Axonal endings terminating on dendrites of identified large trigeminospinal projection neurons in rat trigeminal nucleus oralis

The retrograde horseradish peroxidase technique was used to: (1) identify and assess the overall morphology of large neurons in the ventrolateral portion (VL) of rat trigeminal nucleus oralis projecting to cervical, thoracic and lumbosacral levels of the spinal cord; and (2) characterize the synaptic endings terminating on their dendrites. The morphology of large VL neurons projecting to all spinal levels is similar. They have 25–50 μm pyramidal-shaped somata which emit 3–6 primary dendrites. These primary dendrites give rise to spherical to elliptical-shaped dendritic arbors measuring up to 700 μm in diameter. Labeled axons enter either a deep axon bundle or the medial portion of the spinal V tract. Dendrites of labeled neurons are contacted by axonal endings of 3 types. The most numerous endings are filled with clear, spherical synaptic vesicles and usually form a single asymmetrical contacts along the entire length of dendritic shafts. Synapsing less frequently on dendritic shafts are endings containing pleomorphic synaptic vesicles and forming single symmetrical synaptic contacts. The least frequently encountered synaptic terminal contains flattened synaptic vesicles and makes a single symmetrical synaptic contact with a dendritic shaft.     

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 shaft. The type 2 dendrite receives 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 dendrodendritic synapses from type 2 dendrites. The types 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→2→1) and indirectly by increasing transmitter release at the axodendritic synapses of the C axonal endings through their dendroaxonic synapses (2→C→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 action potentials because of the reciprocal pairing of dendroaxonic and axodendritic synapses (C?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→2→1).     

Phenylethanolamine N-methyltransferase-containing terminals synapse directly on sympathetic preganglionic neurons in the rat

The ultrastructural morphology as well as neuronal and glial associations of phenylethanolamine N-methyltransferase (PNMT)-containing terminals in the intermediolateral cell column (IML) of the thoracic spinal cord were examined in the rat utilizing the peroxidase-antiperoxidase (PAP) method. The PNMT-immunoreactive terminals were 0.5–1.4 μm in diameter and contained a few mitochondria, a large population of small clear vesicles and from 1 to 6 large dense-core vesicles. The terminals formed synapses primarily with dendrites. The type of axodendritic association (i.e. symmetric or asymmetric) varied with the size of the dendrite, such that the majority of synapses on large dendrites were symmetric and those on smaller dendrites and dendritic spines were asymmetric. Moreover, most of the synaptic associations of PNMT-containing terminals were with the smaller dendritic processes. Many of the PNMT-labeled terminals, as well as their postsynaptic targets, were closely invested with, or apposed to fibrous astrocytic processes. In a subsequent set of experiments, we combined immunoautoradiographic labeling for PNMT with horseradish peroxidase (HRP) retrograde identification of sympathetic preganglionic neurons (SPNs) in the IML to determine whether or not SPNs receive direct synaptic input from the adrenergic terminals. In these sections, PNMT-containing terminals directly synapsed on the HRP-containing (i.e. retrogradely labeled SPNs) perikarya and dendrites. The axosomatic synapses observed between PNMT-labeled terminals and SPN perikarya were exclusively symmetric: whereas the type of axodendritic association varied depending upon the size of the dendrite such that the majority were asymmetric. The findings provide ultrastructurral evidence that in the rat IML, adrenergic (i.e. PNMT-containing) terminals (1) may be either excitatory (asymmetric) or inhibitory (symmetric) depending on their site of termination and (2) can influence sympathetic nerve discharge through a direct effect on the SPN cell membrane.     

The postnatal development of the substantia nigra: A light and electron microscopy study

The early postnatal development of neurons, dendrites, and synaptic connectivity in kitten substantia nigra (SN) was studied by light and electron microscopy. The compact and reticular divisions of the SN are present at birth but boundaries are indistinct. Most nigral neurons stain deeply in routine histological sections and their diameters increase slightly with age. Ultrastructurally, cell bodies are characterized by eccentrically located and often invaginated nuclei surrounded by cytoplasm rich in well-formed or-ganelles. Axosomatic synapses are infrequent and cell surfaces are enveloped by glial processes. Immature dendritic features, including growth cones and filiform processes, are commonly observed during the first 10 days. Gradually the dendritic profiles elongate and thicken and contours become smoother, retaining only scattered spinelike appendages. Clear examples of the three synaptic types described in cat are found in newborn kittens, but immature terminals contain fewer synaptic vesicles and mitochondria. Approximately 90% of synapses present at birth in both nigra subdivisions are Type I, which contain large pleomorphic vesicles and contact dendrites symmetrically. Asymmetrical contacts characterize most of the remaining definable synapses. The postnatal increase in synaptic connectivity, which was estimated from random photographs of pars reticulata neuropil, is twofold during the first 50 days of life. Initially young dendrites are enveloped by glia and then gradually become ensheathed by axon terminals. Synaptogenesis in pars reticulata reflects the postnatal increase of neostriatal inputs to this subdivision and can be correlated with functional changes in strionigral connectivity.     

Morphology and synaptic connections of myelinated primary axons in the ventrolateral region of rat trigeminal nucleus oralis

Neurons in the ventrolateral (VL) subdivision of rat trigeminal nucleus oralis (Vo) have most of their dendritic arbors confined within this region. This study examines the morphology and synaptic connections of a population of myelinated primary trigeminal axons that arborize within VL and are in a position to provide input directly to VL neurons. Primary axons were visualized for light and electron microscopic analysis by injecting 30% horseradish peroxidase (HRP) in 2% dimethylsulfoxide (DMSO) into the sensory root of the trigeminal nerve and allowing 24-36 hours for the anterograde transport of HRP into the terminal axonal arbors. This population is characterized by its cone-shaped terminal arbors, which generate many axonal endings (2-8 micron in diameter) along unmyelinated terminal strands. These arbors arise from collaterals emanating from thinly myelinated (2-5 micron in diameter) parent branches descending in the spinal V tract, which, on the basis of their size, are considered to be small myelinated (A sigma) primary trigeminal axons. HRP-labeled P endings belonging to this population of primary axons are scalloped, filled with spherical to ovoid (40-70 nm in diameter) synaptic vesicles, and lie centrally in glomeruli where they make asymmetrical axodendritic synapses on dendritic shafts and spine heads. It is at these synapses that this population of primary trigeminal axons is probably transferring its input directly to the dendritic arbors of VL neurons. The dendritic shafts and spine heads also receive symmetrical to intermediate axodendritic synapses from endings containing flattened (70 X 29 nm) synaptic vesicles. These terminals also establish axo-axonic synapses on the P ending. Other synaptic components found less often in the glomeruli include small terminals containing oval (14-23 nm) synaptic vesicles that establish symmetrical to intermediate synapses on the P ending, boutons containing pleomorphic (35-80 nm) synaptic vesicles that form symmetrical to intermediate synapses on the P ending as well as on dendritic shafts, and small peripheral endings containing round (20-40 nm) synaptic vesicles that establish asymmetrical synapses on dendritic shafts.     

Differentiation of spinous synapses in the mouse organ of corti

The inner hair cells, the primary auditory receptors, are perceived only as a means for transfer of sound signals via the auditory nerve to the central nervous system. During initial synaptogenesis, they receive relatively few and mainly somatic synapses. However, around the onset of hearing (10-14 postnatal days in the mouse), a complex network of local spinous synapses differentiates, involving inner hair cells, their afferent dendrites, and lateral olivocochlear terminals. Inner hair cell spines participate in triadic synapses between olivocochlear terminals and afferent dendrites. Triadic synapses have not yet been confirmed in the adult. Synaptic spines of afferent dendrites form axodendritic synapses with olivocochlear terminals and somatodendritic synapses with inner hair cells. The latter are of two types: ribbon-dendritic spines and stout dendritic spines surrounded only by a crown of synaptic vesicles. Formation of spinous afferent synapses results from sprouting of dendritic filopodia that intussuscept inner hair cell cytoplasm. This process continues in the adult, indicating ongoing synaptogenesis. Spinous processes of olivocochlear synaptic terminals contact adjacent afferent dendrites, thus integrating their connectivity. They develop about 14 postnatal days, but their presence in the adult has yet to be confirmed. Differentiation of spinous synapses in the organ of Corti results in a total increase of synaptic contacts and in a complexity of synaptic arrangements and connectivity. We propose that spinous synapses provide the morphological substrate for local processing of initial auditory signals within the cochlea.     

Fornix afferents to the anteroventral thalamic nucleus: An EM study in the rat

LENN, N. J. Fornix afferents to the anteroventral thalamic nucleus: An EM study in the rat. BRAIN RES. BULL. 3(6) 589–593, 1978.—Three types of synapses occur in the anteroventral thalamic nucleus (AVN). Type 1 consists of small (0.5–0.8 μm) axonal endings densely packed with spherical synaptic vesicles. They form markedly asymmetrical synaptic contacts with distal portions of dendrites. Degenerative changes in these axons following destruction of the fornix identify them as the endings of the subicular projection to AVN. Type 2 synapses consist of large (1.0–1.5 μm) axonal processes containing spherical vesicles which form asymmetrical synapses on more proximal dendrites. Type 3 endings consist of large unidentified processes containing spherical, and occasionally flattened, synaptic vesicles forming symmetrical contacts with the largest stem dendrites. Neither of these synaptic types were modified by fornix lesions. The synaptic arrangements within AVN are simpler than other thalamic nuclei in that serial synapses and synaptic glomeruli are not present.     

An electron microscopic analysis of the trans-synaptic effects of peripheral nerve injury subsequent to tooth pulp extirpations on neurons in laminae I and II of the medullary dorsal horn

To examine the effects of peripheral nerve injury on second-order neurons in laminae I and II of the medullary dorsal horn, tooth pulps of all mandibular teeth in adult cats on one side were extirpated. This procedure severed and removed the receptors and terminal branches of the primary trigeminal neurons which innervate the tooth pulps of these teeth. The empty pulp chambers were then filled with dental cement to prevent regeneration. At 30 and 60 days postoperatively, membrane-lined cavities had formed inside many of the small-caliber dendrites of second-order neurons in laminae I and II. Cavity formation occurred mainly in dendritic shafts less than 2 micron in diameter and involved dendrites with synaptic vesicles as well as those without synaptic vesicles. The cavities extensively hollowed out these dendrites, often occupying more than half the cross-sectional diameter of the shafts and extending for appreciable distances in the long axis of the shaft. The process of cavitation ultimately resulted in the destruction of the affected dendrites. Many cavities became patent to the intercellular space with the cavity membrane establishing continuity with the dendritic membrane. Many cavities often formed in a single dendrite, and such severely cavitated dendrites became reduced to a trabeculated shell which ultimately fragmented into several small pieces. The presence of synaptic connections from a number of different kinds of axonal endings, including scalloped and dome-shaped endings, was not sufficient to prevent cavitation. The actual severing of synaptic connections on the cavitated dendrite appeared to be a relatively late event in the process since small pieces of dendritic debris could still be found clinging to their axodendritic synapses. Evidence that dendrites were being lost from the neuropil was most readily apparent in many of the disrupted glomeruli in lamina II in which many of the scalloped depressions in the central axonal endings that normally contained small dendrites were empty. Many central axonal endings remained in synaptic contact with only a single dendrite which often showed signs of cavitation. Such central endings showed only subtle remaining traces of their normal scalloped contours. This study demonstrates that injury to the distal branches of primary trigeminal neurons which innervate tooth pulps resulted in trans-synaptic degenerative changes in the dendritic arbors of second-order neurons which destroyed fine-caliber higher order dendrites.     

An electron microscopic study of synaptic organization in the medial superior olive of normal and experimental chinchillas

The medial superior olive (MSO) was studied in normal animals to determine the types of synaptic endings and their distribution over the surface of MSO neurons. Unilateral lesions were made in the anteroventral cochlear nucleus (AVCN) of experimental animals to determine the source of at least one synaptic type in the MSO. The surfaces of MSO neurons in normal animals were studded with three distinct types of synaptic endings distinguished mainly by the size of their synaptic vesicles. There were endings with large vesicles, 510 Å in mean diameter; endings with small vesicles, 380 Å; and endings with vesicles intermediate in size. 435 Å. The large vesicle ending typically was greater than 2 μm in maximum diameter. It appeared as the termination of a myelinated axon or as a swollen portion of a node and made multiple asymmetrical synapses. Large vesicle endings occurred exclusively on dendrites where they formed 85% of the synaptic endings. Small vesicle endings typically were less than 2 μm in diameter. They appeared as the termination of a fine unmyelinated axon and made only one symmetrical synapse. Small vesicle boutons occurred infrequently over the entire neuronal surface. Intermediate vesicle synaptic endings were similar to large vesicle endings except that they were present only on the cell body, axon hillock, and proximal portions of the dendrites where they formed most of the synapses. In AVCN lesioned animals degenerating myelinated axons and large vesicle synaptic endings were distributed to the lateral dendrites of the ipsilateral MSO and medial dendrites of the contralateral one. In addition, a few degenerating axons and large vesicle endings were found among the ipsilateral medial dendrites. The changes in the degenerating endings were characterized by an early proliferation of neurofilaments and swelling of the endings followed by collapse of the endings and increase in electron density, disappearance of filaments and synaptic vesicles, and phagocytosis of the degenerated endings by reactive glial cells. No degenerative changes were observed in the small and intermediate vesicle endings. The results of this study indicate that the more numerous large vesicle endings presynaptic to the MSO dendrites are the axon terminals of neurons in the AVCN. The persistence after lesions of the small and intermediate vesicle endings suggests that they arise from as yet unidentified sources.     

Spatial relationships between the terminations of somatic sensory motor pathways in the rostral brainstem of cats and monkeys. II. Cerebellar projections compared with those of the ascending somatic sensory pathways in lateral diencephalon

In order to classify the presynaptic elements contacting the principle class of globus pallidus neurons, electron microscopic examination of serial sections made from a medially located large globus pallidus neuron, labeled with intracellular horseradish peroxidase, was undertaken. In addition, the use of labeled and light microscopically reconstructed material allowed us to quantitatively determine the distribution of each bouton type along the soma and dendrites. Six types of presynaptic terminals contacting the labeled cell have been recognized. Type 1 endings, the most numerous (84%), make symmetrical contacts on all portions of the cell, except spines, contain large pleomorphic, and a few large dense-core vesicles. Type 2 endings are filled with small spherical-to-ellipsoidal synaptic vesicles. They make asymmetrical contacts only with higher-order dendrites and account for 12% of synaptic contacts onto the labeled neuron. Type 3 endings are large, contain sparsely distributed large pleomorphic vesicles, and make two symmetrical synapses per bouton, one onto a spine head and the other onto the underlying dendritic shaft. They are infrequent (0.2%), being found only in association with dendritic spines. Type 4 endings contain large pleomorphic synaptic vesicles and no dense-core vesicles. They make symmetrical contacts with the short primary dendrites. Type 5 endings contain a mixture of small clear pleomorphic vesicles and numerous large dense-core vesicles. They contact only the cell body and the short primary dendrites, making up 20% of somatic synaptic contacts but less than 1% of contacts onto dendrites. Type 6 boutons contain oval and flattened synaptic vesicles and establish symmetrical contacts with higher-order dendritic branches and the cell body.     

Projections from auditory cortex to the cochlear nucleus in rats: Synapses on granule cell dendrites

Previous work has demonstrated that layer V pyramidal cells of primary auditory cortex project directly to the cochlear nucleus. The postsynaptic targets of these centrifugal projections, however, are not known. For the present study, biotinylated dextran amine, an anterograde tracer, was injected into the auditory cortex of rats, and labeled terminals were examined with light and electron microscopy. Labeled corticobulbar axons and terminals in the cochlear nucleus are found almost exclusively in the granule cell domain, and the terminals appear as boutons (1–2 μm in diameter) or as small mossy fiber endings (2–5 μm in diameter). These cortical endings contain round synaptic vesicles and form asymmetric synapses on hairy dendritic profiles, from which thin (0.1 μm in diameter), nonsynaptic “hairs” protrude deep into the labeled endings. These postsynaptic dendrites, which are typical of granule cells, surround and receive synapses from large, unlabeled mossy fiber endings containing round synaptic vesicles and are also postsynaptic to unlabeled axon terminals containing pleomorphic synaptic vesicles. No labeled fibers were observed synapsing on profiles that did not fit the characteristics of granule cell dendrites. We describe a circuit in the auditory system by which ascending information in the cochlear nucleus can be modified directly by descending cortical influences. © 1996 Wiley-Liss, Inc.     

A quantitative study of synaptic reorganization in red nucleus neurons after lesion of the nucleus interpositus of the cat: an electron microscopic study involving intracellular injection of horseradish peroxidase

A quantitative electron microscopic analysis of the corticorubral projection was performed in the red nucleus (RN) of adult cats to determine morphological correlates of synaptic reorganization that occur following a lesion of the interpositus nucleus (IP).Corticorubral synaptic endings were identified by lesioning the sensorimotor cortex 2–6 days before electrophysiological experiments. Horseradish peroxidase (HRP) was injected into electrophysiologically identified RN neurons. Sagittal sections 100 μm thick were cut and reacted by diaminobenzidine. Sections containing HRP-positive neurons were selected and embedded in Epon.In normal cats, degenerating corticorubral terminals in the RN region frequently made contact with dendritic profiles, having small cross-sections, while a few made contact with somatic profiles. Similar results were obtained when degenerating terminals making contact with HRP-filled dendrites were analyzed.In the experimental animals, the cortical lesion was performed more than 8 weeks after lesion of the IP. In these animals, degenerating corticorubral terminals were frequently found on proximal dendrites and somata in RN region and HRP-positive neurons in contrast to the findings in normal cats.The results indicate that new corticorubral synapses were formed on proximal dendrites and somata of RN neurons as a consequence of IP lesions.     

Fine structure and synaptic connections of the common spiny neuron of the rat neostriatum: A study employing intracellular injection of horseradish peroxidase

Medium-sized spiny neurons of the rat neostriatum, identified by intracellular injection of horseradish peroxidase, were examined at both light and electron microscopic levels. These neurons were characterized by their heavy investment of dendritic spines, beginning about 20 μm from the soma and continuing to the tips of the dendrites. Their axons arose from the soma or from a large dendritic trunk very near the soma, and tapered rapidly to form a main axonal branch from which arose several smaller initial collaterals. These arborized extensively throughout an area of about the same size as, and highly overlapping with, the dendritic field of the cell, while the main axon could be followed for distances of up to 1 mm in the direction of the globus pallidus. Three major synaptic types were seen in contact with spiny neurons. Boutons containing small round synaptic vesicles formed synapses exclusively with spiny regions of the dendrites, and most of these were axo-spinous. Small, very pleomorphic synaptic vesicles characterized a second bouton type of unknown origin, which made contacts with somata, initial segments, and dendrites, but not dendritic spines. Boutons containing large pleomorphic synaptic vesicles had the most widespread distribution, contacting all regions including dendritic spines. Spines receiving these contacts also were postsynaptic to boutons containing small round vesicles. Axon collaterals of spiny cells formed synapses with large pleomorphic vesicles and made synapses with somata, initial segments of axons, dendrites, and dendritic spines of striatal neurons, including other spiny cells.     

Morphology and synaptic connections of ultrafine primary axons in lamina I of the spinal dorsal horn: candidates for the terminal axonal arbors of primary neurons with unmyelinated (C) axons

Neurons in Rexed's lamina I have the bulk of their dendritic arbors confined within this lamina. This study examines the morphology and synaptic connections of primary axons which generate axonal endings in lamina I of the spinal dorsal horn and are in position to deliver their inputs directly to lamina I neurons. Primary axons were made visible for light and electron microscopical study by applying horseradish peroxidase (HRP) to the severed central stumps of cervical and lumbar dorsal roots and allowing sufficient time for the orthograde movement of the HRP into the terminal axonal arbors. Golgi preparations provided supplementary light microscopical views of these axons. Lamina I receives the terminal arborization of two very different kinds of primary axons. One of these generates many ultrafine endings along unbranched, long rostrocaudally oriented, strand-like collaterals which arise from thin parent branches in Lissauer's tract. In view of these thin parent branches, most ultrafine primary axons are considered to be unmyelinated (C) primary axons. The second kind of primary axon generates large caliber endings on branched collaterals. These arise from relatively thick parent branches in Lissauer's tract which, on the basis of their size, are considered to be myelinated (A delta) primary axons. The scalloped endings of both primary axons lie in the interior of glomeruli where they form axodendritic synapses on small dendritic shafts and spines. It is at these synapses that these two kinds of primary axons are thought to transfer nociceptive and thermal inputs directly to the dendritic arbors of lamina I neurons. Transmitter release at these axodendritic synapses in response to primary inputs can be modified, probably diminished or inhibited, by synaptic events within the glomeruli from at least three sources. Synaptic vesicle-containing dendrites form dendroaxonic synapses on primary endings and two kinds of axons form axoaxonic synapses either on primary endings or on the intervaricose segments of the primary axons.     

Cellular substrates for interactions between dynorphin terminals and dopamine dendrites in rat ventral tegmental area and substantia nigra

Dynorphin and other kappa opioid agonists are thought to elicit aversive actions and changes in motor activity through direct or indirect modulation of dopamine neurons in ventral tegmental area (VTA) and substantia nigra (SN), respectively. We comparatively examined the immunoperoxidase localization of anti-dynorphin A antiserum in sections through the VTA and SN of adult rat brain to assess whether there were common or differential distributions of this opioid peptide relative to the dopamine neurons. We also more directly examined the relationship between dynorphin terminals and dopamine neurons in VTA and SN by combining immunoperoxidase labeling of rabbit dynorphin antiserum and immunogold-silver detection of mouse antibodies against tyrosine hydroxylase (TH) in single sections through the VTA and SN. Light microscopy showed dynorphin-like immunoreactivity (DY-LI) in varicose processes. These were relatively sparse in VTA and were unevenly distributed in the SN, with little labeling in the pars compacta (pcSN) and the highest density of DY-LI in the medial and lateral pars reticulata (prSN). Electron microscopy established that the regional differences were attributed to differences in density (number/unit area) of immunoreactive profiles. The profiles containing DY-LI were designated as axon terminals based on having diameters greater than 0.1 μm, few microtubules and many synaptic vesicles. In both the VTA and SN, the dynorphin-labeled terminals contained primarily small (35–40 nm) clear vesicles. These vesicles were rimmed with peroxidase immunoreactivity and were often seen clustered above axodendritic synapses. These synaptic specializations were usually symmetric; however a few asymmetric densities also were formed by immunoreactive terminals in both VTA and SN. Additionally, most of the dynorphin-labeled terminals contained 1–2, but occasionally 7 or more intensely peroxidase positive dense core vesicles (DCVs). Approximately 60% of the DCVs were located near axolemmal surfaces. The axolemmal surfaces contacted by immunoreactive DCVs were more often apposed to dendrites in the VTA; while in the SN other axon terminals were the most commonly apposed neuronal profiles. In both regions, a substantial proportion of the plasmalemmal surface in contact with the labeled DCVs was apposed to astrocytic processes. In dually labeled sections through the VTA, 22% (n = 138) of the terminals containing DY-LI formed synapseson or were apposed to TH-labeled dendrites, while 16% were in contact with unlabeled dendrites. The remainder were apposed to other dynorphin labeled and unlabeled terminals and/or astrocytes. In dually labeled sections through the prSN, 37% (n = 216) of the terminals containing DY-LI formed synapses or were apposed to TH-labeled dendrites, while 28% contacted unlabeled dendrites. The remainder were in contact with axon terminals or astrocytes. These findings demonstrate the morphologically heterogeneous terminals containing DY-LI in rat VTA and SN provide a substantial monosynaptic input to dopamine and non-dopamine targets. The finding of symmetric and asymmetric synapses, mixed vesicle populations, and associations with dendrites, terminals, and astrocytes suggests multiple sites for dynorphin actions in both VTA and SN.     

Quantitative ultrastructural changes in rat cortical synapses during early-, mid- and late-adulthood

Quantitative ultrastructural analysis of rat parietal cortex was undertaken to determine the nature of the synaptic changes occurring in the molecular layer over a series of ages in early- (3 months), mid- (6 and 10 months) and late- (17 months) adulthood.The total number of synapses remained constant until 10 months of age, but decreased significantly by 17 months. Asymmetrical synapses on dendritic shafts were lost earlier (by 6 months) than asymmetrical synapses on dendritic spines (by 17 months). Symmetrical axodendritic synapses remained constant throughout adulthood.Analysis of synaptic terminal parameters revealed the following. Both individual and total presynaptic terminal areas decreased over the age range studied. Individual and total postsynaptic terminal areas, however, remained constant over the 3–17-month period. Positive correlations were obtained for the relationships between presynaptic terminal area and both age and synaptic vesicle number. The presynaptic terminal area was largest and contained the greatest number of vesicles at 3 months of age. This age was, in addition, characterized by the least numbers of mitochondria in the presynaptic terminal and spine apparatus in the postsynaptic terminal. The vacuolar and tubular cisternae of the presynaptic terminal were considerably reduced at 17 months.These data suggest that in the molecular layer of the cerebral cortex the period of adulthood is characterized by a diversity of synaptic changes. The 3-months age may reflect the end of the developmental phase and may be marked by changes in synaptic functional activity. The asymmetrical axodendritic synapses may constitute an intermediate form of synapse, capable of being transformed into axospinous synapses as dendritic spines continue to be formed in the adult.     

EM autoradiographic study of the projections from the dorsal nucleus of the lateral lemniscus: a possible source of inhibitory inputs to the inferior colliculus

The fine structure of the projection from the dorsal nucleus of the lateral lemniscus (DNLL) to the inferior colliculus is examined in the cat. Anterograde axonal transport of 3H-leucine and EM autoradiographic techniques are used to label axonal endings from DNLL. The primary finding is that axonal endings from DNLL contain pleomorphic synaptic vesicles and make symmetrical synaptic contacts. This morphology is associated with inhibitory synapses. The projection from DNLL is the source of approximately one-third of the axonal endings with pleomorphic vesicles in the central nucleus of the inferior colliculus. In the contralateral central nucleus, only labeled endings with pleomorphic vesicles are found. By comparison, on the ipsilateral side, both endings with pleomorphic vesicles and, to a lesser degree, endings with round vesicles are labeled. Endings from DNLL are more numerous per unit area on the contralateral side. About half of the labeled axonal endings from DNLL terminate upon small dendrites, and another third terminate upon more proximal dendrites and several types of cell bodies. Many axonal endings form multiple synaptic contacts, sometimes on more than one postsynaptic structure. Sites of termination for axonal endings include dendritic spines and branch points of dendrites. These data support the hypothesis that the DNLL pathway to the inferior colliculus may have an inhibitory function. Previous studies show that DNLL neurons exhibit immunoreactivity to GAD and GABA antibodies. The crossed projection of DNLL to the inferior colliculus forms tonotopically organized bands that terminate as endings with pleomorphic vesicles. These endings may supply GABAergic inputs to the inferior colliculus. Thus, bands from DNLL could provide inhibitory inputs and overlap with bands from other sources that provide excitatory inputs. Overlapping bands may form unique synaptic domains in the inferior colliculus. The uncrossed projections from DNLL may provide the inferior colliculus with a more diffusely organized projection that could include excitatory and inhibitory inputs. Since the DNLL on one side may inhibit the opposite DNLL and the inferior colliculus, the DNLL pathway may regulate ascending inhibition to the midbrain. Presumed inhibitory inputs from DNLL to the inferior colliculus could be involved in binaural information processing and contralateral dominance.     

A qualitative electron microscopic study of the corticopontine projections after neonatal cerebellar hemispherectomy

The present study shows that 3–5 days following leions of the dentate and interposed nuclei in normal adult rats degenerating axons and axon terminals can be detected in the contralateral pontine gray. The degenerating axon terminals form Gray's type I axo-dendritic contacts with fine intermediate dendrites measuring between 0.8–2.4 μm. The present study also investigates, by electron microscopy, the synaptic rearrangement of the sensorimotor corticopontine projections following neonatal left cerebellar hemispherectomy¹⁹. Following neonatal left cerebellar hemispherectomy, the right sensorimotor and adjacent cortex (SMC) presents a very dense ipsilateral and a modest amount of contralateral corticopontine projections in contrast with a predominantly ipsilateral corticopontine projection seen in the normal adult rat. As with the ipsilateral corticopontine projection seen in the normal adult animal, the bilateral corticopontine projections seen in the experimental animals form contacts with dendrites suggestive of Gray's type I synapses. While the corticopontine projections in normal control animals form synapses with fine dendrites measuring 0.2–1.2 μm the corticopontine projections in the experimental animals form synaptic relations with fine dendrites and with intermediate dendrites measuring 0.2–2.4 μm. As the normal cerebellopontine fibers from the dentate and interposed nuclei also form axo-dendritic synapses on fine and intermediate dendrites and the contacts formed are also of Gray's type I synapses, it is possible that some of the newly formed corticopontine fibers in the experimental animals might have replaced the cerebellopontine fibers synapsing on intermediate dendrites. Synaptic rearrangement appears to take place as suggested by the presence of synaptic complexes in which one axon terminal contacts two of more dendrites or two or more axon terminals contact one dendrite. Such complexes are frequently seen to undergo degeneration following the right SMC lesion in the experimental animals. Other complex synaptic structures are also present in both the right and left pontine gray in the experimental animals. They are not seen to undergo degeneration following the right SMC lesions. Occasional features of neuronal reaction could still be seen both sides of the pontine gray for as long as 3–6 months after the neonatal cerebellar lesions.     

The synaptic organization of the motor nucleus of the trigeminal nerve in the opossum

The motor nucleus of the opossum trigeminal nerve consists of a main body and a small dorsomedial cell cluster. The cell bodies form a unimodal population with areas that range from 150–2700 μm². Golgi impregnations reveal that each neuron has three to six primary dendrites which radiate in all planes from the cell body. Within 300 μm from the soma, the primary dendrites divide into secondary branches and these, in turn, bifurcate into thinner distal dendrites. The overall diameter of the dendritic tree often extends as much as 1 mm, with a rare branch leaving the confines of the nucleus to enter the neighboring reticular formation. Somatic and dendritic spines are often present and are either sessile or complex appendage forms. The perikarya and initial dendritic trunks of trigeminal neurons are contacted by four types of presynaptic terminals which cover more than 40% of the membrane. Most endings are 1–3 μm long and contain either spherical (S) or pleomorphic (P) synaptic vesicles. Another, less common, type of bouton is marked by large dense-core (DC) vesicles. Approximately 8% of the terminals on trigeminal cell bodies are large (2–5 μm) with spherical synaptic vesicles and are always associated with a subsynaptic cistern (C-boutons). These terminals very often interdigitate with adjacent synaptic endings. S-, P-, and C-boutons synapse on the dendritic tree of trigeminal neurons in the following characteristic pattern: proximal dendrites (greater than 5 μm in diameter) are contacted by all three types of terminals; intermediate-sized dendrites (between 2.5 and 5.0 μm in diameter) are most often contacted by S-boutons although P-boutons are also present; and small, distal dendrites (less than 2.5 μm in diameter) are almost always contacted by S- boutons. Both S- and P-boutons contact spines. In order to determine the ultrastructural identity of some of the major afferent systems to the trigeminal motor nucleus, adult opossums were subjected to two different types of lesions. Three and 5 days subsequent to lesions which destroyed most of the trigeminal mesencephalic nucleus, degenerating terminals containing spherical vesicles were found. These endings were S-boutons on more distal parts of the dendritic tree while on the cell body and proximal dendrites they were C-boutons. Seven days after a mesencephalic lesion, expanded glial processes approximated the trigeminal cell membrane. Two days subsequent to lesions which transected commissural fibers from the contralateral trigeminal complex, degenerating S- and P-boutons were found in contact with intermediate and distal parts of the trigeminal dendritic tree.     

Ultrastructure and synaptology of the nucleus ambiguus in the rat: The compact formation

The fine structure of the esophagomotor compact formation of the nucleus ambiguus was studied. Esophageal motoneurons are atypical in that they have extensive direct somato somatic and somato-dendritic appositions without intervening glial processes. A unique feature is the presence of finger- and leaf-like somatic protrusions which partially wrap longitudinally oriented dendrites and occasionally, small groups of dendrites and axons. The neuropil contains many longitudinally oriented, small-diameter dendrites of relatively uniform size (1.1 ± 0.4 S. D. μm in diameter). Motoneuronal somatic profiles have 0–5 synapses per profile which represents a synaptic density of 10.6 synapses per soma. Axodendritic synapses measure 0.5 × 0.7 μm in the transverse plane and are up to 3.0 μm long in the sagittal plane. Many axon terminals contact both a soma and dendrite in close apposition. Most axon terminals (>90%) contain round vesicles and form asymmetric junctions with somata and dendrites. Axon terminal degeneration after electrolytic lesions and labelling after injections of wheat germ agglutinin-horseradish peroxidase in the nucleus of the tractus solitarius show that afferent connections to the compact formation form axodendritic synapses. The ultrastructure and synaptology of esophageal motoneurons is characterized by the close apposition of somata and dendrites (somatic-dendritic bundling), and the longitudinal orientation of dendrites (dendritic bundling), axons and axon terminals in the neuropil. These features may be important morphological substrates for synchronization and coordination of esophageal motoneuronal activity and esophageal peristalsis. © 1995 Wiley-Liss, Inc.