Sharing Receptive Fields with Your Neighbors: Tuning the Vertical System Cells to Wide Field Motion

In the blowfly, the direction-selective response of the 60 lobula-plate tangential cells has been ascribed to the integration of local motion information across their extensive dendritic trees. Because the lobula plate is organized retinotopically, the receptive fields of the tangential cells ought to be determined by their dendritic architecture. However, this appears not always to be the case. One compelling example is the exceptionally wide receptive fields of the vertical system (VS) tangential cells. Using dual-intracellular recordings, Haag and Borst (2004) found VS cells to be mutually coupled in such a way that each VS cell is connected exclusively to its immediate neighbors. This coupling may form the basis of the broad receptive fields of VS cells. Here, we tested this hypothesis directly by photoablating individual VS cells. The receptive field width of VS cells indeed narrowed after the ablation of single VS cells, specifically depending on whether the receptive field of the ablated cell was more frontal or more posterior to the recorded cell. In particular, the responses changed as if the neuron lost access to visual information from the ablated neuron and those VS cells more distal than it from the recorded neuron. These experiments provide strong evidence that the lateral connections among VS cells are a crucial component in the mechanism underlying their complex receptive fields, augmenting the direct columnar input to their dendrites.