Neuronal classes in the isocortex of a monotreme,the Australian echidna (Tachyglossus aculeatus)

We have used Valverde-Golgi and Golgi-Colonnier techniques to analyze cortical neuronal morphology in four regions (frontal cortex, primary motor cortex, primary somatosensory cortex, primary visual cortex) of the isocortex of the echidna (Tachyglossus aculeatus). Eight classes of neurons could be identified--pyramidal, spinous bipolar, aspinous bipolar, spinous bitufted, aspinous bitufted, spinous multipolar, aspinous multipolar and neurogliaform. All except the pyramidal neurons were morphologically similar to neuronal classes seen in eutherian and metatherian isocortex. Pyramidal neurons made up a small proportion of all cortical neurons encountered in our preparations of echidna cortex (34% in visual cortex, 35% in somatosensory cortex, 41% in frontal cortex and 49% in motor cortex) compared to both reported values in eutherian cortex and values we found in rat cortex impregnations prepared in an identical fashion to the echidna material (75% in rat motor and 78% in rat somatosensory cortex). Many pyramidal neurons in the echidna isocortex were atypical (30-42% depending on region) with inverted somata, short or branching apical dendrites and/or few basal dendrites, very different from the usual pyramidal neuron morphology in eutherian cortex. Dendritic spine density on apical and basal dendrites of echidna pyramidal neurons in somatosensory cortex and apical dendrites of motor cortex pyramidal neurons was also lower than that found in the rat. The present findings are consistent with both pyramidal neurons and the many diverse types of non-pyramidal neurons having already emerged as discrete morphological entities very early in mammalian cortical evolution, at the time of divergence of the therian and prototherian lineage.     

A reassessment of the forms of nonpyramidal neurons in area 17 of cat visual cortex

The nonpyramidal neurons in area 17 of cat visual cortex have been examined in Golgi preparations. From their dendritic patterns, neurons are classified as being multipolar, bitufted, or bipolar, and on the basis of the abundance of dendritic spines as spinous, sparsely spinous, or smooth. When neurons are so classified seven different types of nonpyramidal neurons are encountered in layers II through V. Three of the types of multipolar neurons in layers II through V have spherical dendritic trees. The small multipolar cells have smooth dendrites and are the smallest neurons in the cortex. They have short dendrites and dense local axonal plexuses and occur throughout layers II to V The sparsely spinous stellate cells have longer dendrites, are confined to layer II/III, and have local axonal arborizations, whereas the spinous stellate cells are limited to layer IV. A fourth type of multipolar neuron in layers II through V is the basket cell. Such neurons have elongate dendritic trees and either smooth or sparsely spinous dendrites. Depending upon the orientation of the neurons in the sections, their axons appear to form arcades or long, horizontally extended branches, or a mixture of these two axonal patterns. The terminal portions of the axons of these basket cells pass around the cell bodies of adjacent neurons. The two types of bitufted neurons in layers II through V have vertically oriented dendritic trees. One type, the chandelier cell, has smooth dendrites and a characteristic axon forming vertical strings of terminals. The other sparsely spinous bitufted neurons have axons producing vertically oriented plexuses. The remaining type of neuron encountered in layers II through V is a bipolar cell. The bipolar cell has a single major dendritic trunk arising from each pole of the cell body, and each of these gives rise to a very narrow, long, and vertically oriented dendritic tree. The axon usually takes origin from one of the primary dendrites. In layer I are horizontally oriented, bitufted cells with smooth dendrites. The axons of these horizontal cells of layer I arise from one of the primary dendritic trunks and appear to form a plexus confined to layer I. Horizontally oriented neurons are also present in deep layer VI, but the horizontal cells of layer VI are bipolar. The other two neuronal types in layer VI are multipolar cells with sparsely spinous dendrites. The larger of these two types resembles the basket cells in layers II through V, the only important difference between them being that in addition to the long horizontal branches, the axons of the basket cells of layer VI have a long ascending branch which reaches at least as far as layer IV. The other sparsely spinous cells of layer VI are medium sized. Their axons take a descending and oblique course before elaborating a locally distributed plexus. The various types of neurons defined in this study are compared with neurons described by previous authors who have examined the populations of nonpyramidal cells in area 17 of cat visual cortex and in other visual and nonvisual cortical areas of cats, monkeys, and rodents. In some cases it has been possible to postulate the functional roles that particular types of neurons might play within cat visual cortex.     

Form and distribution of neurons in rat cingulate cortex: Areas 32, 24, and 29

The cytoarchitecture of rat cingulate cortex is described. This includes the topographical distribution and layering patterns of Brodmann's areas 25, 32, 24, and 29a, b, c, and d. Area 24 is subdivided into a ventral area 24a and a dorsal area 24b, but an area 23 could not be identified between areas 24 and 29 An analysis of Golgi impregnations in areas 32, 24, and 29 demonstrates that most neuronal types recognized in neocortical areas are also present in cingulate cortex. Besides typical and inverted pyramidal cells, there is a wide variety of nonpyramidal cells, including multipolar, bitufted, and bipolar cells. Small multipolar cells with small somata, a dendritic tree limited to one or two layers, sparse to moderately spinous dendrites and one of two varieties of short axonal trajectories are present in layers I and II of areas 32, 24, and 29d. Medium multipolar cells occur mainly in layers III and V; they have extensive dendritic trees which traverse three or more layers, moderately spinous dendrites, and an axonal plexus which either ascends or descends in the cortex. Large multipolar cells are also frequent in layers III and V; their extensive dendritic trees are essentially spine free and they have axons which form dense terminations, particularly in the layer above the one in which the cell body is located Neurons with elongated somata and a primarily vertical orientation of the dendritic tree are either bitufted or bipolar. Bitufted cells are most frequent in layers II and III of areas 32, 24, and 29d. These cells have dendritic trees which form “hourglass shaped” fields, dendrites which are moderately spinous, and axons which form either extensive horizontal and vertical projections or are “chandelier” in form. Bipolar cells, in contrast, are found in layers II–V; their sparsely spinous dendrites form narrow dendritic trees which are oriented vertically and extend across four or more layers, and their axons have the same vertical orientation as the dendritic tree It is concluded that the form of the axonal arbors of nonpyramidal cells frequently mimics the extent and shape of their dendritic trees. Thus, small multipolar cells with limited, spherical dendritic trees may have axons which arch sharply and emit short, terminal branches. In contrast, medium and large multipolar cells have more extensive dendritic and axonal arbors which traverse two, three, or more layers. Of the fusiform cells, bitufted ones with their “hourglass” dendritic trees have extensive vertical and horizontally oriented axonal branches, while bipolar cells have narrow, vertically oriented dendritic and axonal arbors The granular layers II–IV of area 29c contain the following types of neurons: small and fusiform pyramids, medium-sized pyramids, large stellate cells, and medium multipolar cells. Fusiform pyramids are the only neurons unique to cingulate cortex. They are similar to the variety of pyramidal cells, but have an oval soma and only one basal dendrite which extends from the base of the cell body to arborize in layer IV. Large stellate cells differ from large multipolar cells in that they have densely spinous dendrites and axons which enter the white matter.     

The forms of non-pyramidal neurons in the visual cortex of the rat.

Rapid Golgi preparations from area 17 of young adult rats have been studied to determine the morphology and distribution of non-pyramidal neurons. Such cells were observed in all of the cellular laminae of the cortex, but were particularly prevalent in layers IV and V. Non-pyramidal neurons were categorized according to two features: (1) dendritic projection pattern, and (2) abundance of dendritic spines. Dendritic patterns were classified as multipolar, bitufted, and bipolar, and spine patterns as spinous, sparsely spinous, and spine-free. Spinous dendrites were associated only with multipolar neurons, while sparsely spinous and spine-free dendrites were each associated with cells of all three non-pyramidal dendritic patterns. The most frequently observed non-pyramidal cell types were multipolar cells of the spine-free and sparsely spinous varieties. All of the general cell types encountered have been described in the literature on non-pyramidal neurons, indicating the lack of any unique forms in rat area 17. An analysis of the dendritic projections of individual non-pyramidal neurons through particular cortical laminae made possible an evaluation of common sources of dendrites present in the neuropil of each layer. Non-pyramidal cell axons were impregnated only in small numbers. Spinous multipolar axons invariably exhibited a descending main branch, while the axons of bipolar neurons were distributed in a narrow vertical field. Axonal patterns of remaining cell types, including Golgi type II arborizations, did not appear to correlate consistently with dendritic morphology. Axons of the basket cell type and "horsetail" axons associated with double bouquet cells of Cajal's original type were not impregnated.     

Neurons of the lateral entorhinal cortex of the rhesus monkey: a Golgi, histochemical, and immunocytochemical characterization.

This study identifies the neuronal types of the rhesus monkey lateral entorhinal cortex (LEC) and discusses the importance of these data in the context of the connectional patterns of the LEC and the possible role of these cells in neurodegenerative diseases. These neuronal types were characterized with the aid of Golgi impregnation techniques. These characterizations were based upon their spine densities, dendritic arrays, and, where possible, axonal arborizations. The cells could be segregated into only spinous and sparsely spinous types. The most numerous spinous types were pyramidal neurons. Other spinous types included multipolar, vertical bipolar and bitufted, and vertical tripolar neurons. The sparsely spinous neuronal types consisted of multipolar, horizontal bipolar and bitufted, and neurogliaform cells. These cells were further classified with the aid of histochemical stains and immunocytochemical markers. Nicotinamide adenine dinucleotide phosphate-diaphorase (NADPH-d) histochemistry stained multipolar, bipolar, and bitufted neurons. Stain for cytochrome oxidase (CO) was found in pyramidal and nonpyramidal cell types. Immunocytochemical techniques revealed several nonpyramidal neurons that contain somatostatin (Som) or substance P (SP). This study complements previous analyses of the neuronal components described in the LEC and adds further information about the distribution of selected neurochemicals within this cortex.     

Structure of the piriform cortex of the opossum. I. Description of neuron types with golgi methods

The piriform cortex was studied in the adult opossum with rapid Golgi and Golgi-Cox techniques. Most pyramidal cells in the deep part of layer II and layer III resemble those in other parts of the cerebral cortex by virtue of a single apical dendritic trunk, multiple basal dendrites, a large number of small to medium dendritic spines, and a deeply directed axon. Pyramidal cells in the superficial part of layer II are similar with the exception that “secondary” apical dendrites often emerge directly from the cell body rather than from a single primary trunk. With conservative criteria for categorization, nine different types of nonpyramidal cells were distinguished, four of which have not been previously described. Layer I contains a small number of neurons with both smooth and spiny dendrites including distinctive fusiform cells with large somatic appendages. As in other species, the most common type of nonpyramidal neuron in layer II is the semilunar cell which has only apically directed dendrites. These cells have distinctive large spines confined to their distal dendritic segments. The mid to deep portion of layer III contains multipolar neurons with smooth dendrites that resemble the well-known large stellate cells in neocortex. In addition, layer III contains three non-pyramidal neuron types with spiny dendrites: (1) fusiform and multipolar cells with complex, branched dendritic appendages and somatic spines, (2) very large multipolar cells (up to 35 μm mean diameter) with large-diameter dendrites that give rise to abruptly tapering side branches and filiform spines, and (3) multipolar cells with profusely spiny dendrites. In all three layers, small neurons have been found with spherical cell bodies and “axoniform” dendrites that resemble the so called neurogliaform neurons described in a variety of brain areas. A striking feature of the organization of the piriform cortex is that, with the exception of the neurogliaform neurons, the different types of nonpyramidal cells tend to be segregated in individual layers or sublayers. Physiological implications of the results are discussed. Remarks are also made concerning the potential of the piriform cortex as a model cortical system.     

Morphology of Golgi-Cox-impregnated barrel neurons in rat SmI cortex

Golgi-Cox-impregnated neurons in the barrel cortex of the rat were studied qualitatively and quantitatively. Adult rat brains were sectioned perpendicular to or parallel to the cortical representation of the large facial vibrissae at 125 micron. Cortical laminar and barrel boundaries were identified from the Nissl counterstain. Over 200 well-impregnated neurons in cortical layers I-IV were selected for classification and further detailed study. Three broad classes of neurons were recognized: (1) pyramidal cells with conical somata, a stout apical dendrite, and spines; (2) class I nonpyramidal cells having small spherical somata and spiny dendrites; and (3) class II nonpyramidal cells having larger ellipsoid somata and smooth or beaded dendrites. The class I cells were further subdivided into "star pyramids" (cells with an apical dendrite) and spiny stellate cells (cells in which all dendrites were of similar length). The class II cells also were subdivided into multiform cells (with multiple dendrites radiating from the soma) and bipolar cells (with two principal dendritic trunks arising from the superficial and deep aspects of the soma). The position of these various cell types in the superficial cortical laminae was mapped in sections normal to the pia. Numerous examples of the class I and class II neurons were drawn with respect to the barrels in layer IV and the extent of their processes noted. Finally, approximately 250 barrel-related class I and II neurons were studied quantitatively using a computer-microscope and digitizing tablet. The density of the Golgi-impregnated neurons corresponds to the pattern of cell density seen with the Nissl counterstain. The various cell types are not uniformly distributed as a function of cortical depth. Cells with apical dendrites were found principally in the supragranular layers and star pyramids in the superficial one-half of layer IV. Spiny stellate cells are concentrated in layer IV and the smooth cells are present in greatest number in deep layer III and deeper layer IV. On the basis of these distributions we suggest that layer IV be subdivided into two sublaminae. The class I and class II neurons can be distinguished according to quantitative criteria which apply in either plane of section used. Class I neurons have smaller projected somal areas, more proximal dendritic branching, and shorter dendrites when class I and II neurons are measured in three dimensions.(ABSTRACT TRUNCATED AT 400 WORDS)     

Maturation of rat visual cortex. III. Postnatal morphogenesis and synaptogenesis of local circuit neurons

The postnatal development of 3 types of local circuit neurons in rat visual cortex was examined in Golgi and electron microscopic preparations. During the first postnatal week, smooth and sparsely spinous stellate, bitufted and bipolar neurons were identified in Golgi material by their characteristic dendritic arborizations. Morphological differentiation begins during this week, as each neuron sprouts dendrites which extend, branch and produce spines, and ends by day 21. This differentiation was traced by quantifying the somatic area and number of primary dendrites on stellate, bitufted and bipolar neurons in layer II/III or layer V. Neurons in deep cortex differentiate earlier than those in superficial laminae. On day 3, axons are evident as short, straight processes, however, by day 6, many axons have branches and varicosities. The increase in the complexity of the axonal trees continues during the second and third postnatal weeks. Since the axons of stellate and bitufted neurons form synapses with the somata of pyramidal neurons, an index of the synaptogenesis of these neurons was traced by counting the numbers of synapses on the somata of pyramidal neurons. The mean number of axosomatic synapses increases steadily from day 3 to day 30. Layer V pyramidal neurons form axosomatic synapses before pyramidal neurons in layer II/III. In conclusion, the morphology of local circuit neurons develops during the period after they migrate into cortex. The principle that cortical local circuit neurons develop after projection neurons only applies for the synaptogenesis of the axon, but not for the maturation of the cell body and dendrites.     

Structure of layer II in cat primary auditory cortex (AI)

The cytoarchitecture, myeloarchitecture, neuronal architecture, and intrinsic and laminar organization of layer II were studied in the primary auditory cortex (AI) of adult cats. The chief goal was to describe the different types of cells and axons to provide a framework for experimental studies of corticocortical connections or of neurons accumulating putative neurotransmitters. A further goal was to differentiate layer II from layer III. Layer II extends from 150-200 micron to about 400 micron beneath the pia and has two subparts. The superficial stratum, layer IIa, has many small, chiefly non-pyramidal neurons, primarily with round or oval perikarya, and a sparse, fine, and irregularly arranged axonal plexus. Layer IIb somata are larger and more densely packed and there is a more developed vertical and lateral axonal plexus. The border with layer III was marked by numerous large pyramidal cells with a thicker apical dendrite with more developed basal dendritic arbors than those of layer II pyramidal cells. Eight varieties of neurons were recognized in Golgi-impregnated material. These included small and medium-sized pyramidal cells, whose apical dendrites often ramified in layer I; bipolar and bitufted cells with polarized, sparse dendritic arbors; small smooth or sparsely spinous multipolar cells with radiating dendrites and small dendritic fields; spinous multipolar cells, whose large dendritic fields had more extensive apical than basal arbors; large sparsely spinous multipolar cells with smooth, robust apical dendrites; tufted multipolar cells with highly developed apical dendrites and some dendritic appendages; and extraverted multipolar cells with a broad, candelabra-shaped dendritic configuration, and with most dendrites oriented at right angles to the pia. The axons of the different cell types had the following general dispositions: those arising from the pyramidal cells could often be traced into the white matter but had many local branches as well; those of the other neurons had more or less extensive local axonal collateral systems and fewer branches which appeared to be corticofugal. However, the complete trajectory of the axons was not always impregnated in the adult material.(ABSTRACT TRUNCATED AT 400 WORDS)     

Nonpyramidal neurons in the primate basolateral amygdala: A Golgi study in the baboon (Papio cynocephalus) and long-tailed macaque (Macaca fascicularis)

Nonpyramidal GABAergic interneurons in the basolateral nuclear complex (BNC) of the amygdala are critical for the regulation of emotion. Remarkably, there have been no Golgi studies of these neurons in nonhuman primates. Therefore, in the present study we investigated the morphology of nonpyramidal neurons (NPNs) in the BNC of the baboon and monkey using the Golgi technique. NPNs were scattered throughout all nuclei of the BNC and had aspiny or spine-sparse dendrites. NPNs were morphologically heterogeneous and could be divided into small, medium, large, and giant types based on the size of their somata. NPNs could be further divided on the basis of their somatodendritic morphology into four types: multipolar, bitufted, bipolar, and irregular. NPN axons, when stained, formed dense local arborizations that overlapped their dendritic fields to varying extents. These axons always exhibited varying numbers of varicosities representing axon terminals. Three specialized NPN subtypes were recognized because of their unique anatomical features: axo-axonic cells, neurogliaform cells, and giant cells. The axons of axo-axonic cells formed “axonal cartridges,” with clustered varicosities that contacted the axon initial segments of pyramidal neurons (PNs). Neurogliaform cells had small somata and numerous short dendrites that formed a dense dendritic arborization; they also exhibited a very dense axonal arborization that overlapped the dendritic field. Giant cells had very large irregular somata and long, thick dendrites; their distal dendrites often branched extensively and had long appendages. In general, the NPNs of the baboon and monkey BNC, including the specialized subtypes, were similar to those of rodents.     

The non-pyramidal cells in layer III of cat primary auditory cortex (AI)

The form and location of non-pyramidal neurons in layer III of the primary auditory cortex (AI) of adult cats is described in Golgi, Nissl, and other material. The cells were compared to the profiles of retrogradely labeled, commissurally interconnected cells. A principal finding is that certain non-pyramidal and pyramidal cells project interhemispherically to AI; a second conclusion is that the retrogradely labeled commissural cells form small clusters or narrow strips separated by unlabeled patches even after massive injections in the opposite AI. The non-pyramidal cells of origin have not yet been conclusively identified, but they must include one (or more) of the following six types of cells observed in Golgi-impregnated material: tufted or bitufted cells with a radially elongated dendritic arbor; sparsely spinous stellate neurons with thin, smooth dendrites and vertically disposed axonal branches; small stellate cells with varicose dendrites, a restricted dendritic field, and a profusely branched local axon; bipolar neurons with long, thin dendrites; medium-sized multipolar cells with radiating, sparsely branched dendrites; and small stellate neurons with smooth dendrites and a tiny dendritic field. These non-pyramidal cells are found throughout layer III but are more numerous in the upper part, layer IIIa, where they mingle with the small pyramidal neurons. As a rule the axonal branches of non-pyramidal cells are more numerous than those arising from layer III pyramidal neurons, and although they have many axonal collaterals, most project locally and vertically in narrow radial strips. In contrast, pyramidal cell axons have ascending and descending components which invade large, lateral territories in many cortical layers. Layer III non-pyramidal neurons are similar to those in layer IV in certain respects, although their dendritic fields are more spherical and less tufted than those of layer IV cells, and their axons have more local, limited targets. These axons appear to contribute but little to the conspicuous, lateral fiber striae in layer III. The primary intrinsic targets of non-pyramidal cell axons appear to be the apical dendrites of medium-sized and large layer III pyramidal cells, and recurrent branches to the parent cell; their fine, distal branches fortify the vertical plexus in layer III, and certain axons may descend into layer IV. Since layer III in AI receives both commissural and thalamic input, it is possible that these parallel, afferent channels are to some degree segregated, and to some degree convergent, onto particular types of cells.(ABSTRACT TRUNCATED AT 400 WORDS)     

Classes of neurons in relation to the laminar organization of the lateral geniculate nucleus in the tree shrew, Tupaia belangeri

We used the rapid Golgi and horseradish peroxidase (HRP) techniques to study the dendritic spread of relay neurons in functionally distinct laminae of the tree shrew dorsal lateral geniculate nucleus (LGNd). On the basis of their dendritic spread in relation to laminar and interlaminar zones, we describe three classes of relay neurons. Unilaminar neurons with multipolar radiate, bitufted, and intermediate types of dendrites. Dendrites of these neurons are confined to one lamina only, but also can have some of their segments in adjacent interlaminar zones. Multilaminar neurons with multipolar radiate, bitufted, and intermediate types of dendrites. Independent of the site of their cell bodies in a laminar or interlaminar zone, these neurons spread their dendrites over two or more laminae. Interlaminar neurons whose cell bodies and dendrites are confined to a single interlaminar zone. Unilaminar neurons are found in all the laminae. In the medial three laminae, they are more of the radiate type, whereas in laminae 4 and 5 their dendrites tend to be more of a tufted nature. Lamina 6 shows a preponderance of the elongated bitufted type. Multilaminar neurons, although less common as compared to the unilaminar, are also observed in all the laminae. Some neurons have their dendrites confined to an interlaminar zone. By retrograde transport of HRP injected into the visual cortex, we have shown that these neurons are, in fact, relay neurons. In addition to relay neurons, there are small interneurons with "axoniform" dendrites and an unmyelinated axon whose arborization is confined within the limits of the neuron's dendritic spread. Neurons of this type are not labeled with HRP injected into the visual cortex. We conclude that although each lamina is functionally specialized by input from ipsilateral or contralateral retina and by segregation of neurons responding to on or off stimuli, some multilaminar neurons can be found in each lamina. Thus, laminar as well as interlaminar zones contain a class of neurons that could provide a cross-talk between the functionally specialized laminae. Most relay neurons in all the laminae, however, confine their dendrites to their home lamina. Thus, the dendritic architecture of relay neurons allows for processing of information both within channels and between channels.     

Inverted Pyramidal Neurons and Interneurons in Cat Cortical Subplate Zone are Labelled by Monoclonal Antibody SP1

During development, the subplate zone of the cat neocortex contains neuronal populations with distinct morphological and neurochemical phenotypes. A subset of those are specifically recognized by a mouse monoclonal antibody termed SUBPLATE-1 (SP1), which was generated against tissue homogenates of kitten cortical white matter. SP1 stains cell bodies and proximal dendrites, but rarely distal dendrites, axonal arbors or spines. In order to characterize morphologically the SP1 imunoreactive subplate cell types, we combined SP1 immunohistochemistry with intracellular iontophoretic injections of Lucifer yellow. The majority of double-labelled neurons were inverted pyramids with a single thicker spine-covered dendrite that descended into the white matter and a tuft of thinner spinous dendrites that ascended from the upper somatic pole, but generally remained confined to the white matter. Other double-labelled neurons were multipolar to bitufted, although often equipped with one thicker descending dendrite. In inverted pyramidal cells, the axons originated from the descending dendrite or, more rarely, from the lower portion of the soma, and descended into the white matter. They formed collaterals recurring toward the grey matter. The presence of dendritic spines on double-labelled pyramidal cells and the axonal arborization patterns were two novel features not revealed previously by SP1 immunohistochemistry alone. The inverted pyramidal morphology was typical for double-labelled neurons located in the subplate szone below the apices of the gyri, whereas those located below the flanks or sulci or deep in the white matter soften displayed a bitufted or multipolar spinous morphology. A minority of the double-labelled neurons were multipolar with smooth dendrites and locally branching axons. These results suggest that in the cat subplate zone, a majority of the cells expressing the SP1 antigen are spinous, and we termed the spinous subplate cells ‘subplate pyramidal neurons’.     

Dementia of frontal lobe type and motor neuron disease. A Golgi study of the frontal cortex.

Neuropathological findings in a 38 year old patient with dementia of frontal lobe type and motor neuron disease included pyramidal tracts, myelin pallor and neuron loss, gliosis and chromatolysis in the hypoglossal nucleus, together with frontal atrophy, neuron loss, gliosis and spongiosis in the upper cortical layers of the frontal (and temporal) lobes. Most remaining pyramidal and non-pyramidal neurons (multipolar, bitufted and bipolar cells) in the upper layers (layers II and III) of the frontal cortex (area B) had reduced dendritic arbors, proximal dendritic varicosities and amputation of dendrites as revealed in optimally stained rapid Golgi sections. Pyramidal cells in these layers also showed depletion of dendritic spines. Neurons in the inner layers were preserved. Loss of receptive surfaces in neurons of the upper cortical layers in the frontal cortex are indicative of neuronal disconnection, and are "hidden" contributory morphological substrates for the development of dementia.     

Topographic projection from the optic tectum to the auditory space map in the inferior colliculus of the barn owl

In the barn owl (Tyto alba), the external nucleus of the inferior colliculus (ICX) contains a map of auditory space that is calibrated by visual experience. The source of the visually based instructive signal to the ICX is unknown. Injections of biotinylated dextran amine and Fluoro-Gold in the ICX retrogradely labelled neurons in layers 8-15 of the ipsilateral optic tectum (OT) that could carry this instructive signal. This projection was point-to-point and in register with the feed-forward, auditory projection from the ICX to the OT. Most labelled neurons were in layers 10-11, and most were bipolar. Tripolar, multipolar, and unipolar neurons were also observed. Multipolar neurons had dendrites that were oriented parallel to the tectal laminae. In contrast, most labelled bipolar and tripolar neurons had dendrites oriented perpendicular to the tectal laminae, extending superficially into the retino-recipient laminae and deep into the auditory recipient laminae. Therefore, these neurons were positioned to receive both visual and auditory information from particular locations in space. Biocytin injected into the superficial layers of the OT labelled bouton-laden axons in the ICX. These axons were generally finer than, but had similar bouton densities as, feed-forward auditory fibers in the ICX, labelled by injections of biocytin into the central nucleus of the inferior colliculus (ICC). These data demonstrate a point-to-point projection from the OT to the ICX that could provide a spatial template for calibrating the auditory space map in the ICX.     

Tectoreticular pathways in the turtle, Pseudemys scripta. II. Morphology of tectoreticular cells

The morphology of tectoreticular neurons in turtles was examined with serial section reconstructions of neurons retrogradely filled with HRP. Six classes of tectal neurons project into the three tectobulbar pathways characterized in the preceding paper (Sereno, '85). (1) Large multipolar neurons with somata in the central gray layers, and with moderately branched dendrites sometimes spanning over a millimeter, project into the dorsal tectobulbar pathway, TBd. Their dendrites are covered with fine spicules and tend to arborize in the lower third of the superficial gray layers. (2) Medium-sized neurons with multiple radial dendrites and somata in the central white and upper periventricular layers probably project into the ipsilateral intermediate tectobulbar pathway, TBi. Their dendrites also bear fine spicules and usually reach the tectal surface. (3) Small radial cells in the periventricular layers, and (4) small bitufted radial cells in the superficial gray project into the small caliber component of the ipsilateral ventral tectobulbar pathway, TBv(sm). (5) Medium-sized central gray neurons with stratified dendrites, and (6) medium-sized central gray neurons with horizontal dendrites probably project into the medium caliber component of the ventral tectobulbar pathway, TBv(med). In contrast to TBd and TBi neurons, these last four classes emit a spray of long, filamentous dendritic appendages in the central gray and have dendritic arbors near the top of the superficial gray. The morphology of the neurons described in this and the preceding paper is briefly discussed in light of current ideas about tectally mediated sensorimotor transformations.     

Laminar distribution and morphology of gamma-aminobutyric acid (GABA)-immunoreactive neurons in the medial and dorsomedial areas of the cerebral cortex of the lizard Podarcis hispanica

The morphology and laminar distribution of immunolabeled neurons in the medial and dorsomedial telencephalic cortices of the lizard Podarcis hispanica were examined in vibratome sections after preembedding gamma-aminobutyric acid (GABA)-immunocytochemistry. In both cortical areas and at all rostrocaudal levels, GABA-immunoreactive neurons were found in all cortical layers, with the largest number (74%) of GABA-positive cells in layer 3. GABA-positive neurons were classified into pyramidlike, vertical-fusiform, multipolar, and horizontal neurons. Cells that could be so classified were counted in each cortical lamina. In the medial cortex, multipolar and horizontal-bipolar cells dominated layer 1. Layer 2 displayed mainly horizontal and pyramidlike cells at its outer margin and pyramidlike cells at its inner margin. In layer 3, horizontal cells were the prevalent group. In the dorsomedial cortex, layer 1 mainly contained small multipolar neurons (35% of layer-1 cells) in its outer third and vertical-fusiform neurons (37% of layer-1 cells) in its inner two thirds. In layer 2, 47% of the few GABA-positive perikarya were pyramidlike. The largest population of neurons in layer 3 was that formed by multipolar cells (45% of layer-3 cells). Ultrastructural examination revealed that GABA-immunoreactive neurons possessed indented euchromatic nuclei with a central nucleolus. Their cytoplasm contained numerous mitochondria and a very well-developed granular endoplasmic reticulum. Their somata were contacted by numerous unstained boutons making asymmetric contacts and by a few symmetric synapses of GABA-positive terminals. Dendrites of GABA-immunoreactive cells were thin, with irregular outlines, and generally aspinous. Like the somata, dendrites were contacted by many unstained asymmetric synapses. Some dendritic profiles also received symmetric contacts from GABA-positive boutons. GABA-positive terminal-like puncta were found throughout the layers, with a maximal concentration in layer 2. Electron microscopy confirmed that nearly all of the puncta represent GABA-positive terminal boutons. Comparison of GABA-immunoreactive cells in Podarcis with those found in the mammalian hippocampus suggests that these cells may be inhibitory neurons, as in the hippocampus of mammals.     

Axonal patterns and topography of short-axon neurons in visual areas 17, 18, and 19 of the cat

In a Golgi study of short-axon cells in areas 17, 18, and 19 of the adult cat, 21 main axonal arborization patterns are distinguished and related to laminar position and dendritic morphology. Multipolar neurons exclusive to layer 2/3 exhibit the greatest diversity of axons: These may be arranged in a local tuft, a single descending stem with recurrent collaterals, a columnar descending plexus, horsetaillike bundles, a dense intralaminar plexus, or a varicose local arbor. Multipolar cells of layers 2--5 may have local basket or chandelier axons or a neurogliform axonal plexus, and axons in layer 4 may branch into a columnar basket plexus. Two types of multipolar cells are described in layers 5 and 6. Also, neurons with a bitufted dendritic tree have different axonal patterns: cone-shaped axons, arcade axons, profuse ascending plexuses, and columnar or diffuse ascending and descending arbors. The axons of bitufted cells in layer 6 ascend or form a local tuft. Finally, giant bitufted cells with local axons, bitufted or multipolar cells with horizontal axons, and bipolar cells are described. The neuronal types established on the basis of their axonal arbor are compared to previous classifications of cortical neurons. The location of neurons thus classified has been recorded and evaluated. Most cells show no topographical specificity and occur indistinctly in the three visual areas, while two types are exclusive to area 17. Horsetail neurons accumulate at the 17/18 and 18/19 borders. Multipolar cells of layer 2/3 with a dense intralaminar plexus and chandelier cells are concentrated in the region where the central visual field is represented.     

Calretinin-immunoreactive local circuit neurons in area 17 of the cynomolgus monkey,Macaca fascicularis

The connections of local circuit neurons immunoreactive for calcium-binding protein calretinin (CR-ir) were studied in area 17 of the macaque monkey visual cortex. Most CR-ir neurons were located in layers 2 and 3A. They were polymorphic and included bitufted, multipolar, pyramid-shaped neurons with smooth dendrites and Cajal-Retzius cells. The majority of CR-ir neurons were γ-aminobutyric acid (GABA)-immunopositive (approximately 90%), and comprised about 14% of the total GABAergic neuron population. The axons of CR-ir cells had local arbors within layers 1–3, but the major trunks descended to deep layers 5 and 6 where they formed dense terminal fields within narrow columns (100–150 μm). This specific innervation of layers 5 and 6 appeared as a distinct feature of area 17 as it was not seen in the adjacent area 18. CR-ir boutons (n = 168) were GABA-ir (95%) and formed symmetric synapses. In layers 1–3, the majority of postsynaptic targets (n = 64) were GABAergic local circuit neurons [postsynaptic target distribution: GABA-positive dendrites (67%) and somata (14%), and GABA-negative dendrites (13%) and spines (6%)]. In deep layers, the most synapses (80%; n = 187) were formed with pyramidal cells where they provided a basket-type innervation [postsynaptic target distribution: GABA-positive dendrites (19%) and somata (1%), and GABA-negative dendrites (50%), spines (20%) and somata (10%)]. Unlike other GABAergic neurons, which innervate mainly pyramidal neurons, the CR-ir subpopulation only has pyramids as a preferred target in the deep layers (layers 5 and 6); however, in the superficial layers of the area 17, they selectively form synapses mainly with other GABAergic cells. Thus, the CR-ir neurons appear to have a dual function of disinhibiting superficial layer neurons and inhibiting pyramidal output neurons in the deep layers. J. Comp. Neurol. 379:113-132, 1997. © 1997 Wiley-Liss, Inc.     

Kainate-activated cobalt uptake in the primary gustatory nucleus in goldfish: visualization of the morphology and distribution of cells expressing AMPA/kainate receptors in the vagal lobe

Gustatory afferent fibers of the vagus nerve that innervate taste buds of the oropharynx of the goldfish, Carassius auratus, project to the vagal lobe, which is a laminated gustatory nucleus in the dorsal medulla. As in the mammalian gustatory system, responses by second-order cells in the goldfish medulla are mediated by N-methyl-D-aspartate (NMDA) and non-NMDA ionotropic glutamate receptors. We utilized a cobalt uptake technique to label vagal lobe neurons that possess cobalt-permeable ionotropic glutamate receptors. Vagal lobe slices were bathed in kainate (40 microM) or glutamate (0.5 or 1 mM) in the presence of CoCl(2), which can pass into cells through the ligand-gated cation channels of non-NMDA receptors made up of certain subunit combinations. Cobalt-filled cells and dendrites were observed in slices that were activated by kainate or glutamate, but not in control slices that were bathed in CoCl(2) alone, nor in slices that were bathed with the non-NMDA receptor antagonist 6,7-dinitroquinoxaline-2,3-dione (10 microM) in addition to an agonist. Likewise, simple depolarization of the cells with KCl failed to induce cobalt loading. Cobalt-filled round unipolar cells, elongate or globular bipolar cells, and multipolar cells with elongate or polygonal perikarya were distributed throughout the cell layers in the sensory zone of the vagal lobe. Numerous labeled neurons had dendrites spanning layers IV and VI, the two principal layers of primary afferent input. Apical and basal dendrites often extended radially through neighboring laminae, but many cells also extended dendrites tangential to the lamination of the sensory zone. In the motor layer, cell bodies and proximal dendrites of small, multipolar neurons, and large motoneurons were regularly loaded with cobalt.