Functional and structural topography of horizontal inhibitory connections in cat visual cortex.

The functional organization of long-horizontal inhibitory connections was studied in cat visual cortical area 17, using a combination of electrophysiological recording and anatomical tracing in the same tissue. Orientation maps were obtained by recording multiunit activity from layer III at regular intervals (100-300 microns) in a region of approximately 1.3 mm2 of cortex at a depth corresponding to the location of the basket cell axons reconstructed later. Before the physiological mapping, the neuronal tracer biocytin had been iontophoretically injected at one functionally characterized site. On the basis of light microscopic features a total of five biocytin-labelled large basket axons, BC1-BC5, were reconstructed from series of horizontal sections of two cats. The parent somata and dendritic fields of three axons (BC1, BC4 and BC5) could also be reconstructed. The axonal field of basket cell BC1 had an overall lateral spread of 1.8 mm. The axons of basket cells BC4 and BC5 spanned a distance of 3.05 and 2.85 mm, respectively. The distribution pattern of histologically reconstructed recording sites and of five labelled basket cell axons were directly compared in the same sections. The results show that a single large basket cell provides input to regions representing the whole range of orientations, i.e. iso-orientation (+/- 30 degrees), oblique orientation (+/- [30-60] degrees) and cross-orientation (+/- [60-90] degrees) to that at the basket cell's soma. Furthermore, the differential effect mediated by the same large basket cell at sites of different orientation preference was numerically estimated for two basket cells (BC4 and BC5) whose preferred orientations could be determined on the basis of recording sites adjacent to their parent somata. We counted the number of axonal terminals of these basket cells at iso-, oblique- and cross-orientation sites and found no significant difference in the average density of terminals at sites of either orientation preference. The functional topography of large basket cell axons indicates that the same basket cell can mediate iso-, oblique- and cross-orientation inhibition at different sites. Hence, we assume that large basket cells serve a complex physiological role depending on the location of target cells in the orientation map.