Author(s): Erginkaya, Mert ; Cruz, Tomás ; Brotas, Margarida ; Marques, André ; Steck, Kathrin ; Nern, Aljoscha ; Torrão, Filipa ; Varela, Nélia ; Bock, Davi D. ; Reiser, Michael ; Chiappe, M. Eugenia
Date: 2025
Persistent ID: http://hdl.handle.net/10362/183110
Origin: Repositório Institucional da UNL
Subject(s): Neuroscience(all)
Funding Information: We thank R. Parekh and Janelia CAT for introducing us to FAFB and training us in EM tracing. K. Coates and F. Li for reviewing some of our manually traced neurons in FAFB. S. Huston for tracing of CNMNs, VCNMN and some cLPTCrn cells together with S. Imtiaz and B. Gorko, and for helping identify neck motor neurons. A. Li and R. Wilson for their help in reconstructing DNa02. S. Namiki and G. Card for their help in identifying DNs. J. Goldammer for identifying potential split-Gal4 candidates for H2rn cells and helping identify S-Neurons. H. Otsuna, G. Jefferis and P. Schlegel for introducing us to their tools for computational neuroanatomy and for helping with EM data analysis. A. Zhao for his input on LPT naming, response predictions and feedback on the manuscript. N. Eckstein and J. Funke for sharing neurotransmitter predictions for LPT partners before publication. We thank the Princeton FlyWire team and members of the Murthy and Seung laboratories, as well as members of the Allen Institute for Brain Science, for development and maintenance of FlyWire (supported by BRAIN Initiative grants MH117815 and NS126935 to Murthy and Seung). We also acknowledge members of the Princeton FlyWire team and the FlyWire consortium for neuron proofreading and annotation (Supplementary Table lists all contributors). We thank the Murphy and Seung laboratories and the Jefferis laboratory for their contribution with 31.83% and 46.27% of the total editions in FlyWire neurons, respectively. In addition, we acknowledge the contribution of the Seeds and Hampel laboratory, the Wilson laboratory, the Bidaye laboratory, the Borst laboratory, the Kim laboratory and the Selcho laboratory for additional contributions. We thank members of the Cambridge Connectomics Group (G. Jefferis and M. Costa) including L. Serratosa, A. Javier, S. Fang, K. Eichler and P. Schlegel for contributing to the proofreading of FlyWire Neurons. Proofreading in Cambridge was supported by the Wellcome Trust (Collaborative Award 203261/Z/16/Z) and National Institutes of Health (NIH) (BRAIN Initiative 1RF1MH120679-01). Development and administration of the FAFB tracing environment and analysis tools were funded in part by NIH BRAIN Initiative grant 1RF1MH120679-01 to D. Bock and G. Jefferis, with software development effort and administrative support provided by T. Kazimiers (Kazmos) and E. Perlman (Yikes). We also thank G. Maimon and C. Lyu for sharing sytGCaMP7f flies before publication. G. Rubin and H. Dionne (Rubin laboratory) for transgene constructs and reinjections. M. Silies for sharing the UAS-GCaMP6f, UAS-FLP recombinant line. E. S\u00F6nmez for help with testing Split-Gal4 combinations and help with validating FlpStop recombinants. The CR Fly Platform for assisting fly stock generation, maintenance and GABA staining. L. Venkatasubramanian for her help with the initial bIPS>TrpA1 behavior experiments. T. Fujiwara for help with finding and testing potential Split-Gal4 combinations for H2rn and uLPTCrns and help with building the two-photon calcium imaging setup. W. Stagnaro for sharing unpublished work about multisensory processing in LPTCrns and bIPS cells. Past and present Chiappe Laboratory members for useful discussions and feedback on experiments and the manuscript. This work was supported by the Champalimaud Foundation and the research infrastructure Congento, LISBOA-01-0145-FEDER-022170. M.E.C. is supported by European Research Council Starting Grant ERC-2017-STG-759782 537 and European Research Council Consolidator Grant ERC-2022-CoC-101088936. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript. Publisher Copyright: © The Author(s) 2025.
Many animals navigate using optic flow, detecting rotational image velocity differences between their eyes to adjust direction. Forward locomotion produces strong symmetric translational optic flow that can mask these differences, yet the brain efficiently extracts these binocular asymmetries for course control. In Drosophila melanogaster, monocular horizontal system neurons facilitate detection of binocular asymmetries and contribute to steering. To understand these functions, we reconstructed horizontal system cells’ central network using electron microscopy datasets, revealing convergent visual inputs, a recurrent inhibitory middle layer and a divergent output layer projecting to the ventral nerve cord and deeper brain regions. Two-photon imaging, GABA receptor manipulations and modeling, showed that lateral disinhibition reduces the output’s translational sensitivity while enhancing its rotational selectivity. Unilateral manipulations confirmed the role of interneurons and descending outputs in steering. These findings establish competitive disinhibition as a key circuit mechanism for detecting rotational motion during translation, supporting navigation in dynamic environments.
