Orientation topography of layer 4 lateral networks revealed by optical imaging in cat visual cortex (area 18)

The functional specificity of corticocortical connections with respect to the topography of orientation selectivity was studied by optical imaging of intrinsic signals and bulk injections of fluorescent latex beads (green and red) and biocytin into layer 4. The distributions of retrogradely labelled cells and anterogradely labelled axon terminals were histologically reconstructed from all cortical laminae, and the resulting anatomical maps compared with the optically imaged functional maps. Layer 4 injections produced extensive horizontal labelling up to 2-3 mm from the injection centres albeit without the clear patchy pattern described after layer 2/3 injections (Gilbert & Wiesel 1989, J. Neurosci., 9, 2432-2442; Kisvarday et al. 1997, Cerebral Cortex, 7, 605-618). The functional (orientation) distribution of the labelled projections was analysed according to laminar location and lateral spread. With regard to the former, no major difference in the orientation topography between supragranular- (upper tier), granular- (middle tier) and infragranular (lower tier) layers was seen. Laterally, proximal and distal projections were distinguished and further dissected into three orientation categories, iso- (+/- 30 degrees), oblique- (+/- 30-60 degrees) and cross-orientations (+/- 60-90 degrees) with respect to the orientation preference at the injection sites. The majority of distal connections (retrograde and anterograde) was equally distributed across orientations (35.4% iso-, 33.7% oblique-, and 30.9% cross-orientations) that are equivalent with a preponderance to dissimilar orientations (oblique- and cross-orientations, 64.6%). In one case, distal excitatory and inhibitory connections could be morphologically distinguished. For both categories, a marked bias to dissimilar orientations was found (excitatory, 63.7%; inhibitory, 86.6%). Taken together, these results suggest that the long-range layer 4 circuitry has a different functional role from that of the iso-orientation biased (52.9%, Kisvarday et al. 1997, Cerebral Cortex, 7, 605-618) layer 2/3 circuitry, and is perhaps involved in feature difference-based mechanisms, e.g. figure ground segregation.