A Survey of the Cytology and Synaptic Organization of the Insular Trigeminal—Cuneatus Lateralis Nucleus in the Rat,Including an Identification of Spinal Afferent Inputs

The cytology and synaptic organization of the insular trigeminal—cuneatus lateralis (iV-Cul) nucleus was examined in the rat. In addition, the ultrastructural morphology and synaptic connectivity of anterogradely labeled spinal afferent axons terminating in iV-Cul were examined following injection of horseradish peroxidase (HRP) into the cervical spinal cord. The uniformity of the ultrastructural features of iV-Cul neurons supports the presence of a homogeneous neuronal population. The most prominent feature of the iV-Cul neuropil is the presence of numerous interdigitating astrocytic processes, which extensively isolate neuronal somata and processes. iV-Cul contains a heterogeneous population of axonal endings that can be separated into three categories, depending upon whether they contain predominantly spherical-shaped agranular synaptic vesicles (R endings), predominantly pleomorphic-shaped agranular synaptic vesicles (P endings), or a heterogeneous population of dense-core vesicles (DC endings). The R endings represent the majority of axonal endings in iV-Cul and establish asymmetrical axodendritic and axospinous synaptic contacts, primarily along the distal portions of the dendritic tree. P endings establish symmetrical axosomatic, axodendritic, and axospinous synaptic contacts and exhibit a more generalized distribution along the somadendritic tree. DC terminals establish asymmetrical axodendritic synaptic contacts with distal dendritic processes and are the least frequently observed endings in the iV-Cul neuropil. Numerous synaptic glomeruli, exhibiting a single large central R bouton that establishes multiple axodendritic or axospinous synapses, characterize the iV-Cul neuropil. Axoaxonic synapses are conspicuously absent from the iV-Cul neuropil and glomeruli. The anterograde HRP labeling of spinal afferent axons that terminate in iV-Cul indicates that the terminals along these fibers are of the R type and that they are engaged predominantly in synaptic glomeruli. The results of this study indicate that the synaptic organization of iV-Cul is distinctly different from that of neighboring somatosensory nuclei, and supports the recent suggestion that this nucleus should be considered a separate precerebellar spinal relay nucleus in the lateral medulla.     

Fine structural characteristics and synaptic connections of trigeminocerebellar projection neurons in rat trigeminal nucleus oralis

In order to classify the presynaptic terminals contacting trigeminocerebellar projection neurons (TCPNs) in rat trigeminal nucleus oralis (Vo), electron-microscopic examination of sequential thin sections made from TCPNs located in the border zone (BZ) of Vo, labeled by the retrograde transport of horseradish peroxidase, was undertaken. The use of BZ TCPNs, labeled in Golgi-like fashion so that many of their dendrites and axons were visible, allowed for the determination of the distribution of each bouton type along the soma and dendrites, as well as for the characterization of the morphology and synaptic relations of the labeled axon and its terminals. Three types of axon terminals contacting labeled BZ TCPNs have been recognized, depending upon whether they contain primarily spherical-shaped, agranular synaptic vesicles (S endings); predominantly flattened, agranular synaptic vesicles (F endings); or a population of pleomorphic-shaped, agranular synaptic vesicles (P endings). The S endings represent the majority of axon terminals contacting labeled BZ TCPNs and establish asymmetrical axosomatic and axodendritic synaptic contacts. Many S endings are situated in one of two types of synaptic glomeruli. One type of glomerulus has a large S ending at its core, whereas the other contains a small S ending. Large-S-ending glomeruli include only labeled distal dendrites of BZ TCPNs; small-S-ending glomeruli contain either a labeled soma, proximal dendrite, or distal dendritic shaft. The remaining S endings are extraglomerular, synapsing on distal dendrites. P endings are less frequently encountered and establish intermediate axosomatic and axodendritic synapses. These endings exhibit a generalized distribution along the entire somatodendritic tree. F endings make symmetrical axodendritic synapses with distal dendrites, are only found in glomeruli containing small S endings, and are the least frequently observed ending contacting labeled BZ TCPNs. The majority of axonal endings synapsing on labeled BZ TCPNs are located along distal dendrites, with only a relatively few synapsing terminals situated on proximal dendrites and somata. The axons of labeled BZ TCPNs arise from the cell body and generally give rise to a single short collateral near their points of origin. This collateral remains unbranched and generates several boutons within BZ, while the parent axon acquires a myelin sheath and, without branching further, travels dorsolaterally toward the inferior cerebellar peduncle. The collateral boutons resemble extraglomerular S endings. They contain agranular, spherical-shaped synaptic vesicles and make asymmetrical axodendritic synapses with small-diameter unlabeled dendritic shafts in the BZ neuropil.     

Distribution of synaptic boutons in the mesencephalic trigeminal nucleus of the rat--a quantitative electron-microscopical study.

The distribution of synapses and synaptic bouton types in the mesencephalic trigeminal (Me5) nucleus was examined in a quantitative electron-microscopical study. Of 588 terminal boutons that were counted in the compact caudal part of the Me5 nucleus, less than 8% formed synapses on the somata of the predominantly unipolar Me5 neurons. About 79% formed synapses on fibres located between the Me5 somata, while about 13% of the vesicle-containing terminals had no clear synaptic specialization. All of these non-synaptic terminals were G type boutons, with pleomorphic and large characteristic dense-core vesicles. Approximately 60% of the axosomatic synapses were of the S type, containing spherical vesicles and an asymmetrical or symmetrical synaptic specialization. About 20, respectively 15% of the axosomatic synapses, were of the F, respectively P type; both are symmetrical synapse types containing either a majority of flat or pleomorphic vesicles. Less than 10% of the axosomatic synapses were of the G type. Although some proportional differences were noted, an almost similar bouton type distribution pattern was found for the axodendritic synapses suggesting that the axosomatic and axodendritic synapses in the Me5 nucleus are part of the same afferent fibre plexus covering the Me5 nucleus.     

Ultrastructural organization of the synapses in ganglia of the hen intestinal nerve under various conditions of its activity

The interneuronal connections in ganglia of the caudal part of the hen intestinal nerve of Remak are presented as axodendritic and axosomatic synapses and symmetric axo-axonal, dendro-dendritic and axodendritic contacts, often forming complicated complexes. Under conditions of preliminary decentralization or under certain disturbances of nervous connections with the intestine, a part of synapses remains, and a part of them degenerates, this demonstrates participation of peripheral afferent neurons in formation of the synaptic apparatus of the ganglia mentioned. The axonal terminals differentiate by composition of the synaptic vesicles: some contain mainly light agranular vesicles, others--a large amount of granular ones. The characteristic peculiarities of the hen intestinal nerve ganglia, in contrast to analogous mammalian ganglia, are abundant axosomatic synapses in some neurons, and presynaptic terminals, containing a large number of granular vesicles.     

Age-related changes in the synapses of the rat's neostriatum

By means of transmission electron microscopy, the age-related changes in axospinous (ASS) and axodendritic (ADS) synapses in the dorsal part of the rostral neostriatum in two groups of Wistar rats: young (3-month-old), and senescent (25-month-old) were examined. The changes in different parameters, characterizing the ASS and ADS: synaptic density (SD), number of synaptic vesicles (SV), number of synaptic contact zone (SCZ), and number of dendritic spines, bearing synapses (DS) were investigated morphometrically. The SD of the ASS decreased significantly during aging, but the SD of the ADS did not changed significantly. The mean area of the synaptic boutons increased significantly during aging in two types of synapses. The mean number of vesicles per synaptic bouton increased, but the number of vesicles per microm2 of synaptic bouton, and per microm3 of the neuropil decreased. The mean SCZ length increased in both types of synapses. The total SCZ length per 1000 microm2 of the neuropil, and the total area of the SCZ per 1000 microm3 of the neuropil decreased in ASS, but the same parameters of the ADS did not changed significantly. The mean number of synaptic DS per 1000 microm2 of the neropil decreased during aging, but the mean area of the synaptic DS increased. The present results support the hypothesis that the synaptic contacts change significantly during aging, and the ASS are more vulnerable during aging than the ADS.     

Morphofunctional types of synapses in the neurosecretory cells of the carp preoptic nucleus]

The ultrastructure of synaptic endings of the neurosecretory cells of the nucleus preopticus was examined in adult Cyprinus carpio L. Two of synpatic endings occur: type I--small agranular vesicles and large granular vesicles, type II--only agranular vesicles. The functioning of the nucleus preopticus neurosecretory cells in Cyprinus carpio L is presumably controlled by the synpatic endings of the adrenergic (synaptic endings of type I) as well as of the cholinergic (synaptic endings of type II) origin. By visual and morphometric methods different kinds of synpatic endings are distinguished among both the types of synapses according to their particular functional states. A quantitative analysis of the correlation of these kinds of synpatic endings allows a suggestion in respect to the state of the synaptic apparatus on the perikaria of neurosecretory cells.     

The fine structure of the dorsal column nucleus and the nucleus of bischoff of the python (Python reticulatus)

Three types of neuronal perikaryal profiles were identified in the dorsal column nucleus and the nucleus of Bischoff of the python (Python reticulatus). Type I neuronal profiles are large (diameters 12–20 μm) with a deeply indented uncleus. The cisterns of rough endoplasmic reticulum (rER) are mostly randomly dispersed. Axosomatic synapses are few. Type II neuronal profiles (9–11 μm) have a smooth, round, or slightly oval nucleus. Several small stacks of rER are present. Type III neuronal profiles (8–10 μm) have little cytoplasm. The nuclear margin is irregular but not deeply infolded. The rER usually consists of a single long perinuclear ribosome-studded cistern. Two types of astrocytic profiles have been identified. Both types contain abundant filaments. Type I astrocytes are large cells, and the nucleus is very irregular in shape. Type II astrocytes are smaller and are found among the myelinated axons in the dorsal funiculus. Two classes of axon terminals have been identified. One class contains round synaptic vesicles (R profiles) and the other flattened vesicles (F profiles). Some R profiles are small (SR profiles), others are large (LR profiles). Some R profiles also contain a few large, dense-cored vesicles. The R and F profiles establish axodendritic and axoaxonal synapses, some of which are located in the synaptic glomeruli and others in the extraglomerular neuropil. In most of the axoaxonal synapses, the presynaptic element is an F profile and the post synaptic element an LR profile. Occasionally, LR profiles are presynaptic to F profiles. The findings in the python are compared with those of the dorsal column nuclei of the rat, cat, and monkey.     

Neurotensin immunoreactivity in the central nucleus of the rat amygdala: an ultrastructural approach

Neurotensin (NT) was demonstrated in the central nucleus of the rat amygdala (CNA) using a modification of the avidin-biotin complex immunohistochemical technique. Electron-dense reaction product (particles were 15-25 nm in diameter) was localized in perikarya, dendrites, axons, and axon terminals. It was found also associated with profiles of rough endoplasmic reticulum, mitochondria, microtubules, and small agranular as well as large granular vesicles. In distal dendrites, the reaction product was associated with microtubules, vesicles, and postsynaptic densities. Axon terminals of three types formed synaptic contracts with NT-immunoreactive neurons in the CNA: one was characterized by numerous round or oval agranular vesicles, the second by numerous pleomorphic vesicles, and the third by agranular vesicles that were loosely distributed and pleomorphic. All three types formed symmetric axosomatic and asymmetric axodendritic contacts. NT-immunoreactive axon terminals containing small round agranular vesicles stood out clearly from the intermingling profiles of immunonegative structures. We found numerous glomeruli, each consisting of a central NT-immunoreactive dendrite surrounded by all three types of axon terminals. We observed that some NT-immunoreactive terminals formed symmetric axoaxonal contacts with each other, providing evidence for the presence of local NT-to-NT circuits, whereas many others synapsed with axon terminals devoid of NT immunoreactivity.     

Synaptology of three peptidergic neuron types in the central nucleus of the rat amygdala

The synaptology of neurotensin (NT)-, somatostatin (SS)- and vasoactive intestinal polypeptide (VIP)-immunoreactive neurons was studied in the central nucleus of the rat amygdala (CNA). Three types of axon terminals formed synaptic contacts with peptide-immunoreactive neurons in the CNA: Type A terminals containing many round or oval vesicles; Type B terminals containing many pleomorphic vesicles; and Type C terminals containing fewer, pleomorphic vesicles. Peptide-immunoreactive terminals were type A. All three types of terminals formed symmetrical axosomatic and asymmetrical axodendritic contacts. However, type B and peptide-immunoreactive terminals frequently formed symmetrical axodendritic synaptic contacts. VIP-immunoreactive terminals also formed asymmetrical axodendritic contacts. SS- and NT-immunoreactive terminals commonly formed symmetrical contacts on SS- and NT-immunoreactive cell bodies, respectively. VIP-immunoreactive axon terminals were postsynaptic to nonreactive terminals. Type B terminals appeared more frequently on VIP neurons than on NT or SS neurons.     

Long-term effects of alloxan-induced diabetes on the nucleus ventralis posterolateralis in the thalamus of the rat.

The present paper describes the long-term ultrastructural changes in the nucleus ventralis posterolateralis of the thalamus of male Wistar rats after alloxan-induced diabetes. Degenerating dendrites were characterized by an electron-dense cytoplasm with scattered endoplasmic reticulum and ribosomes. Degenerating axon terminals were characterized by an electron-dense cytoplasm and clustering of small spherical agranular vesicles. Degenerating axon terminals formed axosomatic synapses with seemingly normal cell bodies and axodendritic synapses with normal as well as degenerating dendrites. Degenerating axons (both myelinated and unmyelinated) were readily encountered in the neuropil. Activated microglial and astrocytic cells in the neuropil were in the process of phagocytosis or had residua in their cytoplasm.     

Demonstration and localization of synapsin I in vestibular receptors in the cat: immunocytochemical study

The presence and localization of synapsin I, a neuron-specific phosphoprotein, was investigated in the cat vestibular epithelium, using a rabbit antisynapsin I anti-serum. The staining was performed by immunofluorescence or by a peroxidase-antiperoxidase (PAP) technique. A strong immunoreactivity was observed with both methods. This immunoreactivity appeared as spherical patches distributed in the lower part of the epithelium. This distribution pattern is very similar to that of the efferent synaptic endings which form axodendritic synapses with the afferent nerve chalice of type I hair cells, or axosomatic synapses with type II hair cells. Some of the nerve chalices were also labelled; in this case, the immunoreactivity was more evident with PAP staining. These results thus suggest the presence of large amounts of synapsin I in the vestibular efferent nerve endings. These endings are known to be filled with numerous synaptic vesicles. This localization of synapsin I is well correlated with previous work that report a close association between synapsin I and small synaptic vesicles. The presence of synapsin I in sensory endings such as the afferent nerve chalices was unexpected and is under investigation.     

Formation of new synaptic contacts by Purkinje axon collaterals in the granular layer of deafferented cerebellar cortex of adult rat

In addition to (i) mossy terminals, (ii) Golgi axons, (iii) granule cell dendrites and (iv), occasionally, Golgi cell dendrites, a third axonal profile identified by morphological criteria as the collateral of Purkinje axons, has been found in 2% of all cerebellar glomeruli. These infrequent components of a few glomeruli, however, were never seen in normal cerebellar cortex to establish specialized synaptic contact with glomerular dendrites. Two to four weeks after surgical isolation of the cerebellar cortex, i.e. following the destruction of both efferent and afferent fibres, the number of glomeruli containing (hypertrophic) axonal branches of Purkinje cells has increased to 13% of all surveyed glomeruli. In addition, the Purkinje axon terminals in the mossy fibre-deprived glomeruli were observed to establish numerous Gray II-type synaptic contacts with surrounding granule cell dendrites. It is suggested that the development of heterologous synapses between hypertrophic, or even intact, Purkinje axon collaterals on the one hand and the mossy fibre-vacated granule cell dendrites on the other, is a compensatory, reactive process to the synaptic "desaturation" of granule neurons, which demonstrate a dormant potential of Purkinje cells to form new synaptic contacts in the adult cerebellum.     

Morphology of the cat auditory cortex

The ultrastructural features of the primary auditory cortex of the cats and the character of the endings of geniculo-cortical afferent fibers in the early stages of experimental degeneration evoked by destruction of the medial geniculate body were studied. In all layers of the cortex asymmetrical synapses with round synaptic vesicles on dendritic spines and on thin dendritic branches of pyramidal and nonpyramidal neurons are predominant. Symmetrical synapses with flattened or polymorphic vesicles are distributed chiefly on the bodies of the neurons and their large dendrites. Because there are few symmetrical synapses which could be regarded as inhibitory it is postulated that inhibitory influences may also be transmitted through asymmetrical synapses with round vesicles. Other types of contacts between the bodies of neurons, dendrites, and glial processes also were found in the auditory cortex. Degenerating terminals of geniculo-cortical fibers were shown to terminate chiefly in layer IV of the cortex on pyramidal and nonpyramidal neurons. Degeneration was of the dark type in asymmetrical synapses with round vesicles. The results are dicussed in connection with electrophysiological investigations of the auditory cortex.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 5, No. 5, pp. 519–524, September–October, 1973.     

Ultrastructure of the area postrema of the monkey, Macaca fascicularis

The area postrema of the monkey, Macaca fascicularis, were a pair of oval organs at the caudal end of the floor of fourth ventricle. Their ependymal lining was covered by well-developed microvilli with occasional overlying supraependymal cells. Two types of lining cells were present: pyramidad- and flattened cells. The pyramidal cell showed a long extending basal process resting on the underlying blood vessels. In transmission electron microscopy, the organ showed numerous fenestrated sinusoids characterized by a distinct perivascular space containing mast cells, macrophages and collagen fibrils. The parenchyma of the organ was composed of neurons and glial elements. Only one type of neuron ranging from 9.5 to 15 microns could be distinguished. The neurons contained an indented nucleus surrounded by organelle rich cytoplasm. The soma of the neuron was enclosed by glial element resembling astrocyte. The glial processes terminated on the blood vessel where they were "tunnelled" by a variable number of nerve fibres some of which gained a direct access to the external basal lamina of the perivascular space. Synapses in the neuropil predominantly of the axodendritic variety were observed. Axon terminals containing round agranular vesicles were seen to make synaptic contacts with the neuronal soma. No structural changes were observed in the area postrema following bilateral cervical vagotomy. However, degenerating axon terminals were observed in the subpostremal zone 7, 14 and 21 days after vagotomy suggesting a direct afferent projection into this region.     

Structure of synapes in the supraoesophageal ganglion of the water beetle (Dytiscus marginalis).

1. Light- and electron microscopic investigations prove that synapses, without any exception, are confined to the neuropil. 2. Under the light-microscope, synapses display the shape of terminal boutons at the ends of the nerve fibres; in some cases they appear as smaller or larger plates. Electron microscopic investigations suggest that also varicosities of nerve fibres can be regarded as synapses, though these might have possible arisen from axoplasmatic peristalsis. 3. Electron microscopically the overwhelming majority of the synapses are axodendritic contacts; axo-axonic contacts occur less often. 4. The generally accepted characteristics of synapses are defective. Membrane thickenings and intersynaptic spaces are missing. Accordingly, synapses in the supraoesophageal ganglion of the water beetle differ markedly from those described in Vertebrates. 5. Synaptic vesicles sometimes fill the axoplasm of the nerve fibre completely. In other cases, clusters of synaptic vesicles can be seen, on both sides of the contact. 6. Synaptic vesicles are mixed with neurosecretory granules. Synaptic vesicles may appear also in the dendrites.     

Somato-dendritic synapses in the nucleus reticularis thalami of the rat

In the reticular nucleus of the rat thalamus, about 30% of the synapses are brought about by the perikarya of parvalbumin-immunopositive neurons, which establish somato-dendritic synapses with large dendrites of nerve cells of specific thalamic nuclei. Although the parvalbumin-immunopositive presynaptic structures bear resemblance to goblet-like or calyciform axonal endings, electron microscopic immunocytochemistry and in situ hybridization revealed that these structures are parts of the perikaryal cytoplasm studded with synaptic vesicles. In about 15% of the somato-dendritic synapses, axons are seen to be in synaptic contact with the parvalbumin-immunoreactive perikaryon. Double immunohistochemical staining revealed that the parvalbumin immunoreactive presynaptic perikarya and dendrites contained GABA. It is assumed that the peculiar somato-dendritic synaptic complexes subserve the goal of filtration of impulses arriving at the reticular nucleus from various thalamic nuclei, thus processing them for further sampling.     

Ultrastructure of synapses in the nucleus of the trapezoid body of the bat]

The subsynaptic structure of the synapses in the medial nucleus of the trapezoid body was studied in the bat Myotis oxygnatus. The synaptic endings in the nucleus are represented by large-cup-shaped and small loop-shaped terminations. The cup-shaped terminations are formed of large branches originating from a thick myelinated fibre after loss of myelin from it. Each branch forms a series of contacts alternating with vast enlargements of extracellular space, on the body of the cell and its processes. Large branches are filled with synaptic vesicles, neurofilaments and neurotubules, mitochondria; all these components are distributed rather regularly along the branch diameter. In fine branches of the cup the synaptic vesicles are the main and often the only component. The pattern of the cup branch changes as the distance from the main fibre increases, namely the amount of neurofilaments and neurotubules diminishes up to their disappearance, while the amount and the density of synaptic vesicles increases. The small loop-shaped treminals are different from the cup-shaped ones by the composition of the synaptic vesicles and the structure of the contact zone. In addition to agranular vesicles there are also granular ones. Both types of terminations--cup-shaped and loop-shaped ones -- are found both on the bodies and dendrites. On distal portions of dendrites the terminations are disposed in nests.     

Synaptic apparatus of the feline primary auditory cortex (area Al)

Electron microscope research was conducted on the synaptic apparatus of the feline primary auditory cortex (Al). A total of 2096 profiles of axonal terminals (AT) were found over a total area of 8230 µm² of ultrathin slices at different layers of this cortical layer — an average of 255 profiles per 1000 µm² of the surface area on these slices. The AT profiles occupied about 8.9% of the surface of these cross-sections. It was found that 52% of the AT containing synaptic vesicles formed asymmetrical or symmetrical synaptic contacts (83.9% and 16.1% respectively) and that AT had no contacts which could be considered synaptic junctions on 48% of slices. It was also observed that 45.3% of the AT forming contacts synapsed on spines, 48.5% on dendrites, and 6.2% on neuronal somata. Finally, 95.4% and 4.6% of axo-spinal synapses contained rounded and flattened vesicles respectively; equivalent figures for axodendritic synapses were 79.4% and 20.6% respectively and 19.8 and 80.2% for axosomatic synapses. Calculations revealed an average of 322.8 × 10⁶ AT over 1 mm³ of cat auditory cortex. Organizational aspects of synaptic apparatus at different layers of area A1 were ascertained.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 22, No. 4, pp. 533–543, July–August, 1990.     

The ultrastructural characteristics of the motor neuron synaptic organization in the spinal cord of the frog Rana ridibunda

Electron microscopic studies on the spinal motor nuclei in amphibians indicate significant diversity in chemical synapses formed on motoneurones by axonal endings of supra- and intraspinal systems. High ultrastructural specialization was observed among axosomatic, axodendritic and axoaxonal synapses. Several types of axo-spine synapses and axodentritic synaptic complexes of the "glomerular" type were revealed. New data on ultrastructural peculiarities of chemical synapses presented in this paper, together with earlier detailed data on morphologically mixed and electrotonic synapses, increase our knowledge of evolutionary trends in synaptic organization of motoneurones in the spinal cord and suggest the existence of a complex mechanism of integration of synaptic influences in the spinal cord of lower vertebrates.