Clustered intrinsic connections in cat visual cortex

The intrinsic connections of the cortex have long been known to run vertically, across the cortical layers. In the present study we have found that individual neurons in the cat primary visual cortex can communicate over suprisingly long distances horizontally (up to 4 mm), in directions parallel to the cortical surface. For all of the cells having widespread projections, the collaterals within their axonal fields were distributed in repeating clusters, with an average periodicity of 1 mm. This pattern of extensive clustered projections has been revealed by combining the techniques of intracellular recording and injection of horseradish peroxidase with three-dimensional computer graphic reconstructions. The clustering pattern was most apparent when the cells were rotated to present a view parallel to the cortical surface. The pattern was observed in more than half of the pyramidal and spiny stellate cells in the cortex and was seen in all cortical layers. In our sample, cells made distant connections within their own layer and/or within another layer. The axon of one cell had clusters covering the same area in two layers, and the clusters in the deeper layer were located under those in the upper layer, suggesting a relationship between the clustering phenomenon and columnar cortical architecture. Some pyramidal cells did not project into the white matter, forming intrinsic connections exclusively. Finally, the axonal fields of all our injected cells were asymmetric, extending for greater distances along one cortical axis than along the orthogonal axis. The axons appeared to cover areas of cortex representing a larger part of the visual field than that covered by the excitatory portion of the cell's own receptive field. These connections may be used to generate larger receptive fields or to produce the inhibitory flanks in other cells' receptive fields.     

Development of axonal arbors of layer 4 spiny neurons in cat striate cortex.

Spiny neurons in layer 4 of cat striate cortex are the primary recipients of geniculocortical afferents and provide crucial links to other cortical layers for processing visual information. Using intracellular staining, we examined the development of the local axonal projections of these neurons to determine (1) whether the laminar specificity of their projections emerged specifically or was sculpted from transient exuberant projections and (2) whether the emergence of excitatory connections from layer 4 to layer 2/3 could contribute to the activity-dependent development of clustered horizontal connections of layer 2/3 pyramidal neurons. Differences in the extent of projections to infragranular (layers 5 and 6, which receive sparse projections) versus superficial layers (layers 2/3 and 4, which receive extensive projections) developed specifically from the outset. By postnatal day 15 (P15) projections to infragranular layers matured and were indistinguishable from those in the oldest animal studied (P33). In contrast, projections to superficial layers continued to increase in complexity after P15. Projections within layer 4, which were the most elaborate at all ages studied, reached maturity at about P20, while those to layer 2/3 continued to increase in complexity through P33. No evidence for exuberant projections to any of these cortical layers was observed. At very early postnatal ages (P5) projections to the subplate region were evident. These disappeared by P8-P11, suggesting the presence of transient connections from layer 4 spiny neurons to subplate neurons. Binocular deprivation did not prevent the emergence of projections from layer 4 spiny neurons into layer 2/3 or development of normal laminar differences in projection density. Connections from layer 4 to layer 2/3 emerged after horizontal connections in layer 2/3 were crudely clustered, but in synchrony with the later refinement of clusters. Collaterals from layer 4 cells first crossed into layer 3 at P11, but were extremely short (extending only 50-200 microns beyond the laminar boundary) and uncommon (only 4 of 19 cells). Since by P8 horizontal projections of layer 2/3 pyramidal neurons are already crudely clustered, the emergence of crude clustering is probably independent of layer 4 to layer 2/3 excitatory projections. The proportion of cells projecting to layer 2/3 and the complexity of their arbors both increased in the subsequent weeks, closely matching the timing of both the refinement of crudely clustered horizontal connections and the emergence of visual responsiveness in layer 2/3.(ABSTRACT TRUNCATED AT 400 WORDS)     

Intracortical connectivity of layer VI pyramidal neurons in the somatosensory cortex of normal and barrelless mice

In mice, barrels in layer IV of the somatosensory cortex correspond to the columnar representations of whisker follicles. In barrelless (BRL) mice, barrels are absent, but functionally, a columnar organization persists. Previously we characterized the aberrant geometry of thalamic projection of BRL mice using axonal reconstructions of individual neurons. Here we proceeded with the analysis of the intracortical projections from layer VI pyramidal neurons, to assess their contribution to the columnar organization. From series of tangential sections we reconstructed the axon collaterals of individual layer VI pyramidal neurons in the C2 barrel column that were labelled with biocytin [controls from normal (NOR) strain, 19 cells; BRL strain, nine cells]. Using six morphological parameters in a cluster analysis, we showed that layer VI neurons in NOR mice are distributed into four clusters distinguished by the radial and tangential extent of their intracortical projections. These clusters correlated with the cortical or subcortical projection of the main axon. In BRL mice, neurons were distributed within the same four clusters, but their projections to the granular and supragranular layers were significantly smaller and their tangential projection was less columnar than in NOR mice. However, in both strains the intracortical projections had a preference for the appropriate barrel column (C2), indicating that layer VI pyramidal cells could participate in the functional columnar organization of the barrel cortex. Correlative light and electron microscopy analyses provided morphometric data on the intracortical synaptic boutons and synapses of layer VI pyramidal neurons and revealed that projections to layer IV preferentially target excitatory dendritic spines and shafts.     

Morphological and immunocytochemical observations on the visual callosal projections in the cat

The connections between the left and right 17-18 border regions of the cat's visual cortex were labeled by axonal transport of peroxidase-conjugated wheat-germ agglutinin (WGA-HRP) and examined by light and electron microscopy. The cells of origin of the pathway were further characterized by transport of fluorescent microspheres ("beads") followed by in vitro injection of cells with Lucifer Yellow, and by beads transport followed by immunocytochemistry with antibodies to gamma-aminobutyric acid (GABA). The cells of origin of the callosal pathway were located in the lower part of layer 2/3, the upper part of layer 4, and layer 6. In layers 2/3 and 6, they were pyramidal cells; in layer 4 they were star pyramids or spiny stellate cells. None of them were spinefree or sparsely spinous cells, and none were GABA-positive. The axon terminals of the callosal pathway formed type 1 (asymmetric) synapses, and most of them contacted dendritic spines. Both the cells of origin and the terminals were arranged in patches. The findings suggest that the direct action of the callosal pathway is excitatory. The callosal system appears to represent only a subset of the cell types that have intrinsic horizontal projections within areas 17 or 18.     

Development of visual cortical axons: layer-specific effects of extrinsic influences and activity blockade

During normal cortical development, individual pyramidal neurons form intracortical axonal arbors that are specific for particular cortical layers. Pyramidal neurons within layer 6 are able to develop layer-specific projections in cultured slices of ferret visual cortex, indicating that extrinsic influences, including patterned visual activity, are not required (Dantzker and Callaway [1998] J Neurosci 18:4145-4154). However, when spontaneous activity is blocked in cultures with tetrodotoxin, layer 6 pyramidal neurons fail to preferentially target their axons to layer 4. To determine whether mechanisms that regulate the development of layer 6 pyramidal neuron arbors can be generalized to pyramidal neurons in other layers, we examined the development of layer 5 and layer 2/3 pyramidal neurons in cultured slices of ferret visual cortex prepared on postnatal day 14 or 15. Layer 5 pyramidal neurons developed layer-specific axonal arbors during 5-7 days in vitro. However, unlike layer 6 pyramidal neurons, layer 5 pyramidal neurons formed layer-specific axonal arbors in the presence of tetrodotoxin. In contrast to layer 5 and layer 6 pyramidal neurons, layer 2/3 pyramidal neurons did not form appropriate layer-specific projections during 5-7 days in vitro. Taken together, these data suggest that the development of layer-specific axons is regulated by different mechanisms for neurons in different layers and cannot be categorically classified as either activity-dependent or independent. Instead, the type of pyramidal neuron, the layers targeted, and the type of activity must be considered.     

Anatomical organization of the primary visual cortex (area 17) of the cat. A comparison with area 17 of the macaque monkey.

Golgi and axonal transport techniques have been used to examine the organization of neurons within primary visual cortex, area 17, of the cat. This organization has been compared to that of the primate cortical area 17 as described in previous studies and it is discussed in relationship to the distribution of afferents from the dorsal lateral geniculate nucleus (dLGN). The visual cortex of the cat and monkey show strong similarities in the laminar positions of neurons projecting extrinsically and also in the restriction of spiny stellate neurons to a central lamina (lamina 4) receiving input from the dLGN. However, lamina 4B in the monkey, which contains spiny stellate neurons but does not receive direct input from the dLGN, has no direct counterpart in cat area 17. Axon projections of spiny stellate neurons in the other divisions of lamina 4 differ in cat and monkey: the small, closely packed neurons in the lowermost division of lamina 4 (4B in the cat, 4Cbeta in the monkey) project chiefly within lamina 4 in the cat whereas in the monkey they have a strong projection to lamina 3. In the cat, spiny stellate neurons of lamina 4A project upon lamina 3 whereas in the monkey those in the apparently equivalent zone, 4Calpha, project upon lamina 4B. Most non-spiny stellate neurons examined have precisely organized interlaminar axonal projections which differ from the axon trajectories of neighboring spiny neurons.     

Local connections of excitatory neurons to corticothalamic neurons in the rat barrel cortex

Corticothalamic projection neurons in the cerebral cortex constitute an important component of the thalamocortical reciprocal circuit, an essential input/output organization for cortical information processing. However, the spatial organization of local excitatory connections to corticothalamic neurons is only partially understood. In the present study, we first developed an adenovirus vector expressing somatodendritic membrane-targeted green fluorescent protein. After injection of the adenovirus vector into the ventrobasal thalamic complex, a band of layer (L) 6 corticothalamic neurons in the rat barrel cortex were retrogradely labeled. In addition to their cell bodies, fine dendritic spines of corticothalamic neurons were well visualized without the labeling of their axon collaterals or thalamocortical axons. In cortical slices containing retrogradely labeled L6 corticothalamic neurons, we intracellularly stained single pyramidal/spiny neurons of L2-6. We examined the spatial distribution of contact sites between the local axon collaterals of each pyramidal neuron and the dendrites of corticothalamic neurons. We found that corticothalamic neurons received strong and focused connections from L4 neurons just above them, and that the most numerous nearby and distant sources of local excitatory connections to corticothalamic neurons were corticothalamic neurons themselves and L6 putative corticocortical neurons, respectively. These results suggest that L4 neurons may serve as an important source of local excitatory inputs in shaping the cortical modulation of thalamic activity.     

Presubicular and parasubicular cortical neurons of the rat: Electrophysiological and morphological properties

Intracellular recordings and Neurobiotin-injection were used to examine the electrophysiology and morphology of presubicular and parasubicular cortical neurons in horizontal slices from rat brains. Evoked responses were obtained by stimulation of subicular and entorhinal cortices. Stellate cells were recorded in layers II and V of presubiculum and parasubiculum. Superficial layer cells had spiny dendrites that were found to reach layer I. Deep layer cells had sparsely spiny dendrites or dendrites without spines that did not reach past layer IV. Pyramidal cells were recorded in layers III and V of presubiculum and layers II and V of parasubiculum. Superficial layer cells had spiny dendrites that were found to reach layer I. Deep layer cells had sparsely spiny dendrites or dendrites without spines that could reach layer II. Electrophysiologically, stellate and pyramidal cells were similar to one another, regardless of cell layer, exhibiting repetitive single spiking in response to depolarizing current injection. No cells were found to burst in response to current injection. While there were subtle electrophysiological differences among the cell types, stellate cells were more similar to pyramidal cells from the same or adjacent layers than to other stellate cells from more distant layers. Similarly, pyramidal cells were electrophysiologically more similar to nearby stellate cells than to other distant pyramidal cells. Cells of all layers responded to subicular stimulation with a short latency (<9 ms), excitatory postsynaptic potential. Superficial layer cells responded at short (<9 ms), longer (10–20 ms) and very long latencies (>20 ms) to stimulation of superficial layers of medial entorhinal cortex. Deep layer cells responded at short latencies (<9 ms) to stimulation of deep layers of medial entorhinal cortex. Many cells responded to both subicular and entorhinal inputs. Both pyramidal and stellate cells in the deep layer of pre/parasubiculum could exhibit population bursting behavior in response to stimulation of subiculum or entorhinal cortex. The results define the cellular morphology and basic electrophysiology of presubicular and parasubicular neurons of the rat brain as a step toward understanding the physiology of the retrohippocampal cortices. Hippocampus 7:117–129, 1997. © 1997 Wiley-Liss, Inc.     

Quantification of thalamocortical synapses with spiny stellate neurons in layer IV of mouse somatosensory cortex

The distribution of thalamocortical (TC) and other synapses involving spiny stellate neurons in layer IV of the barrel region of mouse primary somatosensory cortex (SmI) was examined in seven male CD/1 mice. TC axon terminals were labeled by lesion-induced degeneration, which has been shown to label reliably all TC synapses in mouse barrel cortex. Spiny stellate neurons, labeled by Golgi impregnation and gold toning, were identified with the light microscope prior to thin sectioning and electron microscopy. Analysis of eight dendritic segments from seven spiny stellate neurons showed that most of their synapses are with their dendritic spines, rather than with their shafts. Axospinous synapses are primarily of the asymmetrical type, whereas axodendritic synapses are mainly of the symmetrical type. Dendrites of spiny stellate neurons consistently form thalamocortical synapses, most of which involve spine heads rather than spine stalks or dendritic shafts. From 10.4% to 22.9% of all asymmetrical synapses with dendrites of spiny stellate neurons involve TC axon terminals. In general, this is a higher range than the ranges that characterize the TC synaptic connectivity of dendrites belonging to other types of neurons, implying that spiny stellate neurons are perhaps more strongly influenced by TC synaptic input than other types of cortical neurons examined previously. Spines involved in TC synapses were distributed irregularly along each of the stellate cell dendrites; about half of the interspinous intervals between these spines were about 5 microns or less. Modulations of the efficacy of TC synaptic input to dendrites of layer IV spiny stellate neurons are discussed in the light of recently reported computer simulated analyses of axospinous synaptic connections.     

Dendritic morphology of visual callosal neurons in the golden hamster

The visual callosal neurons and the connections between the two cerebral hemispheres in hamsters have been shown to be important for visual functions, but little is known about the detailed morphology of these neurons. In this study, we have used techniques based on retrograde transport of a fluorescent tracer, Granular Blue, and intracellular injection of Lucifer Yellow in fixed brain slices to identify the laminar distribution and dendritic morphology of the visual callosal neurons in the 17/18a border region of the adult golden hamster. The cells giving rise to the callosal projections were morphologically heterogeneous, although they were all spiny neurons. Most were pyramidal cells, but some were stellate cells. They were located in layers II-VI, with cells concentrating in three bands: (1) in the middle three fifths of layer II/III; (2) in layer IV, and (3) in the middle three fifths of layer V. In layer II/III and layer V, the great majority of the cells were pyramidal or star pyramidal neurons. In layer IV, about half were stellate neurons and the rest pyramidal or star pyramidal neurons. In layer VI, they consisted mostly of modified pyramidal cells. The soma areas of the pyramidal and star pyramidal neurons in all the layers ranged from 52 to 335 micron 2 with a mean of 148 micron 2 (n = 92; SD = 64.4). In general, these cells gave rise to 3-5 basal dendrites.(ABSTRACT TRUNCATED AT 250 WORDS)     

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)     

Synaptic connections of intracellularly filled clutch cells: a type of small basket cell in the visual cortex of the cat

Light and electron microscopic quantitative analysis was carried out on a type of neuron intracellularly filled with horseradish peroxidase. Two cells were studied in area 17, one of which was injected intra-axonally, and its soma was not recovered. One cell was studied in area 18. The two somata were on the border of layers IVa/b; they were radially elongated and received synapses from numerous large boutons with round synaptic vesicles. The dendrites were smooth and remained largely in layer IV. The cells can be recognised on the basis of their axonal arbor, which was restricted to layer IV (90-95% of boutons) with minor projections to layers III, V, and VI. Many of the large, bulbous boutons contacted neuronal somata, short collaterals often forming "claw"-like configurations around cells. The name "clutch cell" is suggested to delineate this type of neuron from other aspiny multipolar cells. Computer-assisted reconstruction of the axon showed that in layer IV the axons occupied a rectangular area about 300 X 500 microns, elongated anteroposteriorly in area 17 and mediolaterally in area 18. The distributions of synaptic boutons and postsynaptic cells were patchy within this area. A total of 321 boutons were serially sectioned in area 17. The boutons formed type II synaptic contacts. The postsynaptic targets were somata (20-30%), dendritic shafts (35-50%), spines (30%), and rarely axon initial segments. Most of the postsynaptic somata tested were not immunoreactive for GABA and their fine structural features suggest that they are spiny stellate, star pyramidal, and pyramidal neurons. The characteristics of most of the postsynaptic dendrites and spines also suggest that they belong to these spiny neurons. A few of the postsynaptic dendrites and somata exhibited characteristics of cells with smooth dendrites and these somata were immunoreactive for GABA. It is suggested that clutch cells are inhibitory interneurons exerting their effect mainly on layer IV spiny neurons in an area localised perhaps to a single ocular dominance column. The specific laminar location of the axons of clutch cell also suggests that they may be associated with the afferent terminals of lateral geniculate nucleus cells, and could thus be responsible for generating some of the selective properties of neurons of the first stage of cortical processing.     

Spiny stellates as cells of origin of association fibres from area 17 to area 18 in the cat''s neocortex

Neurons in the cat's area 17 were stained in Golgi-like fashion following injection of horseradish peroxidase into area 18. Such staining allows classification of neurons on the basis of dendritic morphology. The types of neurons found in area 17 are: pyramidal cells in layers 2,3 and 4ab; spiny stellate cells in the lower part of layer 3, and in layer 4ab; and a few pyramidal and spindle cells in layer 5. The axons of the spiny stellate cells are finer than those of pyramidal cells; they give off collatera;s in deeper cortical layers and may bifurcate when entering the white matter. Spiny stellates in area 17 do not project to area 19; after injections are made into area 17, these neurons are found neither in area 18 nor in area 19. The spiny stellate cell with a long axonis thus categorized as a projection neuron which takes part in the pathway from area 17 to ipsilateral and contralateral¹⁰ area 18.     

Glutamate-positive neurons and axon terminals in cat sensory cortex: a correlative light and electron microscopic study

Immunocytochemical methods were used to perform a correlative light and electron microscopic study of neurons and axon terminals immunoreactive to the antiglutamate (Glu) serum of Hepler et al. ('88) in the visual and somatic sensory areas of cats. At the light microscopic level, numerous Glu-positive neurons were found in all layers except layer I of both cortical areas. On the basis of the dendritic staining of Glu-positive cells, two major morphological categories were found: pyramidal cells, which were the most frequent type of immunostained neuron, and multipolar neurons, which were more numerous in layer IV of area 17 than in any other layer. A large number of Glu-positive neurons, however, did not display dendritic labelling and were considered unidentified neurons. Counts of labelled neurons were performed in the striate cortex; approximately 40% were Glu-positive. Numerous lightly stained punctate structures were observed in all cortical layers: the majority of these Glu-positive puncta were in the neuropil. After resectioning the plastic sections for electron microscopy it was observed that: 1) the majority of neurons unidentifiable at light microscopic level were indeed pyramidal neurons except in layer IV of area 17, where many stained cells were probably spiny stellate neurons. Some Glu-positive neurons, however, exhibited clear ultrastructural features of nonspiny nonpyramidal cells; 2) all synaptic contacts made by Glu-positive axon terminals were of the asymmetric type, but not all asymmetric synaptic contacts were labelled. The vast majority of postsynaptic targets of Glu-positive axons were unlabelled dendritic spines and shafts. The present results provide further evidence that Glu (or a closely related compound) is probably the neurotransmitter of numerous excitatory neurons in the neocortex.     

Electrophysiological and morphological correlates in the development of visual cortical circuitry in infant kittens

Geniculate axons in cat visual cortex establish excitatory connections with cortical cells in supragranular and granular layers at birth. They are localized to the granular layer for the first month after birth. Retraction of geniculocortical synapses parallels axonal extension of spiny stellate cells to the supragranular layer and establishment of synapses for intracortical transmission.     

Development of axonal arbors of layer 6 pyramidal neurons in ferret primary visual cortex

We followed the development of axonal arbors of layer 6 pyramidal neurons in ferret striate cortex to determine whether early developing axon collaterals are formed specifically in the correct target layers from the outset or achieve their adult specificity by the elimination of initially exuberant projections. These neurons were chosen for study because they are amongst the first to be generated in the developing ferret's striate cortex, and, in mature animals, these cells have axonal arbors that are highly specific for layer 4 and to a lesser extent layers 2/3 but have few collateral branches in layer 5. The axonal arbors of individual layer 6 pyramidal neurons were reconstructed following labeling in living slices prepared from the striate cortex of ferrets aged 13–35 days postnatal (P13–35). At the earliest ages (P13–15), axonal arbors consisted of a simple axon extending from the base of the cell body into the subplate or white matter and usually forming a few collateral branches but never ascending into layer 5. By P19–20, about one-half of the cells had extended axon collaterals into layer 5 or higher, and these already appeared to branch preferentially in layer 4. All of the cells from older animals had substantial axonal arbors in layers 2–4. By P26–28, there were approximately ten times as many axonal branches in layer 4 as in layer 5. Between P26–28 and P35, there was no significant change in the number of branches in layer 5, but the numbers of both branches and of axon collateral terminations in layer 4 approximately doubled. Thus, the extent of axonal arborization in layer 4 increases dramatically between P13 and P35, and growth is highly specific for correct target layers, with few branches formed in layer 5. © 1996 Wiley-Liss, Inc.     

Local circuit neurons of macaque monkey striate cortex: II. Neurons of laminae 5B and 6

This study investigates the intrinsic organization of axons and dendrites of aspinous, local circuit neurons of the macaque monkey visual striate cortex. These investigations use Golgi Rapid preparations of cortical tissue from monkey aged 3 weeks postnatal to adult. We have earlier (Lund, '87) described local circuit neurons found within laminae 5A and 4C; this present account is of neurons found in the infragranular laminae 5B and 6. Since the majority of such neurons are GABAergic and therefore believed to be inhibitory, their role in laminae 5B and 6, the principal sources of efferent projections to subcortical regions, is of considerable importance. We find laminae 5B and 6 to have in common at least one general class of local circuit neuron-the "basket" neuron. However, a major difference is seen in the axonal projections to the superficial layers made by these and other local circuit neurons in the two laminae; lamina 5B has local circuit neurons with principal rising axon projections to lamina 2/3A, areas whereas lamina 6 has local circuit neurons with principal rising axon projections to divisions of 4C, 4A, and 3B. These local circuit neuron axon projections mimic the different patterns of apical dendritic and recurrent axon projections of pyramidal neurons lying within laminae 5B and 6, which are linked together by both dendritic and axonal arbors of local circuit neurons in their neuropils extending between the two laminae. The border zone between 5B and 6 is a specialized region with its own variety of horizontally oriented local circuit neurons, and it also serves as a special focus for pericellular axon arrays from a particular variety of local circuit neuron lying within lamina 6. These pericellular axon "baskets" surround the somata and initial dendritic segments of the largest pyramidal neurons of layer 6, which are known to project both to cortical area MT (V5) and to the superior colliculus (Fries et al., '85). Many of the local circuit neurons of layer 5B send axon trunks into the white matter, and we therefore, suspect them of providing efferent projections. The axons of lamina 6 local circuit neurons have not been found to make such clear-cut contributions to the white matter.     

Fundamental differences between the thalamocortical recipient layers of the cat auditory and visual cortices.

In visual and somatosensory cortices of several species, spiny stellate cells in layer 4 are the first elements in signal processing where thalamic information is integrated and emergent receptive field properties are generated and sent on to more superficial cortical layers. In vivo and in vitro experiments have provided important information about how the anatomy and physiology of these cells and this layer fit into the functional cortical circuitry. No such data exist for the auditory cortex but are requisite if we are to understand whether ideas about information processing in one sensory cortical area can be generalized to another. Accordingly, we used in vitro slices from which to record and labeled cells in the middle layers of the cat auditory and visual cortices to compare basic anatomical and physiological features of cells recovered in similar layers using the same methods. Our results demonstrate a striking difference in a basic characteristic of two primary sensory cortical areas. In the visual cortex, spiny stellate cells predominate, receive short-latency synaptic inputs, and project to supergranular layers. No such spiny stellate population is encountered in the middle layers of the auditory cortex. Spiny cells that are not stellate or pyramidal are occasionally encountered but, as a group, do not display consistent anatomical or physiological features that might allow them to function as auditory cortical versions of the visual spiny stellates. Rather, pyramidal cells in the lower half of layer 3 and layer 4 appear to have assumed this role.     

Sensory deprivation changes the pattern of synaptic connectivity in rat barrel cortex

We examined whether sensory deprivation during formation of the cortical circuitry influences the pattern of intracortical single-cell connections in rat barrel cortex. Excitatory postsynaptic potentials from layer 5 pyramidal neurons were recorded in vitro using patch-clamp techniques. In order to evoke such postsynaptic potentials presumptive presynaptic neurons were stimulated by photolytically applied glutamate thus generating action potentials. Synaptic connections between the stimulated and the recorded neuron were identified by the occurrence of postsynaptic potentials following photostimulation. Sensory deprivation altered the projections from layer 2/3 neurons to layer 5 pyramidal cells (L2/3-->L5 projections). In slices of non-deprived rats the input probability of L2/3-->L5 projections showed a periodic pattern with more synaptic connections originating from the borders of the barrel columns, and less synaptic connections originating from the centres. After whisker clipping this periodic pattern disappeared completely and the input probability declined monotonically with increasing distance between stimulated and recorded neuron. These results indicate that sensory input is a prerequisite to establish a synaptic projection pattern which is correlated to the columnar organisation of the anatomical barrel structure.     

Interlaminar connections and pyramidal neuron organisation in the visual cortex,area 17, of the Macaque monkey

The patterns of arborisation of apical dendrites of different varieties of pyramidal neurons in area 17 differ and are characteristic for each cell type. They appear to serve as a means of collating within one neuron information derived directly from several different laminae. These different patterns of apical dendrite arborisation provide dendritic links which relate closely to the laminar distribution of axons of the spiny stellate neurons as well as the pyramidal neurons themselves. The axons of spiny stellate neurons lying in laminae IVCβ and IVA (Lund, '73)—Which receive information from parvocellular geniculate layers — project heavily to the lower half of lamina III (IIIB) and to a narrow zone at the top of lamina V (VA); laminae IIIB and VA are in turn linked by a specific variety of pyramidal neuron, with basal dendritic field in lamina VI, whose apical dendrite has marked lateral branching only in laminae VA and IIIB (where it terminates). Pyramidal neurons with basal dendritic field in laminae VA (with vestigial apical dendrite) or in IIIB have recurrent axon projections to lamina IIIA and above (the descending axon projection of lamina IIIB pyramids is principally to lamina VA itself). The pyramidal neurons of laminae IIIA and above have axons which distribute in the same upper laminae as their dendtritic fields and a descending axon projection to lamina VB. Pyramidal neurons with basal dendritic field on lamina VB have an apical dendrite which, if not vestigal, arborises in IIIA or above; their axons in some cases project to the superior colliculus or may be exclusively, or in addition, recurrent, distributing collaterals within laminae VB, VI and in IIIA or above; one variety of pyramidal neuron with basal dentritic field in lamina VI makes a dentritic link with these same regions, its apical dendrite arborising first within lamina VB and then in lamina IIIA and above. Axons of spiny stellate neurons of lamina IVCα (which receives the projection of the magnocellular layers of the lateral geniculate nucleus) as well as distributing widely within lamina IVCα also contribute to laminae IVB and VA; a link is again made by a specific variety of pyramidal neuron, with basal dendtritic field in lamina VI, which shows branching to its apical dendtrite only in laminae VA and as a terminal arborisation in IVCα. Another variety of pyramidal neuron with basal dendtric field in lamina VI has apical dendritic arborisation only in lamina IVB. The pyramidal neurons with basal dendritic field in lamina IVB and apical dendrite arborising in lamina IIIB and above, also contribute axonal collatetrals to lamina IIIA and above; their horizontal axon collaterals, together with the axons of spiny stellate neurons of laminae IVCα and IVB, form the horizontal fiber band of lamina IVB (to which the axons of laminae III and II pyramidal neurons do not contribute. The descending axon projection of the spiny stellate and pyramidal neurons of lamina IVB appears to be principally to lamina VI. The pattern of branching of pyramidal neuron apical dendrites is therefore neither random nor a continuum of one basic pattern; instead it is a series of separate patterns, each spatially distributed in a highly specific and unique fashion relating to the patterns of projection of afferent information through the cortex.