The Journal of General Physiology
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Published online Apr 24 2006. doi:10.1085/jgp.200509470
The Rockefeller University Press, 0022-1295 $8.00
JGP, Volume 127, Number 5, 495-510
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ARTICLE

 Feedback Network Controls Photoreceptor Output at the Layer of First Visual Synapses in Drosophila



Lei Zheng1, Gonzalo G. de Polavieja2,3, Verena Wolfram1, Musa H. Asyali4, Roger C. Hardie5, and Mikko Juusola1

1 Department of Biomedical Science, University of Sheffield, Sheffield S10 2TN, UK
2 Department of Theoretical Physics, Universidad Autónoma de Madrid, 28049 Spain
3 Instituto Nicolás Cabrera de Física de Materiales, Universidad Autónoma de Madrid, 28049 Spain
4 Faculty of Engineering and Architecture, Yasar University, Izmir, Turkey
5 Department of Anatomy, University of Cambridge, Cambridge CB2 3DY, UK

Correspondence to Mikko Juusola: m.juusola{at}sheffield.ac.uk

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.

Abbreviations used in this paper: AC, amacrine cell; ERG, electroretinogram; LMC, large monopolar cell; NS, naturalistic stimulation; SNR, signal-to-noise ratio; WT, wild-type.


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