Synaptic termination of afferents from the ventrolateral nucleus of the thalamus in the cat motor cortex. A light and electron microscopy study

The synaptic termination in the cat motor cortex of afferents from the ventrolateral nucleus of the thalamus (VL) has been studied with experimental light and electron microscopic methods. The distribution of normal synapses on motor cortex pyramidal, stellate, and Betz cells was also examined. Synapses in the motor cortex can be classified into two general types. The first and most prominent type contains flat vesicles, lacks a compact postsynaptic density, and corresponds to Colonnier's ('68) symmetrical synapse. Stellate neurons receive synapses of both types on their cell bodies and proximal dendritic shafts, while pyramidal cells have only symmetrical synapses at these sites. The dendritic spines of both stellate and pyramidal cells are contacted by predominantly asymmetrical synapses. Betz cells, like smaller pyramidal neurons, receive only symmetrical synapses on their cell bodies. The proximal portions of the Betz cells apical dendrites, however, receive both asymmetrical and symmetrical synapses. Following VL lesions, degenerating synapses were mainly found in three cortical layers: the upper third of layer I (18%), layer III (66%), and layer VI (13%). Degenerating synapses were not seen in the lower two-thirds of layer I or in layer II, and were only rarely seen in layer V (3%). Ninety-one percent of the VL synapses were found on spines and 8% on stellate-type dendritic shafts. Stellate cell bodies rarely received VL synapses (1%) and none occurred on pyramidal or Betz cell bodies and their proximal dendrites. A VL synapse within layer III was found on two dendritic spines of a Betz cell apical dendrite. Thus, part of the VL input to layer III synapses on the processes of both motor cortex output neurons (Betz cells in layer V) and cortical interneurons (stellate cells in layer III).     

Intrinsic circuitry: synapses involving the local axon collaterals of corticocortical projection neurons in the mouse primary somatosensory cortex

Pyramidal neurons in the mouse SmI cortex were labeled by the retrograde transport of horseradish peroxidase (HRP) injected into the ipsilateral MsI cortex. Terminals of the local axon collaterals of these neurons (CC terminals) were identified in SmI, and their distribution and synaptic connectivity were examined. To avoid confusion, terminals in SmI cortex labeled by the anterograde transport of HRP injected into MsI were eliminated by lesion-induced degeneration. Lesions of MsI were made 24 hours after the injection of HRP; postlesion survival time was 4 days. Most CC axon terminals occurred in layers III and V where they formed asymmetrical synapses. Of 139 CC synapses in layer III and 104 in layer V, approximately 13% were formed with dendritic shafts. Reconstruction of 19 of these dendrites from serial thin sections showed them to originate from both spiny and nonspiny neurons. Most synapses of CC terminals (about 87%) were onto dendritic spines. In contrast, White and Keller (1987) demonstrated that terminals belonging to the local axon collaterals of corticothalamic (CT) projection cells synapse mainly with dendritic shafts of nonspiny neurons: 92% onto shafts, the remainder onto spines. The distribution of asymmetical synapses onto spines and dendritic shafts was analyzed for neuropil in layers III, IV, and V. Depending on the layer, from 34 to 46% of the asymmetrical synapses in the neuropil were onto dendritic shafts. Results showing that CC and CT terminals form proportions of axodendritic vs. axospinous synapses that differ from each other, and from the neuropil, indicate that local axon collaterals are highly selective with regard to their postsynaptic elements.     

Light and electron microscopic characterization of dopamine-immunoreactive axons in human cerebral cortex.

The distribution and synaptic connections of dopamine axons were studied by light and electron microscopy in human cerebral cortex. For this purpose, dopamine immunoreactivity was characterized in apparently normal anteriolateral temporal cortex, which was removed to gain access to the medial temporal lobe during tumor excision or treatment of epilepsy. Nissl sections showed this to be granular neocortex. Dopamine fibers were distributed throughout this cortex, although there were relatively more fibers in layers I-II and in layers V-VIa, compared to layers III-IV and VIb, resulting in a bilaminar pattern of labeling. In all layers, fibers were seen to form numerous varicosities, and to vary in size from thick to very fine. Fibers were relatively straight, sparsely branched and were oriented in various planes within the cortex. However, in layer I, they often ran parallel to the pial surface. In order to analyze the functional interactions of dopamine fibers, individual cortical layers were surveyed for dopamine synapses. These were usually symmetrical (Gray's type II), although 13% of them were asymmetrical. Approximately 60% of dopamine synapses were made with dendritic spines, and 40% with dendritic shafts, and this ratio was similar in all layers. On both spines and shafts, it was common to see dopamine synapses closely apposed to an unlabeled asymmetric input, suggesting a dopamine modulation of excitatory input. Some postsynaptic dendritic shafts had features of pyramidal cells, including formation of spines. Since pyramidal cells are the major type of cortical spiny neuron, they probably represent the main target of dopamine synapses in this cortex. There were also dopamine profiles apposed to membrane densities on unlabeled axon terminals, suggesting another type of synaptic interaction. These findings provide the first documentation of dopamine synapses in the human cortex, and show that they form classical synaptic junctions. The location of these synapses on spines and distal dendrites, and their proximity to asymmetric synapses, suggest a modulatory role on excitatory input to pyramidal cells.     

Combined golgi and electron microscopic study on the synapses formed by double bouquet cells in the visual cortex of the cat and monkey

The morphology of certain Golgi-stained cells was examined in the striate and peristriate cortex of the cat and in the striate cortex of the rhesus monkey. Neurons in layer III were selected on the basis of their characteristic vertical axon bundles, which are 20–150 μ in diameter and traverse layers II–V Selected neurons were examined under the electron microscope to characterize their synapses and to establish their postsynaptic targets. It was found that double bouquet cells form symmetrical or type II synapses. In the cat the postsynaptic membrane specialization was more extensive than in the monkey. After removing the Golgi precipitate from boutons of two cells in the cat, small pleomorphic and flattened vesicles were found in the boutons Earlier suggestions that double bouquet cells make synapses preferentially with spines of apical dendrites could not be confirmed. Out of 66 boutons in area 17 of the cat, 86.4% formed synapses with dendritic shafts, many of them belonging to nonpyramidal cells, 9% with perikarya of nonpyramidal cells, and only 4.6% with spines. Out of 19 synapses examined in area 18, 74% were contacting dendritic shafts and the rest contacted spines. In the monkey 60% of a total of 35 double bouquet cell synapses made synapses with dendritic shafts. A different type of double bouquet cell with densely spiny dendrites is also described in layer IV of the monkey striate cortex. This neuron formed asymmetrical synapses It is suggested that layer III double bouquet cells with vertical axon bundles are probably inhibitory and act on other nonpyramidal cells and certain parts of pyramidal cells.     

Structure of the piriform cortex of the opossum. I. Description of neuron types with golgi methods

The piriform cortex was studied in the adult opossum with rapid Golgi and Golgi-Cox techniques. Most pyramidal cells in the deep part of layer II and layer III resemble those in other parts of the cerebral cortex by virtue of a single apical dendritic trunk, multiple basal dendrites, a large number of small to medium dendritic spines, and a deeply directed axon. Pyramidal cells in the superficial part of layer II are similar with the exception that “secondary” apical dendrites often emerge directly from the cell body rather than from a single primary trunk. With conservative criteria for categorization, nine different types of nonpyramidal cells were distinguished, four of which have not been previously described. Layer I contains a small number of neurons with both smooth and spiny dendrites including distinctive fusiform cells with large somatic appendages. As in other species, the most common type of nonpyramidal neuron in layer II is the semilunar cell which has only apically directed dendrites. These cells have distinctive large spines confined to their distal dendritic segments. The mid to deep portion of layer III contains multipolar neurons with smooth dendrites that resemble the well-known large stellate cells in neocortex. In addition, layer III contains three non-pyramidal neuron types with spiny dendrites: (1) fusiform and multipolar cells with complex, branched dendritic appendages and somatic spines, (2) very large multipolar cells (up to 35 μm mean diameter) with large-diameter dendrites that give rise to abruptly tapering side branches and filiform spines, and (3) multipolar cells with profusely spiny dendrites. In all three layers, small neurons have been found with spherical cell bodies and “axoniform” dendrites that resemble the so called neurogliaform neurons described in a variety of brain areas. A striking feature of the organization of the piriform cortex is that, with the exception of the neurogliaform neurons, the different types of nonpyramidal cells tend to be segregated in individual layers or sublayers. Physiological implications of the results are discussed. Remarks are also made concerning the potential of the piriform cortex as a model cortical system.     

Distribution and ultrastructure of neurons in opossum piriform cortex displaying immunoreactivity to GABA and GAD and high-affinity tritiated GABA uptake

GABAergic neurons have been identified in the piriform cortex of the opossum at light and electron microscopic levels by immunocytochemical localization of GABA and the GABA-synthesizing enzyme glutamic acid decarboxylase and by autoradiographic visualization of high-affinity 3H-GABA uptake. Four major neuron populations have been distinguished on the basis of soma size, shape, and segregation at specific depths and locations: large horizontal cells in layer Ia of the anterior piriform cortex, small globular cells with thin dendrites concentrated in layers Ib and II of the posterior piriform cortex, and multipolar and fusiform cells concentrated in the deep part of layer III in anterior and posterior parts of the piriform cortex and the subjacent endopiriform nucleus. All four populations were well visualized with both antisera, but the large layer Ia horizontal cells displayed only very light 3H-GABA uptake, thus suggesting a lack of local axon collaterals or lack of high-affinity GABA uptake sites. The large, ultrastructurally distinctive somata of layer Ia horizontal cells receive a very small number of symmetrical synapses; the thin, axonlike dendrites of small globular cells are exclusively postsynaptic and receive large numbers of both symmetrical and asymmetrical synapses, in contrast to somata which receive a small number of both types; and the deep multipolar and fusiform cells receive a highly variable number of symmetrical and asymmetrical synapses on somata and proximal dendrites. Labeled puncta of axon terminal dimensions were found in large numbers in the neuropil surrounding pyramidal cell somata in layer II and in the endopiriform nucleus. Moderately large numbers of labeled puncta were found in layer I at the depth of pyramidal cell apical dendrites with greater numbers in layer Ia at the depth of distal apical segments than in layer Ib. High-affinity GABA uptake was demonstrated in the termination zone of the projection from the anterior olfactory nucleus to the anterior piriform cortex. Cell bodies of origin of this projection displayed heavy retrograde labeling with 3H-GABA. Matching neuropil and cellular labeling was demonstrated with the GABA-BSA antiserum but not with the GAD antiserum, thus suggesting that GABA is normally present in these cells but is taken up from the neuropil rather than synthesized. No comparable high-affinity GABA uptake was demonstrated in the association fiber systems that originate in the piriform cortex.(ABSTRACT TRUNCATED AT 400 WORDS)     

The Convergence of Axon Terminals from the Mediodorsal Thalamic Nucleus and Ventral Tegmental Area on Pyramidal Cells in Layer V of the Rat Prelimbic Cortex

We investigated the ultrastructural basis of the synaptic convergence of afferent fibres from the mediodorsal thalamic nucleus (MD) and the ventral tegmental area (VTA) on the prefrontal cortical neurons of the rat by examining the synaptic relationships between thalamocortical or tegmentocortical terminals labelled with anterograde markers [lesion-induced degeneration or transport of wheat germ agglutinin conjugated to horseradish peroxidase (WGA—HRP)] and randomly selected unlabelled apical dendrites of layer V pyramidal cells in the prelimbic cortex. WGA—HRP-labelled terminals from the VTA ranged in diameter from 0.7 to 2.8 μm and established synaptic contacts with large dendritic profiles, i.e. proximal segments of apical dendritic shafts and spines from layer V pyramidal cells. Symmetrical synapses, i.e. inhibitory synapses, were more often seen than asymmetrical ones. Degenerating terminals from the MD formed asymmetrical synapses on dendritic spines or occasionally on small dendritic shafts of apical dendrites from layer V pyramidal cells, which received tegmentocortical synapses, mostly within layer III. Thalamocortical synapses were more distally distributed over common apical dendrites than tegmentocortical synapses, although some of them overlapped. The numerical density of direct synaptic inputs from the MD and VTA was low. These results suggest that fibres from the VTA exert their inhibitory effects directly on pyramidal cells in layer V via synaptic junctions with apical dendrites of these pyramidal cells, and that the tegmentocortical fibres are in an ideal anatomical position to modulate the reverberatory circuits between the MD and the prelimbic cortex.     

Ultrastructural analysis of synaptic relationships of intracellularly stained pyramidal cell axons in piriform cortex

Axons of pyramidal cells in piriform cortex stained by intracellular injection of horseradish peroxidase (HRP) have been analyzed by light and electron microscopy. Myelinated primary axons give rise to extensive, very fine caliber (0.2 micron) unmyelinated collaterals with stereotyped radiating branching patterns. Serial section electron microscopic analysis of the stained portions of the collateral systems (initial 1-2 mm) revealed that they give rise to synaptic contacts on dendritic spines and shafts. These synapses typically contain compact clusters of large, predominantly spherical synaptic vesicles subjacent to asymmetrical contacts with heavy postsynaptic densities. On the basis of comparisons with Golgi material and intracellularly stained dendrites, it was concluded that dendritic spines receiving synapses from the proximal portions of pyramidal cell axon collaterals originate primarily from pyramidal cell basal dendrites. Postsynaptic dendritic shafts contacted closely resemble dendrites of probable GABAergic neurons identified in antibody and [3H]-GABA uptake studies. Electron microscopic examination of pyramidal cell axon initial segments revealed a high density of symmetrical synaptic contacts on their surfaces. Synaptic vesicles in the presynaptic boutons were small and flattened. It is concluded that pyramidal cells synaptically interact over short distances with other pyramidal cells via basal dendrites and with deep nonpyramidal cells that probably include GABAergic cells mediating a feedback inhibition. This contrasts with long associational projections of pyramidal cells that terminate predominantly on apical dendrites of other pyramidal cells.     

The synaptology of parvalbumin-immunoreactive neurons in the primate prefrontal cortex.

Electron microscopy and immunocytochemistry with a monoclonal antibody against parvalbumin (PV) were combined to analyze the distribution and morphology of PV-immunoreactive (PV-IR) neurons and the synaptology of PV-IR processes in the principal sulcus of the macaque prefrontal cortex. Parvalbumin-IR neurons are present in layers II-VI of the macaque principal sulcus (Walker's area 46) and are concentrated in a band centered around layer IV. PV-IR cells are exclusively non-pyramidal in shape and are morphologically heterogeneous with soma sizes ranging from less than 10 microns to greater than 20 microns. Well-labeled neurons that could be classified on the basis of soma size and dendritic configuration resembled large basket and chandelier cells. A novel finding is that supragranular PV-IR neurons exhibit dendritic patterns with predominantly vertical orientations, whereas infragranular cells exhibit mostly horizontal or oblique dendritic orientations. PV-IR cells within layer IV exhibit a mixture of dendritic arrangements. Vertical rows of PV-IR puncta, 15-30 microns in length, resembling the "cartridges" of chandelier cell axons were most dense in layers II, superficial III, and the granular layer IV but were not observed in the infragranular layers. Cartridges were often present beneath unlabeled, presumed pyramidal cells. PV-IR puncta also formed pericellular nests around pyramidal cell somata and proximal dendrites, suggestive of basket cell innervation. PV-IR axons were occasionally observed in the white matter underlying the principal sulcus. Electron microscopic analysis revealed that PV-IR somata and dendrites are densely innervated by nonimmunoreactive terminals forming asymmetric (Gray type I) synapses as well as by fewer terminals forming symmetric (Gray type II) synapses. The majority of terminals forming symmetric synapses with PV-IR post-synaptic structures were not immunolabeled; however, some of these boutons did contain PV-immunoreactivity. PV-IR boutons exclusively form symmetric synapses and heavily innervate layer II/III pyramidal cells. PV-IR axon cartridges formed numerous axo-axonic synapses with the axon initial segments of pyramidal cells 15-20 microns beneath the axon hillock and also terminated on large axonal spines of the initial segment. Furthermore, we failed to observe a mixture of PV-immunoreactive and non-immunoreactive boutons composing a single axon cartridge. Pyramidal cell somata and proximal dendrites were also heavily innervated by PV-IR boutons forming symmetric synapses, again, consistent with basket cell innervation. In addition, PV-IR axon terminals frequently formed symmetric synapses with dendritic shafts and spines of unidentified neurons.(ABSTRACT TRUNCATED AT 400 WORDS)     

Pyramidal cells of the rat basolateral amygdala: synaptology and innervation by parvalbumin-immunoreactive interneurons

The generation of emotional responses by the basolateral amygdala is determined largely by the balance of excitatory and inhibitory inputs to its principal neurons, the pyramidal cells. The activity of these neurons is tightly controlled by gamma-aminobutyric acid (GABA)-ergic interneurons, especially a parvalbumin-positive (PV(+)) subpopulation that constitutes almost half of all interneurons in the basolateral amygdala. In the present semiquantitative investigation, we studied the incidence of synaptic inputs of PV(+) axon terminals onto pyramidal neurons in the rat basolateral nucleus (BLa). Pyramidal cells were identified by using calcium/calmodulin-dependent protein kinase II (CaMK) immunoreactivity as a marker. To appreciate the relative abundance of PV(+) inputs compared with excitatory inputs and other non-PV(+) inhibitory inputs, we also analyzed the proportions of asymmetrical (presumed excitatory) synapses and symmetrical (presumed inhibitory) synapses formed by unlabeled axon terminals targeting pyramidal neurons. The results indicate that the perisomatic region of pyramidal cells is innervated almost entirely by symmetrical synapses, whereas the density of asymmetrical synapses increases as one proceeds from thicker proximal dendritic shafts to thinner distal dendritic shafts. The great majority of synapses with dendritic spines are asymmetrical. PV(+) axon terminals form mainly symmetrical synapses. These PV(+) synapses constitute slightly more than half of the symmetrical synapses formed with each postsynaptic compartment of BLa pyramidal cells. These data indicate that the synaptology of basolateral amygdalar pyramidal cells is remarkably similar to that of cortical pyramidal cells and that PV(+) interneurons provide a robust inhibition of both the perisomatic and the distal dendritic domains of these principal neurons.     

GABAergic synaptic boutons in the granule cell layer of rat dentate gyrus

GABAergic synapses in the granule cell layer of the rat dentate gyrus were examined light and electron microscopically with glutamate decarboxylase (GAD) immunocytochemistry. GAD-immunoreactive synaptic boutons formed synapses with axon initial segments and somatic spines as well as somata and dendritic shafts of the granule cell. Most of these synapses were symmetrical, while a few were asymmetrical.     

Quantitative morphological analysis of subicular terminals in the rat entorhinal cortex

In the present report, we describe a morphological and quantitative analysis of subicular synapses in layer V of the lateral entorhinal cortex (LEA) of the rat. Projections from the dorsal subiculum were labeled anterogradely, and areas in LEA showing high terminal density were randomly selected for ultrathin sectioning. More than 400 terminals in LEA were photographed in the electron microscope, and synapse types and postsynaptic targets were identified and, subsequently, quantified with the unbiased disector method. Most subicular terminals appeared to form asymmetrical synapses. A majority of asymmetrical synapses terminated on spines (67.5%), whereas a smaller fraction of asymmetrical synapses (23.5%) terminated on dendritic shafts. A small fraction of the terminals (7%) had symmetrical features. These symmetrical synapses had an almost equal percentage of spines and dendritic shafts as postsynaptic elements. Labeled synapses on somata or axons were never observed. The findings of this study in conjunction with relevant electrophysiological observations (Jones [1987] Neurosci Lett 81:209–214) leads to the conclusion that the subiculo-entorhinal pathway comprises a large excitatory and a smaller inhibitory projection, both making synaptic contacts with presumed principal neurons and interneurons in the entorhinal cortex. © 1995 Wiley-Liss, Inc.     

Substance P-containing pyramidal neurons in the cat somatic sensory cortex.

Light and electron microscopic immunocytochemical methods were used to verify the possibility that neocortical pyramidal neurons in the first somatic sensory cortex of cats contain substance P. At the light microscopic level, substance P-positive neurons accounted for about 3% of all cortical neurons, and the vast majority were nonpyramidal cells. However, 10% of substance P-positive neurons had a large conical cell body, a prominent apical dendrite directed toward the pia, and basal dendrites, thus suggesting they are pyramidal neurons. These neurons were in layers III and V. At the electron microscopic level, the majority of immunoreactive axon terminals formed symmetric synapses, but some substance P-positive axon terminals made asymmetric synapses. Labelled dendritic spines were also present. Combined retrograde transport-immunocytochemical experiments were also carried out to study whether substance P-positive neurons are projection neurons. Colloidal gold-labelled wheat germ agglutinin conjugated to enzymatically inactive horseradish peroxidase was injected either in the first somatic sensory cortex or in the dorsal column nuclei. In the somatic sensory cortex contralateral to the injection sites, a few substance P-positive neurons in layers III and V also contained black granules, indicative of retrograde transport. This indicates that some substance P-positive neurons project to cortical and subcortical targets. We have therefore identified a subpopulation of substance P-positive neurons that have most of the features of pyramidal neurons, are the probable source of immunoreactive axon terminals forming asymmetric synapses on dendritic spines, and project to the contralateral somatic sensory cortex and dorsal column nuclei. These characteristics fulfill the criteria required for classifying a cortical neuron as pyramidal.     

Cholinergic synaptic circuitry in the macaque prefrontal cortex

Surprisingly little is known about the synaptic architecture of the cholinergic innervation in the primate cerebral cortex in spite of its acknowledged relevance to cognitive processing and Alzheimer's disease. To address this knowledge gap, we examined serially sectioned cholinergic axons in supra- and infragranular layers of the macaque prefrontal cortex by using an antibody against the acetylcholine synthesizing enzyme, choline acetyltransferase (ChAT). The tissue bound antibody was visualized with both immunoperoxidase and silver-enhanced diaminobenzidine sulfide (SEDS) techniques. Both methods revealed that cholinergic axons make synapses in all cortical layers and that these synapses are exclusively symmetric. Cholinergic axons formed synapses primarily on dendritic shafts (70.5%), dendritic spines (25%), and, to a lesser extent, cell bodies (4.5%). Both pyramidal neurons and cells exhibiting the morphological features of GABAergic cells were targets of the cholinergic innervation. Some spiny dendritic shafts received multiple, closely spaced synapses, suggesting that a subset of pyramidal neurons may be subject to a particularly strong cholinergic influence. Analysis of synaptic incidence of cholinergic profiles in the supragranular layers of the prefrontal cortex by the SEDS technique revealed that definitive synaptic junctions were formed by 44% of the cholinergic boutons. An unexpected finding was that chohnergic boutons were frequently apposed to spines and small dendrites without making any visible synaptic specializations. These same spines and dendrites often received asymmetric synapses, presumably of thalamocortical or corticocortical origin. Present ultrastructural findings suggest that acetylcholine may have a dual modulatory effect in the neocortex: one through classical synaptic junctions on dendritic shafts and spines, and the other through nonsynaptic appositions in close vicinity to asymmetric synapses. Further physiological studies are necessary to test the hypothesis of the nonsynaptic release of acetylcholine in the Cortex. © 1995 Wiley-Liss, Inc.     

Structure of the mitral cell in the olfactory bulb of the goldfish (Carassius auratus)

The mitral cell in the olfactory bulb of the goldfish was examined by means of light microscopy, high-voltage electron microscopy, and conventional electron microscopy. Mitral cells are located rather diffusely throughout the glomerular and plexiform layers. They do not make their own discrete layer. The cell bodies are rounded or triangular, and are about 10–25 μm in diameter. In Golgi-impregnated material, thick cylindrical dendrites can be seen arising from the cell bodies and branching in the glomerular layer. Dendritic branches of some cells make two or more rather compact tufts, while the dendrites of other cells intermingle loosely with one another. In semithin and thin sections, darkly stained nodules appear to be scattered diffusely in the glomerular layer without clustering into discrete spheres, which are characteristic of the mammalian glomerulus. Hence, instead of the glomerulus, the “glomerular area” is defined as an area consisting of darkly stained nodules with rather pale granular regions surrounding them. Branches of mitral cell dendrites in the glomerular area consist of cylindrical shafts and irregular appendages arising from them. The shafts appear in the pale granular region and the appendages are found in the darkly stained nodules. Synapses can be found on all parts of the mitral cell: the soma, axon hillock, axon initial segment, thick dendritic stems, and dendritic branches. The abundance of synapses seems to vary considerably from part to part, and is highest on the dendritic branches in the glomerular area. The mitral cell is postsynaptic to olfactory nerve terminals and granule cell dendrites, and presynaptic to granule cell dendrites and some processes of unknown origin. Olfactory nerve terminals make asymmetrical synapses specifically on the appendages of the dendritic branches. Of the synapses on the shafts of the mitral cell dendritic branches in the glomerular area, 90% are with granule cell dendrites. Of the synapses between two different kinds of processes 30% are mitral-to-granule asymmetrical synapses, 20% are granule-to-mitral symmetrical synapses, and 50% are reciprocal pairs. Gap junctions and mixed synapses are also seen on branches of mitral cell dendrites. Features of the goldfish mitral cell are compared with those of the mammal. The differences in neuronal organization between the olfactory bulbs of teleosts and mammals are discussed.     

Distribution of synapses on fast and slow pyramidal tract neurons in the cat. An electron microscopic study

Distributions of synapses on various portions of fast and slow pyramidal tract neurons (PTNs) in cat motor cortex were studied with electron microscopy. PTNs were identified by their antidromic invasion following stimulation of the medullary pyramid and were classified into fast and slow PTNs according to conduction velocities of their axons. Two fast and two slow PTNs were intracellularly labeled and, by systematic sampling, electron micrographs from various portions of these neurons were examined to compare the distributions of different types of synapses. It was found that most synapses formed on apical and basal dendrites of fast PTNs were with the dendritic shafts. In slow PTNs, while synapses on apical dendrites were mostly axospinous, about 70% of the sampled synapses on basal dendrites of slow PTNs were established with the dendritic shafts. Virtually all synapses on apical dendrites of slow PTNs belonged to asymmetrical type and most of the synapses sampled from basal dendrites of fast PTNs were also asymmetrical. On the other hand, about 29% of the synapses found on apical dendrites of fast PTNs were symmetrical and a trend was observed for this type of synapses to increase their number with increasing proximity to the cell body. Over 28% of the synapses on basal dendrites of slow PTNs were also symmetrical and seemed to be mainly distributed in layer VI. All synapses formed on the soma were symmetrical both for the fast and slow PTNs.     

The laminar distribution and ultrastructure of fibers projecting from three thalamic nuclei to the somatic sensory-motor cortex of the opossum

The projections of the ventrobasal complex (VB), the ventrolateral complex (VL), and the central intralaminar nucleus (CIN) to the somatic sensory-motor (SSM) cortex of the Virginia opossum were studied with light and electron microscopic autoradiographic methods. VB, VL, and CIN have overlapping projections to SSM cortex and each one also projects to an additional cortical area. Unit responses to somatic sensory stimulation and the areal and laminar distribution of axons in cortex is different for VB, VL, and CIN, but the axons from each form similar round asymmetrical synapses, predominantly with dendritic spines. As in other mammals, VB units in the opossum have discrete, contralateral cutaneous receptive fields. VB projects somatotopically to SSM cortex and also projects to the second somatic sensory representation. Within the cortex, VB axons terminate densely in layer IV and the adjacent part of layer III. A few axons also terminate in the outermost part of layer I and the upper part of layer VI. Most VB axon terminate upon dendritic spines (86.6%), but they also contact dendritic shafts (10%) and neuronal cell bodies (3%). Neurons in VL have no reliable response to somatic stimulation under our recording conditions. VL projects to the SSM cortex and to the posterior parietal area. Throughout this entire projection field VL fibers terminate in layers I, III, and IV most densely, and sparsely in the other cortical layers. The density of termination in the mid-cortical laminae is quite sparse compared to VB, but the projection to layer I is considerably greater. Nearly all (93%) of VL axons contact dendritic spines, the remainder (7%) end dendritic shafts. CIN is a thalamic target of ascending medial lemniscal, cerebellar, spinal, and reticular formation axons. Neurons in CIN respond to stimulation restricted to a particular body part, but typically responses may be evoked from larger areas and at longer latencies than neurons in VB that are related to the same body part. CIN neurons require a firm tap or electrical stimulation within their receptive field to elicit a response in the anesthetized preparation. CIN axons terminate throughout the entire parietal cortex, but unlike VB and VL, CIN fibers end almost exclusively in the outer part of layer I. Approximately 21% of CIN fibers contact dendritic shafts in layer I, which is twice the percentage of shafts contacted by VL or VB axons. All of the other CIN synapses are formed with dendritic spines. These experiments demonstrate three different pathways to SSM cortex. The results suggest that each projection has a unique role in controlling the patterns of activity of neurons within the SSM cortex.     

Distribution of corticocortical and thalamocortical synapses on identified motor cortical neurons in the cat: Golgi, electron microscopic and degeneration study

Details of the terminal connection of corticocortical and thalamocortical fibers on pyramidal and stellate neurons in the cat motor cortex were studied using the electron microscope in combination with the Golgi and axonal degeneration techniques. Corticocortical terminals were examined in 23 identified neurons of which 11 were pyramidal and 12 were stellate. Stellate neurons located in layer III received many degenerating terminals (average 8.4 +/- 2.2 per unit length of dendrite (ULD)) and the majority of these (95%) were found on the proximal dendrites or on the cell bodies. The pyramidal neurons received fewer degenerating terminals (average 2.1 +/- 0.27/ULD) and these were located on more distal dendritic shafts or on dendritic spines. The majority of these synapses were of the asymmetric type. Thalamocortical terminals were examined in 9 pyramidal and 9 stellate neurons. Pyramidal neurons received many terminals (average 6.0 +/- 1.23/ULD) and these were found on the basal as well as the apical dendrites and on dendrite spines. Stellate neurons received fewer terminals (average 4.2 +/- 0.64/ULD) and were located primarily on proximal dendritic shafts. The majority of these synapses were of the asymmetric type. The functional role of these synapses is discussed in relation to the physiological results reported in the preceding paper.     

Morphological and numerical analysis of synaptic interactions between neurons in deep and superficial layers of the entorhinal cortex of the rat

Neurons providing connections between the deep and superficial layers of the entorhinal cortex (EC) constitute a pivotal link in the network underlying reverberation and gating of neuronal activity in the entorhinal-hippocampal system. To learn more of these deep-to-superficial neurons and their targets, we applied the tracer Neurobiotin pericellularly in layer V of the medial EC of 12 rats. Labeled axons in the superficial layers were studied with light and electron microscopy, and their synaptic organization recorded. Neurobiotin-labeled layer V neurons displayed "Golgi-like" staining. Two major cell types were distinguished among these neurons: (1) pyramidal neurons with apical spiny dendrites traversing all layers and ramifying in layer I, and (2) horizontal neurons with dendrites confined to the deep layers. Labeled axons ramified profusely in layer III, superficially in layer II and deep in layer I. Analysis of labeled axon terminals in layers I-II and III showed that most synapses (95%) were asymmetrical. Of these synapses, 56% occurred with spines (presumably belonging to principal neurons) and 44% with dendritic shafts (presumably interneurons). A small fraction of the synapses (5%) was of the symmetrical type. Such synapses were mainly seen on dendritic shafts. We found in two sections a symmetrical synapse on a spine. These findings suggest that the deep to superficial projection is mainly excitatory in nature, and that these fibers subserve both excitation and feed-forward inhibition. There is an additional, much weaker, inhibitory component in this projection, which may have a disinhibitory effect on the entorhinal network in the superficial layers.     

Synaptic relationships between axon terminals from the mediodorsal thalamic nucleus and layer III pyramidal cells in the prelimbic cortex of the rat

A combined study of anterograde axonal degeneration and Golgi electron microscopic technique was designed to examine the distribution and density of axon terminals from the mediodorsal thalamic nucleus (MD) over layer III pyramidal cells in the prelimbic cortex of the rat. The reconstructive analysis of serial ultrathin sections of gold-toned apical and basal dendrites of layer III pyramidal cells showed that degenerating thalamocortical axon terminals from MD formed asymmetrical synaptic contacts predominantly with dendritic spines of the identified basal dendrites as well as apical dendrites. There was little difference in the numerical density of thalamocortical synapses from MD per unit length of both apical and basal dendrites.