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

Abstract

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.

TheDrosophilaSK Channel (dSK) Contributes to Photoreceptor Performance by Mediating Sensitivity Control at the First Visual Network

“…Flies of either sex were immobilized in a conical fly holder with beeswax, as previously described (Juusola and Hardie, 2001;Zheng et al, 2006). To allow the recording microelectrode to enter the retina/lamina, a small hole with the size of few ommatidia was cut in the dorsal cornea and sealed with Vaseline to prevent the eye from drying.…”

“…In Drosophila, we have not identified different LMC subtypes, but as L1 and L2 occupy the largest volume most recordings were probably in them. It is also possible that we occasionally record from processes of amacrine cells that share histaminergic input with L2 and L1 cells (Shaw, 1984;Zheng et al, 2006Zheng et al, , 2009. However, because the selected recordings to the given stimuli in Drosophila lamina had rather similar hyperpolarizing characteristics, all LMC data were analyzed together.…”

“…4 B, C). Here, we recall that the voltage output of fly photoreceptors constitutes a complex convolution of light current (Hardie and Raghu, 2001), light-insensitive membrane filtering and feedbacks from their neuronal neighbors (Shaw, 1984;Weckström and Laughlin, 1995;Juusola and Hardie, 2001;Zheng et al, 2006).The dSK mutation could, therefore, affect any or all of these mechanisms, leading to the observed fast responses.…”

“…In turn, L2 and AC feedback onto photoreceptor terminals via excitatory inputs (Sinakevitch and Strausfeld, 2004;Kolodziejczyk et al, 2008). Upon light stimulation, photoreceptors depolarize while LMCs/ACs hyperpolarize (Shaw, 1984;Zheng et al, 2006), which thereby reduces excitatory feedback onto the photoreceptors. Accordingly, voltage responses in the photoreceptor-LMC-photoreceptor network appear shaped together and adapt together (network adaptation), presumably to best encode and route light information over multiple pathways Zheng et al, 2009).…”

Visualizing retinotopic half-wave rectified input to the motion detection circuitry of Drosophila

“…The reported inhibitory current through histamine gated chloride channels 32 explains the hyperpolarizing ON-response 37 , however, it does not explain the excitatory OFF-component at the end of a light pulse that has been observed in large flies [33][34][35][36][37] . In Drosophila depolarizing voltage responses to light-OFF have not been observed 38 .…”