A prominent and stereotypical feature of cortical circuitry in the striate cortex is a plexus of long-range horizontal connections, running for 6-8 mm parallel to the cortical surface, which has a clustered distribution. This is seen for both intrinsic cortical connections within a particular cortical area and the convergent and divergent connections running between area 17 and other cortical areas. To determine if these connections are related to the columnar functional architecture of cortex, we combined labeling of the horizontal connections by retrograde transport of rhodamine-filled latex microspheres (beads) and labeling of the orientation columns by 2-deoxyglucose autoradiography. We first mapped the distribution of orientation columns in a small region of area 17 or 18, then made a small injection of beads into the center of an orientation column of defined specificity, and after allowing for retrograde transport, labeled vertical orientation columns with the 2-deoxyglucose technique. The retrogradely labeled cells were confined to regions of orientation specificity similar to that of the injection site, indicating that the horizontal connections run between columns of similar orientation specificity. This relationship was demonstrated for both the intrinsic horizontal and corticocortical connections. The extent of the horizontal connections, which allows single cells to integrate information over larger parts of the visual field than that covered by their receptive fields, and the functional specificity of the connections, suggests possible roles for these connections in visual processing.

Anatomical studies in the visual cortex have shown the presence of long-range horizontal connections with clustered axonal collaterals, suggesting interactions over distances of several millimeters. We used cross-correlation analysis in cat striate cortex to detect interactions between cells over comparable distances. Using one cell as a reference, we recorded from other cells with a second electrode at varying distances and looked for correlated firing between the two recording sites. This technique allowed us to combine a physiological measure of the strength and type of connection between cells with a characterization of their receptive field properties. The observed interactions were excitatory, and extended over horizontal distances of several millimeters. Furthermore, the interactions were between orientation columns of like specificity, resulting in a waxing and waning in the strength of interaction as the electrodes passed through different orientation columns. We studied relationships between strength of correlation and other receptive field properties and found a tendency for facilitatory interactions between cells sharing the same eye preference. A large proportion of our correlations was due to common input. This feature, and the similarity of interactions between cells in the same column with the reference cell, suggest a high degree of interconnectivity between and within the columns. As the distance between the two electrodes increased, the overlap of the receptive fields of the cells participating in the interactions gradually diminished. At the furthest distances recorded, the cell pairs had nonoverlapping receptive fields separated by several degrees. The distribution and range of these interactions corresponded to the clustering and extent of the horizontal connections observed anatomically.

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.

Although cells in layer 4 of cat striate cortex represent the first stage in the cortical processing of visual information, they have considerably more complicated receptive field properties than the afferents to the layer from the lateral geniculate nucleus. In considering how these properties are generated, we have focused on the intrinsic cortical circuitry, and particularly on the projection to layer 4 from layer 6. Layer 6 pyramidal cells were injected with horseradish peroxidase and examined at the light and electron microscopic level. The labeled axon terminals were found to form asymmetric synapses and to show a strong preference for contacting dendritic shafts. Serial reconstruction of dendrites postsynaptic to labeled layer 6 cell axon terminals showed that a large proportion of the postsynaptic dendrites belonged to smooth and sparsely spiny stellate cells, suggesting a selective innervation of these cell types. In contrast, the geniculate projection to layer 4 made synapses primarily with dendritic spines and, as a result, the large majority of terminals ended on spiny cells. Since smooth and sparsely spiny stellate cells are thought to mediate inhibition within the cortex, we suggest that one effect of the layer 6 to layer 4 projection could be to contribute to inhibitory features of the receptive fields of layer 4 cells.

No abstract