Feedback Network Controls Photoreceptor Output at the Layer of First Visual Synapses in <i>Drosophila </i>

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  • Lei Zheng
    1Department of Biomedical Science, University of Sheffield, Sheffield S10 2TN, UK
  • Gonzalo G. de Polavieja
    2Department of Theoretical Physics, Universidad Autónoma de Madrid, 28049 Spain
  • Verena Wolfram
    1Department of Biomedical Science, University of Sheffield, Sheffield S10 2TN, UK
  • Musa H. Asyali
    4Faculty of Engineering and Architecture, Yasar University, Izmir, Turkey
  • Roger C. Hardie
    5Department of Anatomy, University of Cambridge, Cambridge CB2 3DY, UK
  • Mikko Juusola
    1Department of Biomedical Science, University of Sheffield, Sheffield S10 2TN, UK

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<jats:p>At the layer of first visual synapses, information from photoreceptors is processed and transmitted towards the brain. In fly compound eye, output from photoreceptors (R1–R6) that share the same visual field is pooled and transmitted via histaminergic synapses to two classes of interneuron, large monopolar cells (LMCs) and amacrine cells (ACs). The interneurons also feed back to photoreceptor terminals via numerous ligand-gated synapses, yet the significance of these connections has remained a mystery. We investigated the role of feedback synapses by comparing intracellular responses of photoreceptors and LMCs in wild-type Drosophila and in synaptic mutants, to light and current pulses and to naturalistic light stimuli. The recordings were further subjected to rigorous statistical and information-theoretical analysis. We show that the feedback synapses form a negative feedback loop that controls the speed and amplitude of photoreceptor responses and hence the quality of the transmitted signals. These results highlight the benefits of feedback synapses for neural information processing, and suggest that similar coding strategies could be used in other nervous systems.</jats:p>

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