Behavioral/Systems/CognitiveSharing Receptive Fields with Your Neighbors:Tuning the Vertical System Cells to Wide Field MotionKarl Farrow, Alexander Borst, and Juergen HaagDepartment of Systems and Computational Neurobiology, Max-Planck-Institute of Neurobiology, 82152 Martinsried, GermanyIn the blowfly, the direction-selective response of the 60 lobula-plate tangential cells has been ascribed to the integration of local motioninformation across their extensive dendritic trees. Because the lobula plate is organized retinotopically, the receptive fields of thetangential cells ought to be determined by their dendritic architecture. However, this appears not always to be the case. One compellingexample is the exceptionally wide receptive fields of the vertical system (VS) tangential cells. Using dual-intracellular recordings, Haagand 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 photoablatingindividual VS cells. The receptive field width of VS cells indeed narrowed after the ablation of single VS cells, specifically depending onwhether the receptive field of the ablated cell was more frontal or more posterior to the recorded cell. In particular, the responses changedas 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 mechanismunderlying their complex receptive fields, augmenting the direct columnar input to their dendrites.Key words: insect; blowfly; laser ablation; motion detection; neural network; receptive fieldIntroductionIn blowflies, the processing of large field motion is performed inthe posterior division of the third neuropile of the optic lobe, thelobula plate. Within the lobula plate, there exist ⬃60 individuallyidentifiable motion-sensitive neurons (tangential cells) perhemisphere. Among them, the vertical system (VS) cells form oneof the major output elements. The direction-selective response tomotion of tangential cells has been ascribed to the dendritic in-tegration of local motion detector input onto the dendritic tree ofeach cell (Borst and Egelhaaf, 1992; Haag et al., 1992, 2004; Singleand Borst, 1998). Because the input to the lobula plate is orga-nized into retinotopic columns, the expected receptive field ofeach cell should be a consequence of the preferred direction of itslocal motion input, as well as its dendritic location andarchitecture.The 10 VS cells are typically T-shaped, with their overlappingdendritic arborizations lying serially, collectively covering thelobula plate. Their axons project centrally and run close together(Haag and Borst, 2004). They are sequentially named (VS1–VS10), in which the dendrites of the VS1 cell reach the lateral edgeof the lobula plate and the dendritic domains of successive neu-rons shift medially in accordance with their name. VS cells re-spond maximally to downward motion presented at a particularposition with a graded depolarization (Hengstenberg, 1977,1982; Krapp et al., 1998). Based on the retinotopic input to thelobula plate and the area of the lobula plate covered by the den-drites of each cell (12–29% for VS2–VS9) (Hengstenberg et al.,1982), the width of the receptive field should amount to ⬃30 –40°. However, the receptive fields of VS cells are more complexthan thought previously. One interesting characteristic is that VScells respond to downward motion across a much wider slice ofthe visual world than expected by their dendritic extent (Krapp etal., 1998). In addition, the medial VS cells (VS8 –VS10) respondto upward vertical motion in the frontal visual field (Krapp et al.,1998). This is far outside the visual space expected from theirdendritic coverage of the lobula plate.A recent dual-intracellular recording study demonstrated thatVS cells are electrically connected, putatively via their axons(Haag and Borst, 2004). The connection strength was found todecrease with increasing distance between the VS cells. This couldbe explained in the most parsimonious way by assuming thateach VS cell is connected exclusively to its immediate neighbors,forming a row of cells with the VS1 and VS10 cells at oppositeends. To account for the sign reversal found between VS1 andVS8 –VS10 cells in the same study, an additional inhibitory con-nection had been postulated linking the medial and lateral cells.This connection scheme was proposed to be responsible for theextremely wide receptive fields of VS cells and the responsivenessof the medial VS cells to frontal visual stimuli.Here, single VS cells were ablated to address three questionsraised by the current injection experiments of Haag and Borst(2004). First, is the coupling between VS cells responsible fortheir broad receptive fields? Second, are the connections betweenthe VS cells accomplished in a chain-like manner, or does each VSReceived Jan. 13, 2005; revised Feb. 28, 2005; accepted March 5, 2005.This work was supported by the Max Planck Society. We thank Y. Choe for carefully reading this manuscript aswell as D. Reiff and Y. Elada for helpful discussions.Correspondence should be addressed to Karl Farrow, Department of Systems and Computational Neurobiology,Max-Planck-Institute of Neurobiology, Am Klopferspitz 18a, 82152 Martinsried, Germany. E-mail: [email protected]:10.1523/JNEUROSCI.0168-05.2005Copyright © 2005 Society for Neuroscience 0270-6474/05/253985-09$15.00/0The Journal of Neuroscience, April 13, 2005 • 25(15):3985–3993 • 3985cell make reciprocal connections with all others separately?Third, can the posited inhibitory loop input from the VS1 cell tothe medial VS cells account for the sensitivity of the medial VScells to vertical motion in the frontal visual field?Materials and MethodsAnimal preparation. Two- to 7-d-old female blowflies (Calliphora vicina)were briefly anesthetized with CO2and mounted ventral-side up withwax on a small plate of glass. The head capsule was opened from behind,and the trachea and air sacs that normally cover the lobula plate wereremoved. To minimize movements of the brain, the proboscis of theanimal was stretched forward and waxed to its thorax. Also, the antennaswere removed, the antennal muscles