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M Colonnier

Publications and source records attributed to M Colonnier.

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Number and size of neurons and synapses in the motor cortex of cats raised in different environmental complexities.

In a previous study we have shown that the richness of the environment affects the number of neurons, the size of their nuclei, the number of round-asymmetrical synapses per neuron, the numerical density (number per unit volume; NV) of flat-symmetrical synaptic contacts, their number per neuron and their size in the visual cortex of cats. Of these, the number of flat-symmetrical synapses per unit volume is particularly affected (there are nearly twice as many per mm3 in the impoverished cortex). Several studies in the rat have shown that environmentally induced changes in cortical thickness occur in the occipital regions but are much smaller or absent in the frontal regions. In order to determine if the cat motor cortex is also resistant to environmental changes, we have estimated the number and size of neurons and of synapses in individual laminae of motor cortex, area 4 gamma, in six pairs of cats raised either in a colony (EC: enriched condition) or in isolation (IC: impoverished condition). For the neurons, we have found that the numerical density (28,900 neurons per mm3 of EC and 29,500 neurons/mm3 of IC motor cortex), the number under 1 mm2 of cortical surface (49,400 and 49,200 in EC and IC cats), and the size of the neuronal nuclei (82 vs 80 microns2 in EC and IC animals) were not significantly affected. The number of flat-symmetrical synapses per neuron (1,470 in EC vs 1,400 in IC cortex), their size (0.33 micron in both groups) and even their number per unit volume, which was so greatly affected in the visual cortex, remains unchanged (43 million/mm3 and 41 million/mm3 in EC and IC motor cortex). We did find however, a significant difference (p less than 0.05) in the numerical density of round-asymmetrical synapses which is 13% greater in the impoverished motor cortex (216 million/mm3 in EC vs 247 million/mm3 in IC cortex). Our results confirm that the motor cortex is much less affected by the richness of the environment than the visual cortex: In fact, the cat motor cortex is hardly affected at all. Furthermore our results represent the most complete data presently available on the number and size of neurons and synapses in individual laminae of the cat motor cortex.

Animals

Effects of the richness of the environment on six different cortical areas of the cat cerebral cortex.

The number and size of neurons and the cortical thickness were determined in areas 17, 18, 3B, 4 gamma, the posteromedial lateral suprasylvian area, and the primary auditive area of cats raised in an enriched and in an impoverished environment. A significant effect on the numerical density of neurons and on the size of the neuronal nuclei can be demonstrated in areas 17 and 18. We suggest that this preferential effect on occipital cortical regions is due to a different gradient of maturation among cortical regions.

Animals

Synaptophysin expression during synaptogenesis in the rat cerebellar cortex.

In order to study the mechanisms of synaptogenesis in the rat cerebellar cortex, a library of monoclonal antibodies has been generated against proteins of the isolated synapse. One recognizes a glycosylated 38 kDa protein that is concentrated in the synaptic vesicle fraction and resembles synaptophysin biochemically in its molecular weight, charge, and pattern of glycosylation. In the adult cerebellar cortex, the antisynaptophysin(mabQ155) immunoreactivity is codistributed with synapses. Immunoreactivity is strongest in the molecular layer where punctate deposits of reaction product outline the Purkinje cell dendrites. Discrete small profiles, consistent with the distribution of basket cell axon terminals, surround the Purkinje cells, and in the granular layer the synaptic glomeruli are intensely stained. There is no immunoreactivity in the white matter axon tracts. Electron microscope immunocytochemistry confirms the synaptic location of the antigen and suggests that the reaction product is associated with synaptic vesicles. Both round and flat vesicle populations are immunoreactive. Antisynaptophysin(mabQ155) has been used to follow synaptogenesis in the developing rat cerebellum. In the newborn rat (P0), despite the paucity of synapses, there is some specific immunoreactivity, especially in the subcortical white matter. Electron microscopy shows that the antigenicity is associated with vesicles within growth cones, filopodia, and immature axon profiles. During development, antisynaptophysin immunoreactivity increases progressively, along with the maturing cell populations, for both the granule cell-Purkinje cell and the mossy fiber-granule cell synapses. Quantitative biochemical analysis confirms the cytochemical results. These data suggest that neuronal growth cones express a synapse-specific antigen before complete morphological synapses are present.

Aging

Number of neurons in individual laminae of areas 3B, 4 gamma, and 6a alpha of the cat cerebral cortex: a comparison with major visual areas.

The number of neurons per mm3 of tissue (number per volume) and the number under 1 mm2 of cortical surface (number per column) have been estimated for each lamina of seven cytoarchitectural areas of the cat cortex by using a method of size frequency distribution. The areas studied consisted of four visual areas (the binocular and monocular portions of area 17: 17B and 17M; area 18; and the posteromedial lateral suprasylvian area: PMLS), a somatosensory area (3B), and two motor areas (4 gamma and 6a alpha). For both series of measurements, significant differences could be demonstrated among the seven areas studied (one-way ANOVA; P less than .001). The number of neurons per volume in the binocular and monocular regions of area 17 (approximately 49,000/mm3) is 85% greater than that of each of the other regions (approximately 27,000) with a P less than .01 on an a posteriori Tukey test, but there are no significant differences between the latter areas. The number of neurons per column is greater in the binocular portion of area 17 (78,000 under 1 mm2 of cortical surface) than in any other area (P less than .01). Other sensory areas (17M, 18, PMLS, and 3B) have fewer neurons per column (P less than .01) and the numbers do not vary significantly between these regions (range from 56,100 to 61,900). Areas 4 gamma and 6a alpha have still fewer neurons (approximately 44,000; P less than .01, except P less than .05 when compared to PMLS). Thus, the seven areas studied fall under three different categories. Motor areas have the smallest number of neurons per column, sensory areas have more, and the greatest number is found in the binocular region of area 17. It appears that these differences are principally (but not exclusively) due to variations in the number of neurons in layer IV: These variations are largely responsible for the differences that we have found between the binocular portion of area 17 and other sensory areas as well as between the latter and motor areas. We thus cannot confirm the view of Rockel et al. (Brain 103:221-244, '80) that there is a basic uniformity of the number of neurons per unit of cortical surface in different cortical areas of the cat.

Animals

Richness of environment affects the number of contacts formed by boutons containing flat vesicles but does not alter the number of these boutons per neuron.

A recent quantitative analysis of cat visual cortex has demonstrated that the numerical density (Nv) of symmetrical synaptic contacts formed by boutons containing flat vesicles (FS synapses) is nearly twice as large in animals raised in isolation (impoverished condition: IC) as in animals raised in a colony (enriched condition: EC). Although some FS synapses have been shown to be cholinergic there is evidence that many, indeed the vast majority, are GABAergic. In order to estimate whether the change in the Nv of FS contacts was accompanied by a change in the number of boutons containing GABA, we have incubated sections of tissue from both groups of animals in an antiserum for GAD. In spite of the large increase in the number of FS contacts in impoverished cortex, we saw no obvious change in the apparent amount of labelled GAD terminals. In retrospect we realized that though the amount of labelled GAD terminals might reasonably be expected to reflect the number of F-boutons, it might not correspond so closely to the number of contacts formed by these boutons (which is what we had measured in the previous study): The richness of the environment could conceivably affect the number of contacts formed by the F-boutons without affecting the number of boutons! We thus extended our study by estimating the number of F-boutons in the two conditions. For the total cortical thickness, the Nv of F-boutons is only 17% lower (P less than .05) in enriched than in impoverished cats. The diameter of the boutons is 6% larger (P less than .001) in the enriched cortex. Because the F-boutons become fewer in number as they become larger in size, the total percentage volume occupied by these boutons does not change between the two experimental conditions. We conclude that this is the reason why there appears to be no change in the general amount of GAD label between the two groups of cats. More importantly, since the Nv of neurons is also 17% lower in enriched cortex, the number of F-boutons per neuron (and presumably the total number of F-boutons in the visual area) actually remains unchanged. In contrast, the previous study showed that the number of FS contacts per neuron is significantly decreased in enriched cortex. It follows that the number of contacts formed by each bouton must be altered.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals

An electron microscope study of synaptic contacts in the abdominal ganglion of Aplysia californica.

The fine structure of the abdominal ganglion of Aplysia californica has been studied in preparations fixed by immersion in aldehydes, either directly or after a survival of a few hours in artificial sea water. The central core of neuropil is surrounded by a rind of neuronal cell bodies floating in a subcapsular space containing a loose meshwork of neuronal and glial processes, separated by wide extracellular spaces. Large primary processes with deeply infolded membranes leave the neuronal perikarya and enter the neuropil where they branch into smaller processes containing either neurofilaments, neurotubules or both. Some have the appearance of initial segments. The neuropil is not a homogeneous structure. Rather, four types of zones can be distinguished: (1) zones of fibers of passage coursing together in the neuropil and making few synaptic contacts: (2) zones of neurosecretory fibers containing large granules and dense-core vesicles, again making few synaptic contacts: (3) zones with a great variety of synaptic contacts between medium size and small profiles; and (4) glomerular zones. The differentiated membranes of the synapses are characterized by a slight increase in density and by being regularly parallel to each other. Presynaptic densities are sometimes quite prominent but specialized dense cytoplasmic opacities have never been seen bordering the postsynaptic membranes, i.e., all synapses are of the symmetrical type. Interlemmal opacities vary considerably in density. In zone 3, the synaptic vesicles are of several sizes, are round, oval or flat, and are either clear or filled with different types of dense material. The population of vesicles within a single profile may consist either of a homogeneous group of similar vesicles or of various mixtures of two or three kinds of vesicles. In profiles with mixtures of clear and large dense-core vesicles, it is often only the clear vesicles which agglomerate towards the differentiated membranes. In such cases the large dense-core vesicles lie as a peripheral halo around the clear vesicles. Here, and especially in other large neuronal profiles not forming contact in the plane of section, they can be seen to associate specifically with mitochondria and glycogen. It is proposed that they do not contain neurotransmitters but are related to mitochondrial activities such as the storage of ATP or the movement of calcium ions. In profiles with mixtures of clear and small dense-core vesicles, both types of vesicles often touch the presynaptic membrane, suggesting the release of two transmitters or of a modulator or neurohormone with a transmitter, by a single terminal. Serial synapses are present in this zone. The glomerular zones contain small profiles forming many synaptic contacts, some of which are arranged in such a way as to suggest the existence of "reciprocal" serial synapses.

Animals

Synaptic contacts on glial cells in the abdominal ganglion of Aplysia californica.

Two types of glial cells have been identified in the neuropil and in the subcapsular space of the abdominal ganglion of Aplysia californica. In the neuropil, a first type of glial cell has a light staining cytoplasm and gives rise to processes which may contain bundles of filaments, a flocculent material or bundles of microtubules and membranous sacs. Synaptic contacts have been seen very rarely on their somata and more frequently on their "filamentous" and "flocculent" processes. A second type of glial cell has a darkly staining cytoplasm and gives rise to dense processes. Synaptic contacts are frequently seen on these processes. In the subcapsular zone, there are also two types of glial cells, one with a clear and the other with a dense cytoplasm. The processes of the clear glial cells contain glycogen-like particles and sometimes bundles of filaments. These processes surround the bundles of neuronal profiles which form the perisomatic plexus. Such enveloping processes receive synaptic contacts from the neuronal profiles in the bundles. The dense glial cells of the subcapsular zone also receive synaptic contacts, but this is a rare occurrence.

Animals

Thalamic projections of the superior colliculus in the rhesus monkey, Macaca mulatta. A light and electron microscopic study.

The projections of the superior colliculus to the thalamus have been studied in the monkey, Macaca mulatta, with anterograde degeneration techniques. The superior colliculus has been shown to project to the inferior nucleus of the pulvinar in a topographical manner with the lower visual field represented dorsomedially and the upper field ventrolaterally. The peripheral zone is located along the medial border and the fovea at the dorsolateral angle adjacent to the lateral geniculate nucleus. The superior colliculus also sends a dense projection to the ipsilateral intralaminar complex, i.e., to the parafascicular, central lateral and paracentral nuclei, and a lesser projection to the same contralateral nuclei. Degenerating tectal fibers were also found in the lateral geniculate nuclei. Four types of vesicle containing profiles were observed in the inferior pulvinar and paracentral nucleus. The large RL and small RS terminals contain round vesicles of uniform size and form asymmetric contacts mainly with large and small dendrites respectively. The F terminal contains a mixture of small round and flat vesicles. It forms symmetric contacts with dendrites and cell somata. The P profile is very pale and contains a relatively sparse population of vesicles showing a great variation in size. It forms symmetric contacts with medium to large dendrites. It is frequently found postsynaptic to the other types, especially the RL terminal, and is regularly seen as the intermediate element of serial and triadic synaptic arrangements. The experimental electron microscopic study has shown that many fibers from the superior colliculus terminate as RL profiles, undergoing direct dense degeneration, in both the inferior pulvinar and the paracentral nucleus. Others probably end as smaller RS terminals.

Afferent Pathways

Synaptic patterns in the visual cortex of turtle: an electron microscopic study.

The part of turtle general cortex that receives afferent fibers from the dorsal lateral geniculate nucleus and that shows evoked potentials to light stimuli has been studied with the electron microscope. This cortex consists of an outer molecular layer, a perikaryal layer, and a subcellular layer lying on a row of ependymal cell bodies. Neurons in the perikaral lamina are characterized by long spine-bearing apical dendrites ascending through the outer molecular layer and short finer basal dendrites in the subcellular zone. Scattered neurons without apical dendrites occur in both the molecular and subcellular zones. Two types of dendritic spines can be distinguished. Some are large, have a complex irregular shape, contain a variety of membranous sacs and mitochondria, and occasionally, a single bundle of microtubules embedded in an electron-dense background [corrected] opacity. These large spines are the most common postsynaptic element in the outer third of the molecular layer, where they are located on the distal enlargement that contains only electron-dense fuzz. They are the most common post-synaptic element in the lower two-thirds of the molecular layer where they arise from the proximal portion of apical dendrites. Most synaptic contacts are found on the dendritic spines and are of the "round-asymmetrical" type. Not infrequently "flat-symmetrical" synapses are coupled to "round-asymmetrical" contacts on individual large spines. The few contacts present on spine-bearing dendritic shafts are of both types. Axo-somatic contacts are mainly of the "flat-symmetrical" variety. Thus the synaptic patterns on the principal cells of turtle visual cortex are remarkably similar to those found on pyramidal cells of mammalian neocortex. In addition, however, axon terminals, dendrites and glial (ependymal) processes were often seen to give rise to membranous pouches containing large vacuoles and invaginating into dendritic shafts or spines. Rarely, axon terminals were seen to form contacts, identical in appearance to synaptic contacts, on cell bodies in the ependymal lining. More frequently, unusual types of membrane differentiations were present at the site of apposition of the membranes of axon terminals and ependymal processes. They are interpreted as functional neuroependymal contacts.

Animals