We have studied the laminar origins of local long-range connections within rat primary visual cortex (area 17), by using retrograde tracing of nerve cell bodies with fluorescent markers. Injections throughout the thickness of cortex produce distinct laminar labeling patterns which indicate that a substantial number of cells in layers 2/3, 5, and 6 have wide local axon collateral arbors, while the local arbors of layer 4 cells are much narrower. Double labeling experiments which combined area 17 injections with injections into different projection targets of area 17 (opposite area 17, area 18a, and area 18b) show that many cortico-cortically projecting cells make widespread projections within area 17. In contrast, the overwhelming majority of subcortically projecting cells have narrow collateral arbors within area 17. Anterograde tracing of local projections within areas 17 with the lectin Phaseolus vulgaris leucoagglutinin shows an extensive system of horizontally running fibers which terminate in distinct 0.15-0.25 mm wide clusters up to 1.8 mm from the injection site. On horizontal sections the termination pattern resembles a closely spaced lattice. The results indicate that cortico-cortically projecting cells provide for long-range interactions between distant points of the visuotopic map, while subcortically projecting cells mediate information within a cortical column. Interestingly, subcortically projecting cells differ functionally from cortico-cortically projecting cells in that they are not orientation selective (Klein et al., Neurosci. 17:57-78, '86; Mangini and Pearlman, J. Comp. Neurol. 193:203-222, '80; Simmons and Pearlman, J. Neurophysiol. 50:838-848, '83). We therefore suggest that cortico-cortically projecting cells with wide collateral arbors are orientation selective and that clustered long-range projections within area 17 connect columns with similar functional specificity.