The termination of callosal fibres in the auditory cortex of the rat. A combined Golgi--electron microscope and degeneration study

When the corpus callosum of the rat is sectioned, the callosal fibres in the cerebral cortex undergo degeneration. In the auditory cortex (area 41) the degenerating axon terminals form asymmetric synapses, and the vast majority of them synapse with dendritic spines. Some other synapse with the shafts of both spiny and smooth dendrites, and a few with the perikarya of non-pyramidal cells. The degenerating axon terminals are contained principally within layer II/III, in which they aggregate in patches. Using a technique in which neurons within the cortex are Golgi-impregnated, then gold-toned and examined in the electron microscope, it has been shown that the dendritic spines of pyramidal neurons with cell bodies in different layers receive the degenerating callosal afferents. The spines arise from the main apical dendritic shafts and their branches, from the dendrites of the apical tufts, and in some cases from the basal dendrites of the pyramidal neurons. The shafts of some pyramidal cell apical dendrites also form asymmetric synapses with callosal afferents. Since we have encountered no spiny non-pyramidal neurons in Golgi preparations of rat auditory cortex, and because other types of non-pyramidal cells have few dendritic spines, it is concluded that practically all of the dendritic spines synapsing with callosal afferents originate from pyramidal neurons.     

The projection of the lateral geniculate nucleus to area 17 of the rat cerebral cortex. II. Terminations upon neuronal perikarya and dendritic shafts

Summary The forms of dendrites in layer IV receiving degenerating thalamocortical axon terminals directly on their shafts were examined in serial thin sections. Reconstructions showed these dendrites varied in thickness between 2.5 and 0.5 m. They had essentially smooth contours and rarely showed evidence of protrusions or spines. They were further characterized by the presence of many synapses along their shafts. Only about one in 12 of these synapses was formed by degenerating thalamocortical axon terminals.These smooth dendrites emerged from neuronal perikarya that also received degenerating axon terminals which formed asymmetric synaptic junctions. Such cell bodies bore both symmetric and asymmetric synaptic junctions, and not all of the latter were caused to degenerate after a thalamic lesion. These postsynaptic neurons appeared to be of two kinds, ones with thin dendrites that often contained closely packed microtubules, and others with thicker dendrites that emerged from the poles of oval perikarya.     

The projection of the lateral geniculate nucleus to area 17 of the rat cerebral cortex. V. Degenerating axon terminals synapsing with Golgi impregnated neurons

Summary The sites of termination of afferents from the lateral geniculate nucleus to layer IV and lower layer III in area 17 of the rat visual cortex have been determined by use of a combined degeneration—Golgi/EM technique. Degeneration of geniculocortical axon terminals was produced by making lesions in the lateral geniculate body. After the animals had been allowed to survive for two days, the ipsilateral visual cortex was removed and impregnated by the Golgi technique. Suitably impregnated neurons and their processes in layer IV and lower layer III were then gold-toned and deimpregnated for examination in the electron microscope. A search was made for synapses between degenerating axon terminals and the gold-labelled postsynaptic neurons.Geniculocortical synapses were found to involve: (1) the spines of basal dendrites, as well as those of proximal shafts and collaterals of apical dendrites of layer III pyramidal neurons; (2) the spines of the apical dendritic shafts and collaterals of layer V pyramidal neurons; (3) the perikaryon and dendritic spines of a sparsely-spined stellate cell; and (4) the perikaryon and dendrites of a smooth, bitufted stellate cell. In view of this variety of postsynaptic elements it is suggested that all parts of the perikarya and dendrites of neurons contained in layer IV and lower layer III which are capable of forming asymmetric synapses can be postsynaptic to the thalamic input.Finally, an analysis of the known neuronal interrelations within the rat visual cortex is presented.     

Interlaminar connections of tree shrew visual cortex.

The intracortical projections of neurons in layers II and upper III of tree shrew visual cortex were studied after terminal lesions in the supragranular layers of area 17. Examination for terminal degeneration was made using ultrastructural techniques. The majority of degenerating terminals were found in layers V and, to a lesser extent, VI, and were presynaptic to neural profiles in the following distribution: 80.5% on spines of small to medium size dendrites, 19% on dendrite shafts, and less than 1% on neuronal perikarya. Degenerating axons coursed in vertical bundles through layers III, IV, V and VI. These findings are similar to those previously described in rat visual cortex.     

The projection of the lateral geniculate nucleus to area 17 of the rat cerebral cortex, IV terminations upon spiny dendrites

Summary The forms of the spiny dendrites in layer IV receiving degenerating thalamocortical axon terminals have been examined in serial thin sections. Reconstructions of segments of these dendrites show that the axon terminals synapse with both the dendritic spines and the dendritic shafts. No main shafts of apical dendrites of pyramidal neurons were found to synapse with the thalamic afferents, which are received mainly by spiny dendrites 1–2 m in diameter, at least some of which appear to be the oblique branches of apical dendrites. The forms of these postsynaptic dendrites are so variable that is is concluded they arise from more than one morphological type of neuron. The conclusion based on this and previous articles in the series is that most neuronal elements in layer IV which form asymmetric synaptic junctions are potential recipients of the thalamocortical afferents.     

Proliferation of thalamic afferents in cerebral cortex altered by callosal deafferentation

Summary In area 41, the auditory region of rat neocortex, callosal afferents project to layers I through III and thalamic afferents project to deep layer III through IV. Thus, these two extrinsic systems of afferents project simultaneously to only a narrow lamina in mid to low layer III. For this study, this narrow region of overlap is quantitatively examined to determine the distribution of callosal and thalamic afferents by observing degenerating terminals produced by separate callosal and thalamic lesions. The results show that of all asymmetric synapses observed in the neuropil of this narrow zone, 84% are dendritic spines and the balance are dendritic shafts. Although both callosal and thalamic afferents prefer to synapse with dendritic spines in the neuropil, 78% of the thalamic afferents synapse with dendritic spines while 93% of the callosal afferents synapse with dendritic spines.Vaughan & Foundas (1982) have shown that 3 months after callosal lesions in 1-month-old animals, additional thalamic axons have grown into, and proliferated in, this part of mid to low layer III. Quantitative analysis of the distribution of the degenerating thalamic axon terminals in these long-term callosally lesioned animals has been used to determine whether the proliferating thalamic afferents demonstrate any specificity in the pattern of synapses they make or whether the callosally deafferented neurons determine the pattern of synapses. The results indicate that thalamic axons do exhibit axon specificity, for after they have proliferated into the callosal domain, 80% of the degenerating terminals synapse with dendritic spines and 20% synapse with shafts. This distribution is most comparable to the normal distribution of thalamic axons in this region.     

The projection of the visual cortex on the Clare-Bishop area in the cat

Summary Following large lesions of the cat visual cortex, the distribution of degenerating terminal boutons in the Clare-Bishop area was studied electron microscopically. Degenerating boutons were found throughout the cortical layers but mostly in layer III (51% of the total number of degenerating boutons) and layer V (24%). A smaller number of boutons were found in layers II (12%) and IV (9%), and very few in layers VI (3%) and I (1%). No degenerating terminals were observed in the upper two-thirds of layer I. Seventy-six per cent of the total degenerating boutons terminated on dendritic spines, 22% on dendritic shafts, and 2% on somata. Some degenerating boutons made synaptic contacts with somata and dendrites of nonpyramidal neurons. For example, one degenerating bouton was observed in contact with an apical dendrite of a fusiform cell. Three examples of dendritic spines, with which degenerating boutons made synaptic contacts, were found to belong to spinous stellate cells. No degenerating boutons were observed making synaptic contacts with profiles that could conclusively be traced to pyramidal cell somata.     

Types and spatial distribution of vasoactive intestinal polypeptide (VIP)-containing synapses in the rat visual cortex

Summary In the rat visual cortex vasoactive intestinal polypeptide (VIP)-containing structures were studied by means of light and electron microscopy and image analysis. VIP-immunoreactive axon terminals were found to form symmetric synapses with small dendritic shafts, dendritic spines and somata of pyramidal cells and interneurons. VIP-terminals often occured in pairs with VIP-negative, asymmetric synapses on the same postsynaptic structure. VIP-immunostained dendrites and perikarya were contacted by a purely asymmetric and a mixed population of VIP-negative terminals, respectively. Synaptic connections between two VIP-neurons are seldom as compared to the other types of VIP-synapses. Quantitative studies obtained by the image analysis of VIP-stained boutons and dendritic particles in light microscopic preparations suggest a distinct laminar distribution. Dendritic particles are most frequent in layers I–II, whereas axonal boutons have three laminar accumulations: at the border of layers I–II, in layer IV and layer VI. Together with previous results, the present findings argue for a non-random spatial distribution of VIP-boutons.     

The electron microscopic localization of methionine-enkephalin within the superficial layers (I and II) of the spinal cord

The synaptic relationships of methionine-enkephalin containing axon terminals within layers I and II of the rat spinal cord have been investigated using immunocytochemical techniques. Labelled terminals contained large numbers of spherical synaptic vesicles and formed synaptic contacts with dendritic shafts and spines and to a lesser extent with cell bodies within the superficial layers of the dorsal horn. A large number of labelled terminals were seen in apposition to profiles containing pleomorphic vesicles, particularly within layer I and outer layer II. Following rhizotomy, degenerating primary afferent axon terminals were found throughout layers I and II but only in one case was a synaptic relationship with a labelled terminal observed.Thus we were unable to find a morphological correlate of the reported effects of opiates on sensory axons and terminals.     

The termination of thalamo-cortical fibres in the visual cortex of the cat

Summary An electron microscopic study has been made of the site and mode of termination of thalamo-cortical fibres in area 17 of the visual cortex of the cat. Thalamo-cortical fibres had been selectively interrupted 4–5 days before perfusion of the brain. In agreement with previous studies, degenerating axon terminals were found in layer I, in the deep part of layer III, and in layer IV of the cortex. In addition, a few degenerating thalamo-cortical axon terminals were found making synapses upon spines and small dendrites in layer VI. Two examples were seen of degenerating axon terminals making axo-dendritic synapses upon dendrites in continuity with their cell bodies. These neurons were not large stellate cells and were probably pyramidal.     

Light and electron microscopic immunocytochemical analysis of the serotonin innervation of the rat visual cortex

Summary The serotonin afferents of the rat visual cortex were examined immunocytochemically at the light and electron microscopic levels. Immunoreactive fibres were typically thin, tortuous and varicose. Occasionally, some thicker fibres were found. The orientation of labelled axons varied according to laminar position, with fibres running parallel to the pial surface present mainly in layers I and VI, and radially oriented fibres prominent in layers II and III. Branches arising from horizontal or radially oriented fibres were seen to form irregularly shaped loops particularly in layers IV and V. The density of innervation and the prevailing axonal orientation in each cortical layer were similar in both coronal and parasagittal planes.The ultrastructural features of serotonin-labelled axon terminals were examined in single and serial ultrathin sections. While in single sections the majority did not exhibit synaptic specializations, extensive serial section analysis showed that virtually all of these terminals were engaged in junctional complexes. Postsynaptic elements were spines and dendritic shafts, including pyramidal cell apical dendrites, with both symmetrical and asymmetrical membrane specializations. In axospinous synapses, the labelled terminals were usually adjacent to unstained axon terminals contacting the same postsynaptic element.     

Quantification of synapses formed with apical dendrites of golgi-impregnated pyramidal cells: Variability in thalamocortical inputs,but consistency in the ratios of asymmetrical to symmetrical synapses

Five pyramidal cells from the posteromedial barrel subfield of mouse SmI cortex were labeled by Golgi impregnation and then gold-toned and de-impregnated (Fairén, Peters & Saldanha, 1977). Subsequently, 40 to 70 μm-long segments of their apical dendrites occurring in layer IV were graphically reconstructed from serial thin sections to determine the distribution of their synapses. Thalamocortical synapses onto these dendritic segments were identified by lesion-induced degeneration.The synaptic pattern of the pyramidal cell apical dendrites was consistent with previous reports in that most synapses occurred on spines and were asymmetrical and the smaller number of shaft synapses were primarily symmetrical. Some axospinous synapses were formed by degenerating thalamocortical axon terminals. The proportion of thalamocortical synapses onto reconstructed dendritic segments was different for different neurons. For example, thalamocortical axon terminals formed 15% of the synapses involving the spines of the reconstructed segment from a medium superficial layer V pyramidal cell and 10% of the synapses onto portions of the segment from a large layer VI pyramidal cell. In contrast, reconstructed dendritic segments of three other layer VI pyramidal cells formed no more than one thalamocortical synapse.An analysis of the distribution of synapses onto reconstructed dendritic segments revealed that the segments of 3 medium and large pyramidal cells had a ratio of about 12.5 asymmetrical synapses per symmetrical synapse, whereas the segments of 2 small pyramidal cells had ratios of only 6.5 asymmetrical synapses per symmetrical synapse. That these ratios fall into 2 distinct groups suggests that the relative number of asymmetrical and symmetrical synapses is stereotyped within populations of neurons.     

Recurrent axon collaterals of corticothalamic projection neurons in rat primary somatosensory cortex contribute to excitatory and inhibitory feedback-loops

Intrinsic circuitry within the primary somatosensory cortex of the rat was examined in a combined light and electron microscope study. Corticothalamic projection neurons were retrogradely labeled by applying Phaseolus vulgaris leucoagglutinin (PHA-L) into the ventro-posteromedial thalamic nucleus (VPM). Most labeled neurons were pyramidal cells of layer VI. Postsynaptic targets of recurrent axon collaterals originating from these neurons were assessed in layers IV and V. Single labeled cells, complete with recurrent collaterals, could be isolated in barrels in which no anterograde transport had taken place. These findings were confirmed by first eliminating thalamocortical projections from the VPM with kainic acid and then applying PHA-L into the same nucleus. This procedure led to selective retrograde accumulation of tracer in layer VI pyramidal cells. Reconstructed portions of labeled axonal trees reached layer IV, bringing numerous boutons to layers IV, V and VI. The boutons had characteristic drumstick-like shapes. In order to identify postsynaptic targets, 4 sections of axons stemming from 3 neurons were reembedded and serially sectioned for electron microscopy. The ultrastructure of 72 asymmetric synapses, all belonging to identified collaterals, was analysed. Of the 72 terminals, 44 (59.5%) ended on dendritic spines and 30 on shafts of dendrites (40.5%). Perikarya were not among the targets. In a subset of the sample, the nature of the target neurons was examined by postembedding immunohistochemistry for -amino butyric acid (GABA) after staining for PHA-L. A total of 42 labeled terminals was found in layers IV and V; 23 (55%) were located on GABA-negative spines and 19 (45%) on dendritic shafts. Only 6 (32%) of the shafts were GABA-positive. The remaining ones were either clearly GABA-negative, or labeled only at background levels (n=13; 68%). The results show that most synapses of corticothalamic projection neurons found in layers IV and V terminate on spines and shafts of GABA-negative dendrites. This finding suggests that such recurrent collaterals are involved in both excitatory and inhibitory feedback mechanisms.     

Termination of cortical afferents on identified neurons in the caudate nucleus of the cat

Summary A combined Golgi/electron microscopic technique was used to investigate the fine structure and synaptology of Golgi-stained spiny neurons in the caudate nucleus of the cat. In order to study the termination sites of cortical afferents on Golgistained spiny neurons, cortical fibres were caused to degenerate by making extensive cortical lesions 3 days prior to fixation of the animals.When examined in the electron microscope, perikarya of labelled spiny neurons have a round nucleus, a few mitochondria and microtubules, and a poorly developed Golgi apparatus and rough endoplasmic reticulum. Only rarely are axo-somatic contacts seen. Labelled dendrites exhibit a moderate number of microtubules and sometimes elongated mitochondria. Numerous labelled spines are seen in the vicinity of their parent dendrites. They are contacted by smaller type I and type III boutons and larger type IV boutons (Hassler et al. 1978). Large boutons filled with clear round vesicles establish symmetric contacts with labelled dendritic shafts.Degenerating boutons of cortical afferents are seen in contact with spines and, more rarely, with dendritic shafts of Golgi-stained spiny neurons. All degenerating boutons synapsing with labelled structures are found some distance from the cell body. No contacts of degenerating cortical boutons with the soma or with stem dendrites of Golgi-stained spiny neurons are found.     

Dual axonal terminations from the retrosplenial and visual association cortices in the laterodorsal thalamic nucleus of the rat

Light and electron microscopic tracing studies were conducted to assess the synaptic organization in the laterodorsal thalamic nucleus (LD) of the rat and the laminar origins of corticothalamic terminals from the retrosplenial and visual association cortices to LD. A survey of the general ultrastructure of LD revealed at least three types of presynaptic terminals identified on the basis of size, synaptic vesicle morphology, and synaptic membrane specializations: (1) small axon terminals with round synaptic vesicles (SR), which accounted for the majority of terminal profiles and made asymmetric synaptic contacts predominantly with small dendritic shafts and spines; (2) large axon terminals with round synaptic vesicles (LR), which formed asymmetric synaptic contacts mainly with large dendritic shafts; and (3) small to medium-size axon terminals with pleomorphic synaptic vesicles (SMP), which symmetrically synapsed with a wide range of postsynaptic structures from cell bodies to small dendrites. Synaptic glomeruli were identified, whereas no presynaptic dendrites were found. To characterize and identify corticothalamic terminals arising from the retrosplenial and visual association cortices that project to LD, wheat germ agglutinin conjugated to horseradish peroxidase (WGA–HRP) was injected into these cortices. Axons anterogradely labeled with WGA–HRP ended in both SR and LR terminals. On the other hand, dextran-tetramethylrhodamine injected into LD as a retrograde fluorescent tracer labeled large pyramidal cells of layer V as well as small round or multiform cells of layer VI in the retrosplenial and visual association cortices. These findings provide the possibility that corticothalamic terminations from cortical neurons in layer V end as LR terminals, while those from neurons in layer VI end as SR boutons.     

Synaptic connections of morphologically identified and physiologically characterized large basket cells in the striate cortex of cat

Neurons were studied in the striate cortex of the cat following intracellular recording and iontophoresis of horseradish peroxidase. The three selected neurons were identified as large basket cells on the basis that (i) the horizontal extent of their axonal arborization was three times or more than the extent of the dendritic arborization; (ii) some of their varicose terminal segments surrounded the perikarya of other neurons. The large elongated perikarya of the first two basket cells were located around the border of layers III and IV. The radially-elongated dendritic field, composed of beaded dendrites without spines, had a long axis of 300-350 microns, extending into layers III and IV, and a short axis of 200 microns. Only the axon, however, was recovered from the third basket cell. The lateral spread of the axons of the first two basket cells was 900 microns or more in layer III and, for the third cell, was over 1500 microns in the antero-posterior dimension, a value indicating that the latter neuron probably fulfills the first criterion above. The axon collaterals of all three cells often branched at approximately 90 degrees to the parent axon. The first two cells also had axon collaterals which descended to layers IV and V and had less extensive lateral spreads. The axons of all three cells formed clusters of boutons which could extend up a radial column of their target cells. Electron microscopic examination of the second basket cell showed a large lobulated nucleus and a high density of mitochondria in both the perikarya and dendrites. The soma and dendrites were densely covered by synaptic terminals. The axons of the second and third cells were myelinated up to the terminal segments. A total of 177 postsynaptic elements was analysed, involving 66 boutons of the second cell and 89 boutons of the third cell. The terminals contained pleomorphic vesicles and established symmetrical synapses with their postsynaptic targets. The basket cell axons formed synapses principally on pyramidal cell perikarya (approximately 33% of synapses), spines (20% of synapses) and the apical and basal dendrites of pyramidal cells (24% of synapses). Also contacted were the perikarya and dendrites of non-pyramidal cells, an axon, and an axon initial segment. A single pyramidal cell may receive input on its soma, apical and basal dendrites and spines from the same large basket cell.(ABSTRACT TRUNCATED AT 400 WORDS)     

Presynaptic dendrites and serial synapses in the intermediate and deep layers of the cat superior coliculus.

Presynaptic dendrites (PSDs) which participate in the serial synapses have frequently been found in the intermediate and deep layers of the cat superior colliculus. The PSDs are presynaptic to small dendritic shafts or spines with symmetrical membrane thikening, and postsynaptic to axon terminals with asymmetrical synaptic contact. Two types of the axon terminals are observed, both of which contain pleomorphic vesicles.     

Vasoactive intestinal polypeptide immunoreactive neurons in the primary visual cortex of the cat

Summary When cat visual cortex (area 17) is reacted with an antibody to vasoactive intestinal polypeptide (VIP) a variety of neuronal types is labelled. Many of the labelled neurons are bipolar in form and are most common in layers II and III, although significant numbers of bipolar neurons are also encountered in layer V. Multipolar cells are also labelled. These are most frequent in layer IV and have a variety of shapes. In layer I, the labelled cells are of three varieties, i.e. horizontal bipolar cells, horizontal bitufted cells and multipolar neurons, while in layer VI the few VIP-positive neurons are horizontal bipolar cells. This suggests that all of the VIP-labelled neurons in cat area 17 are non-pyramidal in form, and this has been confirmed by electron microscopy. In these preparations, axon terminals are also labelled and under the light microscope it can be seen that these terminals occur both within the neuropil and around the cell bodies of some neurons, particularly neurons in layers II and III. Electron microscopy has shown that all of the labelled axon terminals form symmetric synapses and that those in the neuropil synapse with the shafts of smooth dendrites. These axodendritic synapses account for about 90% of the synapses formed by the labelled axon terminals. The remainder of the labelled axon terminals synapse with the cell bodies of pyramidal neurons. Parallels are drawn between these results and those previously obtained by examining those neuronal elements labelled with VIP antibodies in rat visual cortex.     

Synaptic connections, axonal and dendritic patterns of neurons immunoreactive for cholecystokinin in the visual cortex of the cat

A subpopulation of gamma-aminobutyric acid (GABA) containing neurons was reported to contain cholecystokinin-immunoreactive material in the visual cortex of cat [Somogyi et al., J. Neurosci. (1984) 4, 2590-2603]. In the present study pre-embedding immunocytochemistry was used to identify which of the several types of presumed GABAergic nonpyramidal cells in areas 17 and 18 contain cholecystokinin immunoreactivity. Most of the cholecystokinin-immunoreactive somata were found in layers II-III, they were less frequent in layers I and VI, and relatively rare in layers IV and V. The distribution and density of the axon terminals resembled that of the cell bodies. Two well defined types of cholecystokinin-immunoreactive neuron were distinguished: (1) double bouquet cells in layers II-III with vertically projecting axons, and (2) small basket cells with local axons either restricted to layers II-III, or descending to layer V. Additional cholecystokinin-positive cells showed features of bitufted or multipolar neurons in layers II-VI and horizontal cells in layer I, but these cells could be defined less well due to partial staining. Cholecystokinin-immunoreactive dendrites were found to run horizontally in layer I for several hundred micrometers. Some of the cholecystokinin-immunoreactive cells in layer VI had very long dendrites ascending radially up to layer III, as did their axons. A few cholecystokinin-immunoreactive cells appeared to have two axons and this was confirmed by electron microscopy. All cholecystokinin-immunoreactive neurons and terminals were separated from the basal lamina of blood vessels by glial endfeet. Random samples of boutons from each layer as well as identified terminals traced to their origin from local neurons were examined in the electron microscope. All of the boutons established symmetrical (type II) synaptic contacts with dendritic shafts, spines or somata. Quantitative electron microscopy of the postsynaptic targets of double bouquet cells and small basket cells demonstrated clear differences between these two types of neuron; basket cells having a higher proportion of their terminals in synaptic contact with somata. The findings that several distinct types of cortical neurons, as defined by their synaptic connections, contain cholecystokinin-immunoreactive material and that identified axons of all examined neurons form type II synaptic contacts suggests that the majority, if not all cholecystokinin-positive boutons forming type II contacts originate from local cortical cells. The distribution of targets postsynaptic to cholecystokinin-positive neurons is compared to those of cells labelled by other methods.     

Ultrastructure and synaptic connections of vasoactive intestinal polypeptide-like immunoreactive non-pyramidal neurons and axon terminals in the rat hippocampus

In the hippocampus, antibody raised against vasoactive intestinal polypeptide (VIP) labeled perikarya and processes of non-pyramidal neurons whereas these structures remained unlabeled in pyramidal cells and granule cells. In the present study, VIP-immunostaining was used to investigate the fine structure and synaptic connections of identified non-pyramidal neurons and of imrnunoreactive axon terminals in the CA1 region of the rat hippocampus by means of electron microscopic immunocytochemistry.From a number of cells studied, two VIP-like imrnunoreactive non-pyramidal neurons in the regio superior were selected for an electron microscopic analysis of serial thin sections. These cells were different with regard to the location of their cell bodies and the orientation of their dendrites. One cell was located in the stratum lacunosum-moleculare with dendritic processes oriented parallel to the hippocampal fissure. The second neuron was found in the inner one-third of the stratum radiatum. The dendrites of this cell ran nearly parallel to the ascending apical dendrites of the pyramidal cells. Both cells had a round or ovoid perikaryon and an infolded nucleus. The aspinous dendrites of both neurons were densely covered with synaptic boutons. These terminals were small, filled with spherical vesicles and established asymmetric synaptic contacts. No variations in the fine structure of the presynaptic boutons were found along the course of the labeled dendrites through the various hippocampal layers, although different afferents are known to terminate in these layers.Vasoactive intestinal polypeptide-like immunopositive axon terminals course through all layers of the hippocampus. In the stratum pyramidale they established symmetric synaptic contacts with the perikarya of pyramidal cells. In the stratum radiatum they made symmetric contacts with the shafts of apical dendrites of pyramidal cells but never contacted dendritic spines.The symmetric contacts with pyramidal cell perikarya suggest an involvement of the VIP-like immunoreactive axon terminals in pyramidal cell inhibition.