse density increased. Similarly, the proportion of shaft synapses with underlying polyribosomes was greatest between 1 and 7 d postnatal, and decreased thereafter. While the proportion of synapses with polyribosomes was greatest between 1 and 7 d, the actual number of polyribosome-containing synapses/1000 micron2 of neuropil was negligible at 1 d, increased to a peak at 7 d of age, and then decreased as synapse density increased. Qualitatively, the most dramatic accumulations of polyribosomes were also found at 7 d of age. We conclude that spine-associated polyribosomes represent a structural specialization of dendrites at sites of synapse construction and as such may represent a marker for growing synapses. We propose that these elements produce protein(s) that are critically involved in the formation of the synaptic contact.

Animals↗
PubMed1976

Synapse formation in the mouse olfactory bulb. I. Quantitative studies.

A quantitative study of synapse formation in the mouse olfactory bulb has been carried out using serial sections. Volumetric synaptic density as well as absolute number of synapses per olfactory bulb for eight distinct synaptic types have been determined at 15 different ages, from the beginning of synapse formation at embryonic day 14 (E14) to postnatal day 44 (P44). Synapses are first found in appreciable numbers at E15 when both axo-dendritic and a few dendro-dendritic synapses occur in the presumptive glomerular layer. Initial synapse formation correlates closely with the reorientation of mitral cells from a primitive tangenital to a definitive radial direction. Synapse formation by mitral cell dendrites occurs after mitral cell axons have grown into the future olfactory cortical areas, either simultaneous with or before synapse formation by these axons. Virtually all synaptic types detected in adults have been found on the day of birth, consistent with the idea that olfaction is an important sensory modality for newborn mice. Volumeric density of a given synaptic type generally increases 50--100 times during development while the absolute number increases about 1,000 times. Synapses in glomeruli develop more precociously than those in the time of origin and differentiation of the principal postsynaptic elements of these two divisions (mitral cells and internal granule cells). Correlation of the time of synapse formation of various synaptic types with their putative excitary or inhibitory role determined in adult studies suggests that excitatory synapses generally form somewhat earlier, although throughout nearly all of synaptic development, both excitatory and inhibitory synapses are present. Reciprocal dendro-dendritic synapses in the external plexiform layer appear to have a special mode of formation. It is suggested that a granule-to-mitral dendro-dendritic synapse only forms next to an already existing mitral-to-granule synapse on the same gemmule.

Age Factors↗
PubMed1985

Polyribosomes under developing spine synapses: growth specializations of dendrites at sites of synaptogenesis.

We have previously reported that there is a dramatic increase in polyribosomes associated with dendritic spines during periods of synapse growth induced by denervating lesions. We suggested that polyribosomes at the postsynaptic site may somehow be involved in the growth of synapses. To evaluate this hypothesis further, the present study determines whether synapses which are growing in the developmental period also have accumulations of polyribosomes. We examined the dentate gyrus of the developing rat electron microscopically at 7, 10, 15, 20, and 28 days of age, which spans the major period of synaptogenesis in this structure. Qualitative observations revealed dramatic accumulations of polyribosomes under spine synapses in the youngest animals (7 and 10 days of age). With synapse development, the accumulations of polyribosomes became less dramatic, so that by 28 days of age, the neuropil of the dentate gyrus appeared qualitatively mature. To determine the relationship between polyribosomes under spine synapses and synapse development, quantitative electron microscopic methods were use to evaluate synapse density (number of synapses/100 micron 2), and the incidence of polyribosome-containing spines (proportion of spine synapses with underlying polyribosomes) in the neuropil of the dorsal blade of the dentate gyrus at each age. An inverse relationship was found between synapse density and the proportion of spines with polyribosomes. Synapse density increased in an almost linear fashion between 7 and 28 days of age to levels which were actually somewhat higher than in mature rats, whereas the incidence of polyribosome-containing spines was highest at the youngest ages and decreased with development. Thus, polyribosomes were most prominent under spine synapses during the period of maximal synapse growth. These results, together with our previous observations of increased numbers of polyribosomes under spines during lesion-induced growth, suggest that the polyribosomes represent a structural specialization of dendrites at sites of synapse construction. We propose that they produce protein(s) that are involved in synapse growth.

Animals↗
PubMed1993

Morphological characteristics of perforated synapses in the latter stages of synaptogenesis in rat neocortex: stereological and three-dimensional approaches.

Over recent years attention has been focused on perforated synapses (PSs), on account of their possible involvement in synaptic plasticity in the nervous system. The mechanism invoked has involved the conversion of conventional (non-perforated) synapses into perforated ones, with the latter subsequently splitting to form new daughter synapses. Data challenging this mechanism have emerged from studies using unbiased stereological and three-dimensional reconstruction procedures in early synaptogenesis and also in early- to mid-adulthood. The present study is an attempt to complement these earlier studies by concentrating on the latter part of synaptogenesis and early adulthood in rats (7-60 days postnatal). Using the disector method, the frequency of perforated synapses increases with age from 12% at seven days to 33% at 60 days. Reconstruction of the perforated synapses has led to the description of three sub-types, while quantitation of the reconstructions has highlighted major differences between perforated and non-perforated synapses over this developmental period. For instance, the postsynaptic density of perforated synapses increases in size with age, but remains static in the non-perforated variety; in addition, it is 2-3 times larger in perforated synapses. The proportion of the synaptic contact zone occupied by the postsynaptic density increases in perforated synapses with increasing age, but is static in non-perforated synapses. No evidence has been found to support a perforated synapse splitting model, since perforated synapses are present from early in synaptogenesis, the frequency of non-perforated synapses reaches a peak prior to, but not following, that of perforated synapses, and the size of the postsynaptic density of non-perforated synapses remains constant throughout the period of the study.

Animals↗
PubMed1999

Quantitative fine-structural analysis of olfactory cortical synapses.

To determine the extent to which hippocampal synapses are typical of those found in other cortical regions, we have carried out a quantitative analysis of olfactory cortical excitatory synapses, reconstructed from serial electron micrograph sections of mouse brain, and have compared these new observations with previously obtained data from hippocampus. Both superficial and deep layer I olfactory cortical synapses were studied. Although individual synapses in each of the areas-CA1 hippocampus, olfactory cortical layer Ia, olfactory cortical area Ib-might plausibly have been found in any of the other areas, the average characteristics of the three synapse populations are distinct. Olfactory cortical synapses in both layers are, on average, about 2.5 times larger than their hippocampal counterparts. The layer Ia olfactory cortical synapses have fewer synaptic vesicles than do the layer Ib synapses, but the absolute number of vesicles docked to the active zone in the layer Ia olfactory cortical synapses is about equal to the docked vesicle number in the smaller hippocampal synapses. As would be predicted from studies on hippocampus that relate paired-pulse facilitation to the number of docked vesicles, the synapses in layer 1a exhibit facilitation, whereas the ones in layer 1b do not. Although hippocampal synapses provide as a good model system for central synapses in general, we conclude that significant differences in the average structure of synapses from one cortical region to another exist, and this means that generalizations based on a single synapse type must be made with caution.

Animals↗
PubMed1991

Communicating synapses: types and functional interpretation. Exceptions to Cajal's neuron theory.

The neurons of the dorsal periaqueductal nucleus of the mesencephalon and their synaptic contacts were observed under a transmission electron microscope. We found various types of synapses which constituted an exception to Cajal's neuron theory (law of neuron independence). Some of these synapses had an open communicating or continuity 'passage' between the presynaptic bouton of a neuron (first neuron) and the postsynaptic portion of another neuron (second neuron). The 'communicating' passage (located in the synaptosome) is formed by the continuity of the presynaptic and postsynaptic membrane, and its limits or rims are the reflexion points of the membranes. When only two neurons intervene they could be termed 'simple communicating synapses'. We found three types: I = communicating axosomatic synapses; II = communicating axodendritic synapses, and III = communicating axoaxonic synapses'. When three neurons intervene in the synaptic contact, they could be termed 'complex communicating synapses'. In these, the first and second neurons form a normal synapse, but the lateral portion of the presynaptic bouton of the first neuron also enters into contact with a third neuron, with which it establishes an open communicating or continuity passage. The points of these passages are collateral to the synapse, and may be in the presynaptic or pre-postsynaptic portions simultaneously, communicating collaterally with the third neuron. We found a further three types: IV = complex communicating axosomatic and dendritic synapses; V = complex communicating axoaxonic and somatic synapses, and VI = complex communicating axodendritic and double-somatic synapses. It is suggested that communicating synapses may constitute an exception to Cajal's neuron theory, representing functional states for the acceleration, retardation or modulation of the synaptic function. The neurotransmitters would pass en masse through the communicating passage and the depolarization wave would pass through the rims without being retarded. In the simple communicating synapses, their action would be intensifying. In the complex communicating synapses, their action would be modulating or retarding, since the collateral communicating passage would function as an 'escape valve' through which part of the impulse reaching the presynaptic bouton would escape.

Animals↗
PubMed1993

Pre- and postnatal development of the primary visual cortex of the common marmoset. II. Formation, remodelling, and elimination of synapses as overlapping processes.

During ontogenesis changes in the numerical density of synapses are usually assumed to depend essentially on variations in the formation of synapses. Only the final adjustment to adult synapse densities is thought to include the elimination of synapses in some brain regions of certain species. Here, we focus attention on quantitative aspects of synapse elimination throughout development of area 17 of marmoset monkeys (Callithrix jacchus). Mature synapses, various precursor forms, and indicators of lysosomal degradation of synapses were quantitatively analysed by electron microscopy and morphometric methods. A total number of about 135 x 10(9) synapses was calculated for area 17 in each adult hemisphere corresponding to a volume density of 600 x 10(6) synapses/mm3. At 3 months of age, the respective values were 508 x 10(9)/area and 1,159 x 10(6)/mm3, while at birth these values were 69 x 10(9)/area and 328 x 10(6)/mm3. Consequently, at least three out of four synapses are eliminated between 3 months and adulthood. However, the real number of synapses being eliminated during development is probably much larger if the time course of lysosomal degradation is additionally taken into account. The frequency of lysosomes in presynaptic endings is highest before net-elimination of synapses occurs, i.e., between 1 and 3 months. This suggests that lysosomal degradation is not directly responsible for the majority of synapses removed during ontogenesis but apparently represents a second mechanism for synapse remodelling and elimination. Thus, it appears from this study that remodelling and elimination of synapses are quantitatively as important as their formation, and accompany synaptogenesis from its very onset onwards.

Animals↗