Cytochrome oxidase activity in the striate cortex and lateral geniculate nucleus of the newborn and adult macaque monkey

Summary The laminar location of cytochrome oxidase staining has been compared in the lateral geniculate nucleus and area 17 in newborn and adult macaque monkeys. In area 17 of the adult, the distribution of cytochrome oxidase activity confirmed published findings. In the newborn animals, the tissue reacted as strongly for cytochrome oxidase as in the adult but the pattern of labelling was different in two respects. Firstly in layer 1 activity was stronger and occupied a wider portion of this layer. Secondly, cytochrome oxidase staining in layer 4C occupied two separate bands, a small narrow band at the bottom of 4C and a wider one occupying the full width of 4C and spilling over into 4B. The pattern of cytochrome oxidase activity did not appear to be influenced by eccentricity in the newborn whereas, in the adult, label in 4C was more intense in cortex subserving central vision. In the lateral geniculate nucleus of the adult, the magnocellular layers and the most dorsal parvocellular layer reacted most strongly for cytochrome oxidase. In the newborn, parvocellular layers were more uniformly labelled and the difference between parvo and magnocellular layers more pronounced. These results are discussed in relationship to the development of thalamo-cortical projections in the monkey.     

Hypertrophy of neurons in dorsal lateral geniculate nucleus following striate cortex lesions in infant monkeys

Monkeys whose left striate cortex had been removed in infancy received bilateral injections of horseradish peroxidase (HRP) into the prelunate gyrus (PLG) prestriate cortex. Scattered large neurons in the dorsal lateral geniculate nucleus were retrogradely labeled in both hemispheres. On the lesioned side, the HRP-labeled cell bodies were 58% larger in area, showing an overall increase in soma size and complexity of dendritic field, suggesting a hypertrophy of the geniculate-PLG pathway following a neonatal striate cortex lesion.     

Synaptic targets of HRP-filled layer III pyramidal cells in the cat striate cortex

Summary There are numerous hypotheses for the role of the axon collaterals of pyramidal cells. Most hypotheses predict that pyramidal cells activate specific classes of postsynaptic cells. We have studied the postsynaptic targets of two layer III pyramidal cells, that were of special interest because of their clumped axon arborization near, and also 0.4–1.0 mm from the cell body, in register in both layers III and V. 191 terminations from four sites (layers III and V, both in the column of the cell and in distant clumps) were analysed by electron microscopy. Only one bouton contacted a cell body and that was immunoreactive for GABA. The major targets were dendritic spines (84 and 87%), and the remainder were dendritic shafts. Of these 13 were classed as pyramidal-like (P), 8 smooth cell-like (S) and three could not be classified. Four of five S types, but none of the seven P types tested were immunoreactive for GABA, supporting the fine structural classification. The putative inhibitory cells therefore formed not more than 5% of the postsynaptic targets, and their activation could only take place through the convergence of pyramidal cells onto a select population of GABA cells. The results show that the type of pyramidal cells with clumped axons studied here make contacts predominantly with other pyramidal cells. Thus the primary role of both the intra and intercolumnar collateral systems is the activation of other excitatory cells.     

Synaptic relationships between a multipolar stellate cell and a pyramidal neuron in the rat visual cortex. A combined Golgi-electron microscope study

Summary Two synapsing and impregnated neurons in the rat visual cortex have been examined by a combined Golgi-electron microscope technique in which the Golgi precipitate is replaced by gold particles. One of the neurons is a stellate cell with smooth dendrites and a well impregnated axon, while the other is a layer III pyramidal neuron. Light microscopy showed some boutons from the axonal plexus of the stellate cell closely apposed to the soma and dendrites of the pyramid and it was predicted that synapses were present at these sites. An electron microscopic examination of serial thin sections, in which the profiles of the impregnated neurons are marked by their content of gold particles, showed most of these predicted synapses to exist. Indeed, axon terminals of the stellate cell formed five symmetric synapses with the cell body of the pyramid, one with the apical dendritic shaft and three with basal dendrites. Reasons are given for believing these synapses to be inhibitory.In addition, it was found that one of the axon terminals of the stellate cell synapsed with one of that cell's own dendrites. The significance of this finding is discussed.     

Golgi type II interneurons in the neuronal circuit of the monkey lateral geniculate nucleus

Summary Total excision of areas 17-18-19 in the monkey leads to disappearance of relay cells and corticogeniculate axon terminals in the LGN (lateral geniculate nucleus). The few remaining neurons can be safely considered as Golgi type II cells. Electron microscopic examination of such material revealed small ovoid neurons and synaptic clusters encapsulated by glia. Within the cluster there were the characteristic axon terminal of retinal origin, and a peculiar light and large profile with features of both axons (small, flattened synaptic vesicles) and dendrites (many microtubules, endoplasmic cisterns and free ribosomes) in varying proportions. These elements were also present within the heavily gliotic general neuropil and, in longitudinal section, showed segments with strongly dendritic features, and others with vesicles either scattered or grouped near synaptic specializations. Similar profiles were also seen in normal LGN. Light microscopic examination of Golgi series from adult normal monkeys revealed two types of interneurons in the LGN, both having extremely thin axons which could not correspond in size to the ambiguous profiles described above. The latter could well match the appendages so frequently shown by the dendrites of one of the interneuron types. These findings suggest that the synapses in the glomeruli of LGN previously defined as axo-axonic may in fact be between optic axon terminals and the dendritic profiles with synaptic vesicles delineated in this study. Thence, the role of the Golgi type II interneuron could be interpreted at least in part as lateral inhibition.This research was supported in part by U.S.P.H.S. Grants MH-02261 and K3-EY-16, 865. The technical assistance of Mr. David Kahn and Miss Rosemary Lang is gratefully acknowledged.     

Evidence that the different classes of relay cells of the cat's lateral geniculate nucleus terminate in different layers of the striate cortex

Summary Small electrophoretic injections of horseradish peroxidase (HRP) were made with recording microelectrodes in different layers of area 17 of the cat. The sizes and locations of labeled relay cells in the lateral geniculate nucleus (LGNd) were then studied. Layer I was found to receive inputs mainly from small LGNd cells (13–21 m). These cells were located in the parvocellular C laminae and the MIN. Layer II and the upper portion of layer III were not found to receive LGNd afferents. Lower layer III was found to receive inputs mainly from small to medium-sized relay cells. These cells were located in the A laminae and the parvocellular C laminae. Layer IVab and the layer III-IV border region were found to receive afferents from predominantly large LGNd neurons (> 20 m). These cells were located in laminae A, A₁; C, and the MIN. Layer IVc was found to receive inputs from mostly small to medium-sized cells (15–23 m). Nearly all of these cells were in the A laminae although some small cells in laminae C were observed following layer IVc injections which involved the layer IV–V border region. Layer V, away from the layer IV–V border region, was not found to receive LGNd afferents. Finally, layer VI was found to receive inputs from both large and small relay cells. These cells were all located in the A laminae.In the light of previous findings, these results suggest that the terminals of W, X, and Y cell axons are segregated within the cat's striate cortex: W cells projecting to layer 1, the deeper portion of layer III and the layer IV–V border region; X cells projecting heavily to layer IVc with a minor projection to layer VI and possibly also to lower layer III; Y cells projecting heavily to layer IVab and the layer III–IV border region with a smaller projection to layer VI.     

Orientation of dendrites in the lateral geniculate nucleus of the monkey

Summary Quantitative analysis of dendritic orientation in rapid Golgi sections of the lateral geniculate nucleus of Old World monkeys was performed with the help of a computer-microscope and a tree-analysing program. The orientation of intermediate and terminal dendritic segments of parvocellular and magnocellular multipolar neurons was measured at different ages in relationship to a reference line defined by the major direction of afferent fibres visualized in Golgi preparations and by silver staining. The direction of fibre bundles crossing the nucleus is approximately perpendicular to the layers near their apex, but more oblique laterally and medially. There is a clear tendency for terminal dendritic segments of both parvocellular and magnocellular neurons to be oriented preferentially along these fibres and fewer are perpendicular to them. The orientation of intermediate segments is much less clear, showing a more random orientation with regard to the fibres. There is no obvious influence of the order of branching or of the age of the animal (between late gestation and maturity) on the orientation of terminal and intermediate dendritic segments. A parallel study (Leuba and Garey 1984) suggests that there is greater plasticity in the terminal part of the dendritic tree, and it is possible that the maturation of afferent fibres causes these terminal segments to orient along them very early during normal development.     

Morphology of neurons in the lateral geniculate nucleus of the monkey

Summary Rapid Golgi preparations of the lateral geniculate nucleus of old- and new-world monkeys were analysed in an attempt to classify the neuronal types. Four main types are described. The commonest, the multipolar neurons, are found in all laminae. Their somata can be large, medium or small and bear dendrites with sparse spines. Some have a radiate dendritic arbor and others have dendrites grouped in tufts. The next most frequent class is of bipolar neurons with two thick dendrites arising from opposite poles of the soma, which is usually large. Otherwise the dendrites are similar to those of multipolar neurons. Relatively rare is a class of medium-sized neurons with beaded dendrites, found here only in magnocellular laminae. There is a fourth class of small neurons distinguished by fine axonlike dendritic processes. They are in all laminae and form two subgroups, one with very long, cylindrical dendrites and few axon-like processes, the other with shorter dendritic arbors and many axon-like processes. In addition, a class of capsular neurons is found in the circumgeniculate capsule between layer 6 and the pregeniculate nucleus. They are large neurons with umbrella-like dendritic arbors sending ramifications into layer 6. The interlaminar zones contain scattered somata of all types except beaded and capsular neurons.The work described in this paper forms part of a study for a doctoral dissertation in the University of Lausanne by K.D. Saini     

Synaptic organization of the dorsal lateral geniculate nucleus in the adult hamster

Summary The synaptic organization of the sector of the dorsal lateral geniculate nucleus has been examined by electron microscopy in normal adult hamsters and in adult hamsters subjected to unilateral eye enucleation or intravitreal injection of horseradish peroxidase.Two types of neuropil are apparent. Islands of complex neuropil partially enclosed by astrocyte processes (synaptic glomeruli) are surrounded by a sea of simpler non-glomerular neuropil. The latter is dominated by small axon terminals with spherical synaptic vesicles and Gray type 1 axodendritic contacts (SR-boutons) and also contains axon terminals with flattened synaptic vesicles (F-boutons). The glomerular neuropil contains (i) exclusively postsynaptic dendrites and dendritic protrusions of presumptive projection cells; (ii) pre- and postsynaptic pleomorphic-vesiclecontaining P-boutons (interpreted as appendages of the dendrites of interneurons); (iii) large axon terminals containing spherical synaptic vesicles and large pale mitochondria (R-boutons) which were experimentally identified as retinal terminals and which are presynaptic to both projection cell dendrites and P-boutons at Gray type 1 contacts; (iv) F-boutons (minority component). F-boutons and P-boutons are presynaptic to both projection cell dendrites and P-boutons and P-boutons are the intermediate elements of various serial synapses including triplet (triadic) synapses. Medium-large terminals with spherical synatpic vesicles and dark mitochondria (RLD-boutons) which were commonly invaginated by dendritic spines of projection cells in small glomerulus-like formations were also identified. The origin of RLD-boutons is unknown but SR-boutons probably derive chiefly from ipsilateral visual cortex and possibly also from superior colliculus, and non-glomerular F-boutons probably originate in the ipsilateral thalamic reticular nucleus.No differences in synaptic organization were found between the part of the nucleus which receives uncrossed retinal input and the part which receives crossed input, nor were differences seen in the size, fine structure or relationships between the terminals of identified crossed and uncrossed retinal axons.     

The proportion and size of GABA-immunoreactive neurons in the magnocellular and parvocellular layers of the lateral geniculate nucleus of the rhesus monkey

Summary Neurons containing GABA-immunoreactivity in LGN of the macaque monkey were analyzed quantitatively in semithin (1 m) sections. The percentage of GABA(+) cells per unit area of the sections was 26% in the magnocellular layers and 19% in the parvocellular layers. However, the percentage of GABA(+) cells in a unit volume of LGN, calculated by a stereological method that takes into account the observed difference in size of labeled and unlabeled somata, was 35% in the magnocellular layers and 25% in the parvocellular layers. GABA(+) somata in the magnocellular layers were significantly larger than those in the parvocellular layers. The possible role of GABAergic cells in inhibitory mechanisms of receptive fields of parvo- and magnocellular neurons are discussed in the light of current knowledge of the physiology and neural circuits of macaque LGN.Supported by grants EY 02877 and HD 03352 from the National Institutes of Health     

Retinal ganglion cells that project to the dorsal lateral geniculate nucleus in the macaque monkey

Horseradish peroxidase was deposited in the optic nerve to retrogradely label and reveal the dendritic form of all classes of ganglion cell, or it was injected into the dorsal lateral geniculate nucleus to reveal only those classes projecting to the thalamus. The results were compared with those of the accompanying paper in which the ganglion cells projecting to the midbrain are selectively revealed. Two major classes of ganglion cells are described, the P alpha and P beta cells. For both classes dendritic field size increases with eccentricity from the fovea and there is no overlap in the two classes at any given eccentricity. Cell body size shows a similar mean difference but with a slight overlap. Both cell bodies and dendritic fields are larger along the temporal horizontal meridian than the nasal horizontal meridian, for P alpha and for P beta cells, but these differences are reduced when naso-temporal differences in ganglion cell density are taken into account, that is, size correlates closely with density. Injections restricted to the parvocellular layers of the lateral geniculate nucleus labelled almost exclusively P beta cells, whereas injections confined to the magnocellular layers labelled almost exclusively P alpha cells. As midbrain injections label no P beta cells and few P alpha cells it can be shown that about 80% of ganglion cells are P beta cells projecting to parvocellular lateral geniculate nucleus, and that about 10% are P alpha cells projecting to magnocellular layers. The coverage factor, that is the number of cells covering each point on the retina, varied from 1.9-2.3 for P beta cells, and from 2-7 for P alpha cells. Comparing the results with those of comparable investigations on cats and rabbits shows a much clearer segregation of the terminal targets of different classes of ganglion cell in monkeys, the greatest difference being the absence in the monkey of a projection to the geniculate from gamma- and epsilon-like cells. Further, axons which branch and innervate both thalamus and midbrain are rare in monkeys but common in other mammals. Comparing the results with those from physiological investigations suggests that the P beta cells correspond to colour-opponent cells, whereas P alpha cells correspond to the achromatic broad-band magnocellular cells.     

GABA-immunoreactive basal forebrain afferents innervate GABA-immunoreactive non-pyramidal cells in the cerebral cortex of the lizard Podarcis hispanica.

The basal forebrain projection to the cerebral cortex was studied in the lizard Podarcis hispanica by anterograde transport of Phaseolus vulgaris leucoagglutinin. After injections of the lectin into the septal-basal forebrain area, Phaseolus vulgaris leucoagglutinin-labelled fibres were mainly detected in the outer plexiform layer of the medial cortex and in the inner plexiform layer of the dorsal and dorsomedial cortices. Ultrathin sections from these areas were obtained and processed for postembedding immunogold staining for GABA. Most of the Phaseolus vulgaris leucoagglutinin-labelled boutons in the dorsal and dorsomedial cortical areas were GABA immunoreactive and all the double-labelled boutons established symmetric synaptic contacts on cell bodies and dendrites that were also found to be GABA immunoreactive in all cases. In contrast, Phaseolus vulgaris leucoagglutinin-labelled varicosities in the outer plexiform layer of the medial cortex made asymmetric synaptic contacts on GABA-immunonegative profiles and they were themselves negative for GABA. In double-labelled sections, GABA-, calbindin D28k- and neuropeptide Y-immunoreactive neurons were found to be innervated by multiple Phaseolus vulgaris leucoagglutinin-labelled varicosities in the dorsal and dorsomedial cortical areas, whereas in the medial cortex Phaseolus vulgaris leucoagglutinin-labelled fibres were not observed in contact with any subpopulation of GABAergic cells. The results demonstrate that in lizards the septal-basal forebrain projection to the cortex has a GABAergic component, which selectively terminates on GABAergic non-pyramidal cells including the neuropeptide Y- and the calbindin D28k-containing subpopulations. This synaptic organization is remarkably similar to that in mammals, and suggests that the mechanisms of control of the cortical activity by the basal forebrain have been highly preserved during phylogeny.     

Synaptic reorganization in the lateral geniculate nucleus of the adult cat following chronic decortication

Summary The corona radiata containing all geniculo-cortical and cortico-geniculate fibers was transected in adult cats. One year after the operation synaptic architecture of laminae A and A₁ of the decorticated LGN was investigated utilizing electron-microscopy and Golgi-EM.It was found that synaptic glomeruli became embedded in heavily gliotic neuropile, which contained the dendrites of surviving relay cells in addition to retinal axons and interneuronal processes. In contrast to the intact LGN, where the relay cell dendrites are exclusively postsynaptic, many morphologically identified relay neuronal dendrites of the decorticated LGN also contained large, round synaptic vesicles associated with distinct presynaptic sites. In 60% of all glomeruli, the large presynaptic dendrites of relay neurons occupied a central position and were postsynaptic to retinal axons and interneuronal dendrites/axons, but were presynaptic to other relay dendrites or interneuronal dendritic profiles. Occasional dendro-dendritic synapses between relay cell processes could be observed in the extraglomerular neuropile. Relay cell presynaptic dendrites formed unequivocal Gray I-type synapses, in accordance with the supposed excitatory character of relay cell output.Since sprouting of extrinsic or intrinsic axons could not be observed after decortication, it is proposed that the partial synaptic reorganization of the LGN was primarily due to the compensatory axonization of relay cell dendrites.It is further suggested that the electrophysiologically demonstrated expansion of retinal receptive fields in the chronically decorticated LGN was accomplished by the formation of dendro-dendritic synapses between relay cells and interneurons.     

Ultrastructure of the ventral lateral geniculate nucleus (LGNv) receiving tectal afferents in the cat.

The ultrastructure of the ventral lateral geniculate nucleus (LGNv) associated with the superior colliculus was investigated. In addition to normal synaptic morphology tectal input was examined following unilateral ablation of the superior colliculus at survival times of 2 to 12 days. Eight cats were used (six experimental, two control). Examination of the ventromedial LGNv revealed a prevalence of Flat-Symmetric (FS) synapses (58.2 +/- 1.9%), relative to the usually more abundant, Round-Asymmetric (RA) contacts (41.8 +/- 1.8%). The functional morphology of terminating tectal fibres (although infrequent) was suggestive of the FS type. Since FS connections usually serve an inhibitory purpose, it is suggested that the tectal LGNv connection has a negative modulation function in the fixation and tracking process.     

The projection from the dorsal lateral geniculate nucleus of the thalamus to extrastriate visual association cortex in the macaque monkey

Both autoradiographic and horseradish peroxidase tracing techniques were used to characterize a projection from the dorsal lateral geniculate (DLG) nucleus of the thalamus to visual association cortex (extrastriate cortex) in the macaque monkey. The results show that medium to large caliber DLG axons end to discontinuous terminal "patches" in layers V and lower IV of extrastriate cortex. There is a topographical organization to these projections which are mainly to area 19 and anterior 18 located on the lateral and medial surfaces of the hemisphere. Apparently there are no DLG projections to any of the cortical subdivision located within the lunate and superior temporal sulci.     

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.     

GABA-immunoreactive neurons in the dorsal lateral geniculate nucleus of the rat: characterisation by combined Golgi-impregnation and immunocytochemistry

Summary Identified neurons in the dorsal lateral geniculate nucleus (dLGN) of the rat were studied using a Golgi/EM procedure in combination with post-embedding GABA immunocytochemistry. The results of this investigation identify clearly the GABA-immunoreactive nature of the two morphologically] distinct neuronal populations found within the rat dLGN — thalamocortical relay cells are GABA-immunonegative whilst the putative interneurons are GABA-immunopositive. This immunocytochemical evidence strongly suggests that interneurons synthesize and use GABA to mediate their local inhibitory synaptic mechanisms within the dLGN of the rat.