Visual projection neurons (VPNs) provide an anatomical connection between early visual processing and higher brain regions. Here we characterize lobula columnar (LC) cells, a class of Drosophila VPNs that project to distinct central brain structures called optic glomeruli. We anatomically describe 22 different LC types and show that, for several types, optogenetic activation in freely moving flies evokes specific behaviors. The activation phenotypes of two LC types closely resemble natural avoidance behaviors triggered by a visual loom. In vivo two-photon calcium imaging reveals that these LC types respond to looming stimuli, while another type does not, but instead responds to the motion of a small object. Activation of LC neurons on only one side of the brain can result in attractive or aversive turning behaviors depending on the cell type. Our results indicate that LC neurons convey information on the presence and location of visual features relevant for specific behaviors.DOI: http://dx.doi.org/10.7554/eLife.21022.001

Human tumours exhibit a large degree of cellular and genetic heterogeneity 1. Complex cell interactions in the tumour and its microenvironment are thought to play a significant role in tumourigenesis and cancer progression 2. It is also known that cooperation between oncogenic genetic lesions is required for tumour development 3. However, it is not known how cell interactions contribute to oncogenic cooperation. The genetic techniques available in the fruit fly Drosophila melanogaster allow analysis of the behavior of cells with distinct mutations 4, giving this model organism a privileged position to study cell interactions and oncogenic cooperation. In Drosophila eye-antennal discs, cooperation between the oncogenic protein RasV12 5 and loss-of-function mutations in the conserved tumour suppressor scribble (scrib) 6,7 gives rise to metastatic tumours that display many characteristics observed in human cancers 8-11. Here we show that clones of cells bearing different mutations can cooperate to promote tumour growth and invasion in Drosophila. We found that the RasV12 and scrib− mutations can also cause tumours when they affect different adjacent epithelial cells. We show that this interaction between RasV12 and scrib− clones involves JNK signaling propagation and JNK-induced upregulation of JAK/STAT-activating cytokines, a compensatory growth mechanism for tissue homeostasis. The development of RasV12 tumours can also be triggered by tissue damage, a stress condition that activates JNK signaling. Given the conservation of the pathways examined here, similar cooperative mechanisms could play a role in the development of human cancers.

SUMMARY Studies in mice and humans have demonstrated a role for the immune system in preventing the growth of tumors. Deciphering the mechanisms involved in the immune response to tumors is essential to our understanding of immune recognition and cancer progression. Here we report an innate immune response to tumors in Drosophila melanogaster. We found that circulating blood cells, termed hemocytes, adhere to tumors upon detection of basement membrane disruption, and subsequently counter their growth. Basement membrane components are remarkably conserved throughout the animal kingdom, providing a unique structure for the immune system to sense tissue integrity. Further, we show that tissue damage activates JNK signaling in both tumors and aseptic wounds, causing expression of JAK/STAT-activating cytokines. Cytokine secretion from the injured tissue is amplified into a systemic response through the induction of additional cytokine expression in the hemocytes and the fat body, resulting in hemocyte proliferation. Our findings reveal common mechanisms in the response to tumors and wounds in flies. A similar innate reaction may underlie the response to tumors and tissue damage in vertebrates and humans.