Electron microscopic features of physiologically characterized, HRP-labeled fusiform cells in the cat dorsal cochlear nucleus

We report on the anatomy and physiology of three fusiform cells in the dorsal cochlear nucleus (DCN) of the cat. The extra- and intracellular responses of these cells to pure tones showed features typical of the cell type. Peristimulus time histograms (PSTHs) were usually of the pauser or buildup configuration with chopping behavior noted in certain instances. Intracellular records during stimulus presentations revealed sustained depolarizations for the duration of the tone followed by a prolonged after-hyperpolarization (AHP). On rare occasions, a hyperpolarization corresponding to the pause region of the PSTH was noted. Occasionally, a stimulus-induced depolarization would be maintained after stimulus offset. Rebound excitation was also observed after the AHP. Morphologically, all three cells showed the standard fusiform cell features at the light microscopic level. The cell body gave rise to apical and basal dendritic trees. The apical tree branched frequently and displayed numerous spines distally. The basal tree had fewer branches and fewer, more irregular appendages. The axon originated from the cell body and gave rise to one or more collaterals before leaving the nucleus via the dorsal acoustic stria (DAS). At the electron microscopic (EM) level, the axon collaterals may terminate on a variety of cell types in the DCN, including fusiform cells. Their vesicles are round and the terminals closely resemble many unlabeled terminals seen on the cell body and apical and basal dendrites of our labeled fusiform cells. Terminals containing round vesicles, believed to be eighth nerve terminals, were found, with one exception, only on the basal dendrites. The spine-laden, distal apical dendrites received primarily terminals containing round vesicles, presumed to originate from the unmyelinated axons of granule cells. The cell body and unmyelinated initial segment received mostly terminals containing pleomorphic and flat vesicles, which also made up a large percentage of the dendritic input. Some relevant correlations, between the distribution of synaptic terminals and the observed physiology, may be possible.     

The fine structure of the perigeniculate nucleus in the cat

The fine structure of the cat's perigeniculate nucleus has been analyzed and compared to that of dorsal thalamic relay nuclei. Golgi preparations and electron micrographs of perigeniculate cells commonly show somatic spines. The most common presynaptic elements for these spines and for the adjacent perikaryal surfaces are relatively large axon terminals containing round synaptic vesicles and making multiple asymmetric contacts. These "RLD" terminals (so termed for their round vesicles, large average size of the terminals, and dark mitochondria) are also presynaptic to dendritic spines and shafts of proximal and secondary dendrites. Comparisons with adjacent parts of the dorsal lateral geniculate nucleus show that these RLD terminals are cytologically distinct from retinogeniculate terminals and that small numbers of RLD terminals also occur in the geniculate A laminae. Three other major classes of perigeniculate synaptic terminals, resemble major classes of terminals in the dorsal lateral geniculate nucleus. These include two types of terminal with flat or ovoid synaptic vesicles and dark mitochondria, "FD1" and "FD2" terminals, and a class of small terminal with densely clustered round vesicles and dark mitochondria, "RSD" terminals. RSD terminals, which resemble corticogeniculate axon terminals, represent the only class of perigeniculate terminal that does not contact perikarya. FD2 terminals resemble lateral geniculate presynaptic dendrites and participate in serial and triadic synaptic contacts, being both pre- and postsynaptic; however, in contrast to the arrangement characteristic of thalamic relay nuclei, these contacts do not occur within synaptic glomeruli. A fifth major class of perigeniculate presynaptic terminal has large flat or polymorphic synaptic vesicles and pale mitochondria. These "FP" terminals are seen infrequently in the lateral geniculate A laminae. Similarities between perigeniculate and lateral geniculate fine structure may relate in part to common sources of afferent input to the two nuclei.     

Fine structural survey of the rat's brainstem sensory trigeminal complex

The fine structural organization of the principal sensory trigeminal nucleus was compared with that of the spinal trigeminal nucleus (subnuclei oralis, interpolaris, and the deep layers of caudalis) in adult albino rats. Direct comparisons indicate similarities between all of the subdivisions of the brainstem trigeminal complex both in the major morphological classes of neurons present and in basic patterns of synaptic connections. Major differences between the several subdivisions occur in the relative numbers and distribution of the different cell types. The spinal trigeminal nucleus is distinguished by more numerous large (22-40 micron) polygonal neurons which give rise to long straight primary dendrites. Both the perikaryal surface and the thick primary dendrites of many of these cells are densely innervated by synaptic terminals. Especially large cells of this type are a prominent feature of subnucleus oralis. By contrast, the principal sensory nucleus is distinguished by its high density of small to medium-sized (8-20 micron) round or ovoid neurons. These smaller neurons tend to receive a sparse axosomatic innervation. In addition to these differences the spinal trigeminal neuropil is distinguished by the striking manner in which it is broken up by large rostrocaudally oriented bundles of myelinated axons. Proximal dendrites of polygonal and fusiform neurons often wrap around these large axon bundles. Morphologically heterogeneous populations of synaptic terminals with round vesicles (R terminals) and terminals with predominantly flattened vesicles (F terminals) occur in all of the subdivisions of the trigeminal complex. Both types of terminal make primarily axodendritic synapses, but both also make axosomatic synapses, and axospinous synapses with somatic as well as dendritic spines. In addition, axoaxonic synaptic contacts from F terminals onto large R terminals are seen in all subdivisions. Convincing examples of presynaptic dendrites were not observed in any of the brainstem subdivisions. Synaptic glomeruli, characteristic groupings of dendrites and synaptic terminals, are found throughout the brainstem trigeminal complex. The dendritic elements in these glomeruli tend to be small-diameter dendrites, spines, and large, spinelike appendages. Within the glomerulus these elements are postsynaptic to a single large R terminal and may also be postsynaptic to smaller F terminals. In addition, axoaxonic synaptic contacts from the F terminals onto the R terminal are a consistent feature of trigeminal synaptic glomeruli.(ABSTRACT TRUNCATED AT 400 WORDS)     

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.     

Neuronal and synaptic composition of the mediodorsal thalamic nucleus in the rat: a light and electron microscopic Golgi study.

The distribution and dendritic domain of neurons in each segment of the mediodorsal thalamic nucleus (MD) have been studied in the rat with the Golgi technique. In addition, a combined Golgi method-electron microscopic (Golgi-EM) study was undertaken to determine the distribution of morphologically distinct synapse types along the dendrites of individual identified neurons in MD. All the subdivisions or "segments" of MD (medial, central, lateral) contained both stellate and fusiform cells. The dendritic domain of both types of cells was predominantly restricted to the same segment of MD that contained the cell body of the neuron. Typical stellate neurons were found near the center of each segment, with radiating dendrites that extended to but not across the boundaries of the segment. Fusiform cells were usually located close to the segmental or nuclear boundaries and tended to have dendrites oriented parallel to those borders; again, the dendrites tended not to extend across borders between segments or at the outer edge of MD. In the medial segment of MD many fusiform cells had especially bipolar dendritic configurations, generally with a dorsoventral orientation. Because no small neurons were identified that might correspond to thalamic interneurons, all the impregnated cells in MD are presumed to be thalamocortical projection neurons. These results indicate that cells and their major dendrites are confined to a single segment of MD, with little dendritic overlap across segmental or nuclear borders. The segments of MD may therefore be considered to be relatively independent subnuclei. The distribution of the four types of synapses previously identified in MD (Kuroda and Price, J. Comp. Neurol., 303:513-533, 1991) was determined along several identified dendrites studied with the Golgi-EM method. Primary dendrites were contacted mostly by large axon terminals, including both large, round vesicle (LR) terminals and large, pleomorphic vesicle (LP) terminals, as well as a few small to medium sized terminals with pleomorphic vesicles (SMP). No small terminals with round vesicles (SR terminals) were observed to make synapses with primary dendrites. Secondary and tertiary dendrites received synapses from all types of axon terminals. Higher order dendrites were contracted predominantly by SR boutons, but they also carried some LR and SMP terminals. In addition, SMP boutons were often found to form symmetric contacts with cell somata.     

Observations on the synaptology of intracellularly injected spinothalamic tract neurons in the cat

Single spinothalamic tract cells in the deep lumbar group have been injected with horseradish peroxidase and their dendritic trees examined on the electron microscope. Large dendrites are surrounded by rosettes of from 5 to 12 synaptic terminals. Most terminals contain round vesicles but some terminals contain flattened clear vesicles and others contain membranous tubes or cisterns. Large (mean diameter 100 nm) round, dense-core vesicles are found in both terminals containing clear round vesicles and terminals containing flattened vesicles. As yet none of those terminals on STT cell dendrites have been found participating in axo-axonic synapses, suggesting that presynaptic inhibition or facilitation plays no role in modulating the responses of these cells to presynaptic activity.     

Fine structure of the medullary lateral line area of Chelon labrosus (order perciformes), a nonelectroreceptive teleost

The ultrastructure and synaptic organization of the nucleus medialis and cerebellar crest of the teleost Chelon labrosus have been investigated. The nucleus medialis receives projections from the anterior and posterior lateral line nerves. This nucleus consists of oval neurons and large crest cells (“Purkinje-like” cells) whose apical dendrites branch in the overlying molecular layer, the cerebellar crest. In the dorsal region of the nucleus medialis, the perikarya and smooth primary dendrites of the crest cells are interspersed among myelinated fibers and nerve boutons. The ventral layer of the nucleus medialis contains crest cell perikarya and dendrites as well as oval neurons. The cerebellar crest lacks neuronal bodies, but the apical dendrites of crest cells receive synapses from unmyelinated and myelinated fibers. In the cerebellar crest, two types of terminals are presynaptic to the crest cell dendrites: boutons with spherical vesicles that from asymmetric synapses with dendritic spines and boutons containing pleomorphic vesicles that from symmetric synapses with dendritic spines and boutons containing pleomorphic vesicles that from symmetric synapses directly on the dendritic shaft. Most axon terminals found on the somata and primary dedrites of crest cells in the nucleus medialis have pleomorphic vesicles and form symmetric contacts, though asymmetric with spherical vesicles and mixed synapses can be observed; these mixed synapses exhibit gap junctions and contain spherical vesicles. Unlike crest cells, the oval neuron perikarya receive three types of contacts (symmetric, asymmetric, and mixed). The origins and functions of these different bouton types in the nucleus medialis are discussed. © 1995 Willy-Liss, Inc.     

A note on the synapses between vesicle containing profiles in the pontine nuclei of the cat

In the cat synapses between vesicle containing profiles were observed in ventral and dorsolateral pontine nuclei. The presynaptic elements consisted of two types of axon terminals: axon terminals characterized by a population of small (38-40 nm) round synaptic vesicles (SSV) and axon terminals containing pleomorphic synaptic vesicles (PSV). The postsynaptic pale elements (PP) had pleomorphic vesicles and some features attributed to dendrites. In the dorsolateral pontine nucleus most of PP profiles took part in serial synapses, usually as an intermediate component, they were rarely observed in triads. On the basis of their electron microscopical appearance and synaptic relations they might be considered to represent a dendritic part of putative interneurons.     

Ultrastructure of the mammillotegmental projections to the ventral tegmental nucleus of Gudden in the rat.

This study examines the termination pattern of axons from the medial mammillary nucleus within the ventral tegmental nucleus of Gudden (TV) in rats by using anterograde transport of horseradish peroxidase conjugated with wheat germ agglutinin (WGA-HRP) and visualized with tetramethylbenzidine. The neuropil of TV contains three classes of axodendritic terminals, that is, terminals containing round, flat, and pleomorphic synaptic vesicles. These types make up 55.6%, 26.1%, and 18.3%, respectively, of all normal axodendritic terminals. Injection of WGA-HRP into the medial mammillary nucleus permits ultrastructural recognition of anterogradely labeled terminals within the TV. More than 80% of the labeled terminals contain round synaptic vesicles and form asymmetric synaptic contacts, whereas about 16% contain flat synaptic vesicles with symmetric synaptic contacts. There are a few labeled terminals with pleomorphic vesicles and only a few axosomatic terminals. Almost all labeled terminals are small, having diameters of less than 1.5 microns. Compared with the distributions of normal and labeled terminals with round vesicles, there is an increase of the percentage of labeled terminals with round vesicles on the intermediate dendrites (1-2 microns diameter) and a decrease on the distal dendrites (less than 1 micron diameter). Anterogradely labeled axon terminals often contact retrogradely labeled dendrites. These results suggest that the medial mammillary neurons send mainly excitatory as well as a few inhibitory inputs to the dendrites of TV and have direct reciprocal contacts with the TV neurons.     

Neuronal and synaptic organization of the normal dorsal lateral geniculate nucleus of the squirrel monkey, Saimiri sciureus

The normal cellular architecture and synaptic organization of the dorsal lateral geniculate nucleus (LGN) of Saimiri sciureus has been studied with light and electron microscopic techniques. Golgi preparations reveal at least four types of neurons: type I and II are large and medium-sized cells; type II cells have grape-like dendritic protrusions, while type I cells do not. Type III small neurons have very long dendrites that cross laminar borders freely; and type IV very small neurons resemble glial cells. The last type may correspond to small, spindle-shaped or round, neurons which show somato-dendritic synapses under the electron microscope. Types I and II neurons are regarded as geniculocortical relay cells. Types III and IV are good candidates for interneurons. A serial dorsal to ventral interlaminar dendritic overlap is noted throughout the LGN. With the electron microscope, several types of axonal profiles can be seen: large axons with round vesicles (RL's), small axons with round vesicles (RS's), and intermediate axons with flattened or pleomorphic vesicles (F's). The RL's are retinal terminals; some of the RS's are corticogeniculate fibers; while the F's are believed to be intrageniculate in origin. The F type is then subdivided into F₁ and F₂; F₁ being darker and containing more evenly dispersed synaptic vesicles than F₂. There is also a distinct class of presynaptic dendrites, F_d, which contains pleomorphic vesicles and has a light cytoplasmic density similar to that of the F₂ profiles. It is possible that some or all of the F₂ processes may prove to be dendritic. Somato-dendritic synapses arise from very small neurons and form a part of the normal synaptic organization in the LGN. The RL and RS axons form asymmetrical synaptic contacts, whereas the F (F₁, F₂ and F_d) processes mainly form symmetrical ones. Non-synaptic filamentous contacts are also found. The rules of synaptic connectivity are such that the RL and RS terminals are never synaptic to either the RL or the RS terminals, and presynaptic to other dendrites. If the F profiles contact each other, the F₁ axon is never the post-synaptic element. The RL and F processes synapse upon any part of the perikaryal and dendritic surfaces, whereas the RS terminals do not contact the soma.     

The ultrastructural localization of enkephalin and substance P immunoreactivities in the nucleus tractus solitarii of the cat

In the medial and commissural subdivisions of the nucleus tractus solitarii enkephalin and substance P immunoreactivities were localized within synaptic terminals, unmyelinated axons, and neuronal cell bodies. Both enkephalin and substance P immunoreactivities were contained within synaptic terminals which had a mixture of small clear vesicles and dense core vesicles. The presence of dense core vesicles within both the enkephalin- and substance P-immunoreactive terminals was a consistent feature, although they were not associated with the actual synaptic junction. While enkephalin- and substance P-immunoreactive terminals shared a similar morphology, their respective distributions along the dendritic tree were quite distinct. Enkephalin-immunoreactive terminals contacted mainly the cell body and proximal portions of the dendritic tree. In contrast, substance P-immunoreactive terminals synapsed predominantly with spines and shafts of small to medium-sized dendrites. Few substance P-immunoreactive terminals contacted proximal dendrites and they were never presynaptic to the neuronal cell body. This apparent segregation of synaptic terminals on neurons suggests that enkephalin synapses have a more pronounced effect than substance P terminals.     

Immunocytochemical localization of GABA in the cochlear nucleus of the guinea pig

The immunocytochemical distribution of gamma-aminobutyric acid (GABA) was determined in the cochlear nucleus of the guinea pig using affinity-purified antibodies made against GABA conjugated to bovine serum albumin. Light microscopic immunocytochemistry shows immunoreactive puncta, which appear to be GABA-positive presynaptic terminals, distributed throughout the cochlear nucleus. In the ventral cochlear nucleus, these puncta are often found around unlabeled neuronal cell bodies. While occasional labeled small cells are found in the ventral cochlear nucleus, most GABA-immunoreactive cell bodies are present in the superficial layers of the dorsal cochlear nucleus. Based on size and shape, immunoreactive cells in the dorsal cochlear nucleus are divided into 3 classes: medium round cells with diameters averaging 16 microns, small round cells with average diameters of 9 microns and small flattened cells with major and minor diameters averaging 11 and 6 microns, respectively. Labeled fusiform and granule cells are not seen. A similar distribution of label was seen using antibodies against glutamic acid decarboxylase. Electron microscopic immunocytochemistry of the anteroventral cochlear nucleus shows GABA immunoreactive boutons containing oval/pleomorphic synaptic vesicles on cell bodies and dendrites. Other major classes of terminals, including those with small round, large round and flattened synaptic vesicles are unlabeled.     

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.     

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.     

The ultrastructure of the subnucleus gelatinosus of the nucleus of the tractus solitarius in the cat

The dorsomedial region of the nucleus of the tractus solitarius termed the subnucleus gelatinosus (SNG) was studied at the light and electron microscopic level in the cat. In cresyl violet and luxol fast blue stained sections the SNG contained small neuronal somata that were scattered throughout a pale-staining neuropil containing few myelinated fibers. These neurons were difficult to impregnate with Golgi staining techniques, but in successful impregnations the somata were observed to be 10--19 micrometers in diameter and bore few sparsely branching primary dendrites. Spines were present on the dendrites of some neurons and were more numerous on distal portions of the dendritic tree. Ultrastructural examination of the SNG revealed that the neuronal complement consisted of round, oval, or spindle shaped neurons with little or no organized Nissl substance. Rare myelin-like ensheathments of neuronal perikarya were also observed. Bundles of fine unmyelinated axons that coursed mainly longitudinally were a prominent feature of the area. The most common type of axon terminal observed contained mainly round clear vesicles, approximately 31 nm in diameter, and made asymmetrical synaptic contact with a dendritic profile. Pleomorphic vesicle-containing terminals involved in symmetrical synaptic contact were also commonly seen. Axodendritic and axosomatic synapses were associated with terminals containing either round clear vesicles or pleomorphic vesicles. Less commonly, dendrodendritic and dendrosomatic synapses were seen, the presynaptic elements of which contained pleomorphic vesicles. Following removal of a nodose ganglion, degenerating terminals of vagal afferent fibers were observed throughout the neuropil. Such terminals contained round, clear vesicles with an occasional large, dense-cored vesicle, and made axodendritic and axosomatic synaptic contacts.     

Neuronal associations in the rat suprachiasmatic nucleus demonstrated by immunoelectron microscopy.

The synaptic associations of neurons in the suprachiasmatic nucleus (SCN) of rats were examined by single immunolabeling for somatostatin (SRIH) and arginine vasopressin (AVP), and double immunolabeling for SRIH plus AVP and vasoactive intestinal polypeptide (VIP) plus AVP. Single immunolabeling showed that SRIH neurons, which displayed some somatic and dendritic spines, formed synaptic contacts with immunonegative and positive axon terminals. AVP neurons also formed synaptic contacts with both immunonegative and positive axon terminals. The immunonegative terminals contained small, spherical clear vesicles or flattened clear vesicles. A few immunopositive AVP fibers made synapses with immunonegative somatic or dendritic spines. Double immunolabeling showed synaptic associations between SRIH axons and AVP cell bodies or dendritic processes, and between AVP axons and the somata or dendrites of SRIH neurons. These findings suggest a reciprocal relation between the two types of neurons. Synaptic contacts between AVP neurons and VIP axon terminals were also demonstrated. Previously, we found synapses between SRIH axons and VIP neurons. Thus SRIH neurons appeared to regulate AVP and VIP neurons. On the basis of these findings, two possible oscillation systems of the SCN are proposed.     

Prefrontal cortical efferents in the rat synapse on unlabeled neuronal targets of catecholamine terminals in the nucleus accumbens septi and on dopamine neurons in the ventral tegmental area.

Physiological and pharmacological studies indicate that descending projections from the prefrontal cortex modulate dopaminergic transmission in the nucleus accumbens septi and ventral tegmental area. We investigated the ultrastructural bases for these interactions in rat by examining the synaptic associations between prefrontal cortical terminals labeled with anterograde markers (lesion-induced degeneration or transport of Phaseolus vulgaris leucoagglutinin; PHA-L) and neuronal processes containing immunoreactivity for the catecholamine synthesizing enzyme, tyrosine hydroxylase. Prefrontal cortical terminals in the nucleus accumbens and ventral tegmental area contained clear, round vesicles and formed primarily asymmetric synapses on spines or small dendrites. In the ventral tegmental area, these terminals also formed asymmetric synapses on large dendrites and a few symmetric axodendritic synapses. In the nucleus accumbens septi, degenerating prefrontal cortical terminals synapsed on spiny dendrites which received convergent input from terminals containing peroxidase immunoreactivity for tyrosine hydroxylase, or from unlabeled terminals. In single sections, some tyrosine hydroxylase-labeled terminals formed thin and punctate symmetric synapses with dendritic shafts, or the heads and necks of spines. Close appositions, but not axo-axonic synapses, were frequently observed between degenerating prefrontal cortical afferents and tyrosine hydroxylase-labeled or unlabeled terminals. In the ventral tegmental area, prefrontal cortical terminals labeled with immunoperoxidase for PHA-L were in synaptic contact with dendrites containing immunogold reaction product for tyrosine hydroxylase, or with unlabeled dendrites. These results suggest that: (1) catecholaminergic (mainly dopaminergic) and prefrontal cortical terminals in the nucleus accumbens septi dually synapse on common spiny neurons; and (2) dopaminergic neurons in the ventral tegmental area receive monosynaptic input from prefrontal cortical afferents. This study provides the first ultrastructural basis for multiple sites of cellular interaction between prefrontal cortical efferents and mesolimbic dopaminergic neurons.     

Synaptic circuitry of physiologically identified W-cells in the cat's dorsal lateral geniculate nucleus

The cat's retinogeniculocortical system is comprised of at least 3 parallel pathways, the W-, X-, and Y-cell pathways. Prior studies, particularly at the level of the lateral geniculate nucleus, have focused on X- and Y-cells. In the present study, we describe the synaptic inputs for 2 geniculate W-cells from the parvocellular C-laminae after these neurons were physiologically identified and intracellularly labeled with HRP. For each of the W-cells, we examined electron micrographs taken from over 500 consecutive thin sections; we reconstructed the entire soma plus roughly 15% of the dendritic arbor and determined the pattern of synaptic inputs to these reconstructed regions of each neuron. In several ways, each W-cell exhibits a similar pattern of synaptic inputs. First, we estimate that each W-cell receives approximately 3000-4000 synaptic contacts, which occur most densely on dendrites 50-150 microns from each soma. Second, axosomatic contacts are extremely rare, and most derive from terminals with flattened or pleomorphic vesicles (F terminals). Third, terminals with round vesicles, large profiles, and pale mitochondria (RLP terminals), which are presumed to be retinal terminals, form only about 2-4% of all synapses onto these W-cells; these synapses occur on proximal dendrites. Fourth, F terminals, which provide roughly 15-20% of all synaptic input to these cells, occupy the same region of proximal dendritic arbor as do the RLP terminals. Fifth, and finally, terminals with round vesicles, small profiles, and dark mitochondria (RSD terminals) provide the majority of synapses along all portions of the dendritic arbor. Compared with geniculate X- and Y-cells of the A-laminae (Wilson et al., 1984), these W-cells are innervated by fewer synapses overall and, in particular, by dramatically fewer synapses from RLP (or retinal) terminals. This paucity of direct retinal input to geniculate W-cells might explain the remarkably poor responsiveness of these neurons to visual stimuli and to electrical activation of the optic chiasm.     

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.     

Fine structure of the lateral mammillary projection to the dorsal tegmental nucleus of Gudden in the rat.

The synaptic organization of projections from the lateral mammillary neurons within the dorsal tegmental nucleus of Gudden is studied in the rat with the aid of anterograde transport of horseradish peroxidase conjugated with wheat germ agglutinin (WGA-HRP) and visualized with tetramethylbenzidine. The dorsal tegmental nucleus consists of the pars ventralis (TDV) and the pars dorsalis (TDD). The normal neuropil of the dorsal tegmental nucleus contains three classes of axodendritic terminals, that is, terminals containing round, flat, and pleomorphic vesicles. They make up 44%, 5%, and 51%, respectively, of all axodendritic terminals in the TDV, and 62%, 1%, and 37% in the TDD. Injection of WGA-HRP into the lateral mammillary nucleus permits ultrastructural recognition of many anterograde labeled terminals within both the TDV and TDD. In the TDV, 81% of the labeled terminals contain round synaptic vesicles and make asymmetric synaptic contacts. A few of the labeled terminals contain pleomorphic vesicles and make symmetric synaptic contacts. More than 50% of the labeled terminals contact intermediate dendrites (1-2 microns diameter). In the TDD, almost all labeled terminals are small, contain round vesicles, and make asymmetric synaptic contacts. These terminals mainly contact intermediate as well as distal (less than 1 micron diameter) dendrites. There are only a few labeled terminals with pleomorphic vesicles and no terminals with flat vesicles. The termination pattern of the lateral mammillary neurons in the TDV is similar to that in the TDD. Anterograde labeled axon terminals often contact retrograde labeled dendrites in the TDV. No reciprocal connections are present in the TDD. These results suggest that the TDV and the TDD receive mainly excitatory and a few inhibitory inputs from the lateral mammillary nucleus. The TDV neurons also have direct reciprocal connections with the lateral mammillary neurons.