Network adaptation improves temporal representation of naturalistic stimuli in Drosophila eye
Retinal networks must adapt constantly to best present the ever changing visual world to the brain. Although such processing is often considered sequential, it is likely that adaptation occurs ubiquitously across the whole retinal network. What then are the dynamics and mechanisms of network adaptation in retinal information processing?
Drosophila, with its well-defined genetics, modular eye structure, fully characterized synaptic layout of the first visual neuropil1 and accessibility for electrophysiology of single neurons2, 3 is a powerful model for studying neural adaptation in vivo. The first visual neuropile, the lamina, contains a system of neurons consisting of photoreceptors (R1-R6) and interneurons: large monopolar cells (LMCs; L1-L5) and an amacrine cell (AC) that co-process visual information4. While photoreceptors depolarize and LMCs hyperpolarize to light, owing to a web of feedforward and feedback synapses their graded voltage responses are shaped together3.
Here we exploit an in vivo Drosophila preparation to investigate how the circuits in the fly eye route and process changing information toward the fly brain. We studied adaptation dynamics at the first visual synaptic layer in Drosophila by intracellularly recording responses of photoreceptors (R1-R6) and their histaminergic output neurons, large monopolar cells (LMCs) to naturalistic light contrast series. By analyzing the synaptic throughput in wild-type and mutant flies, we show that visual information processing is dynamically enhanced by network adaptation.
Network adaptation improves both the frequency and amplitude representation of LMC output by enhancing sensitivity to under-represented signals, and the signal-to-noise ratio of this transmission. It happens at different speeds for different brightness of stimulation, requiring a dynamic balance between the light-mediated conductance and feedback-mediated synaptic conductances. This equilibrium can be offset by tampering with either synaptic feedforward or feedback pathways. A faulty feedforward pathway in post-synaptic ort6 mutants speeds up LMC output, mimicking extreme light adaptation; a faulty feedback pathway in L2-shiTS1 flies slows down LMC output, mimicking dark adaptation.
These results highlight the importance of network adaptation for efficient neural coding and as a mechanism for selectively regulating the size and speed of signals in neurons.
References
1. Meinertzhagen IA & O'Neil, S. D. Synaptic organization of columnar elements in the lamina of the wild type in Drosophila melanogaster. J Comp Neurol 305, 232-63 (1991).
2. Juusola, M. & Hardie, R.C. Light adaptation in Drosophila photoreceptors: I. Response dynamics and signaling efficiency at 25 oC. J Gen Physiol 117, 3-25 (2001).
3. Zheng, L. et al. Feedback network controls photoreceptor output at the layer of first visual synapses in Drosophila. J Gen Physiol 127, 495-510 (2006).
4. Meinertzhagen IA & Sorra, K. E. Synaptic organization in the fly's optic lamina: few cells, many synapses and divergent microcircuits. Prog Brain Res 131, 53-69 (2001).
Conference:
Computational and systems
neuroscience 2009, Salt Lake City, UT, United States, 26 Feb - 3 Mar, 2009.
Presentation Type:
Poster Presentation
Topic:
Poster Presentations
Citation:
(2009). Network adaptation improves temporal representation of naturalistic stimuli in Drosophila eye.
Front. Syst. Neurosci.
Conference Abstract:
Computational and systems
neuroscience 2009.
doi: 10.3389/conf.neuro.06.2009.03.002
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Received:
28 Jan 2009;
Published Online:
28 Jan 2009.