We have used a combination of anatomical and physiological techniques to explore the functional organization of vertical and horizontal connections in tree shrew striate cortex. Our studies of vertical connections reveal a remarkable specificity in the laminar arrangement of the projections from layer IV to layer III that establishes three parallel intracortical pathways. The pathways that emerge from layer IV are not simple continuations of parallel thalamocortical pathways. Layer IV and its connections with layer II/III restructure the inputs from the LGN, combining the activity from ON and OFF channels and from the left and right eye and transmit the products of this synthesis to separate strata within the overlying layers. In addition, studies of two other prominent vertical connection pathways, the projections from layer VI to layer IV and from layer II/III to layer V suggest that the parallel nature of these systems is perpetuated throughout the cortical depth. Our studies of horizontal connections have revealed a systematic relationship between a neuron's orientation preference and the distribution of its axon arbor across the cortical map of visual space. Horizontal connections in layer II/III extend for greater distances and give rise to a greater number of terminals along an axis of the visual field map that corresponds to the neuron's preferred orientation. These findings suggest that the contribution of horizontal inputs to the response properties of layer II/III neurons is likely to be greater in regions of visual space that lie along the axis of preferred orientation (endzones) than along the orthogonal axis (side zones). Topographically aligned horizontal connections may contribute to the orientation preference of layer II/III neurons and could account for the axial specificity of some receptive field surround effects. Together, these results emphasize that specificity in the spatial arrangement of local circuit axon arbors plays an important role in shaping the response properties of neurons in visual cortex.