title: Random Photon Absorption Model Elucidates How Early Gain Control in Fly Photoreceptors Arises from Quantal Sampling.
abstract: Many diurnal photoreceptors encode vast real-world light changes effectively, but how this performance originates from photon sampling is unclear. A 4-module biophysically-realistic fly photoreceptor model, in which information capture is limited by the number of its sampling units (microvilli) and their photon-hit recovery time (refractoriness), can accurately simulate real recordings and their information content. However, sublinear summation in quantum bump production (quantum-gain-nonlinearity) may also cause adaptation by reducing the bump/photon gain when multiple photons hit the same microvillus simultaneously. Here, we use a Random Photon Absorption Model (RandPAM), which is the 1st module of the 4-module fly photoreceptor model, to quantify the contribution of quantum-gain-nonlinearity in light adaptation. We show how quantum-gain-nonlinearity already results from photon sampling alone. In the extreme case, when two or more simultaneous photon-hits reduce to a single sublinear value, quantum-gain-nonlinearity is preset before the phototransduction reactions adapt the quantum bump waveform. However, the contribution of quantum-gain-nonlinearity in light adaptation depends upon the likelihood of multi-photon-hits, which is strictly determined by the number of microvilli and light intensity. Specifically, its contribution to light-adaptation is marginal (≤ 1%) in fly photoreceptors with many thousands of microvilli, because the probability of simultaneous multi-photon-hits on any one microvillus is low even during daylight conditions. However, in cells with fewer sampling units, the impact of quantum-gain-nonlinearity increases with brightening light.
authors.affiliation: Centre for Mathematics, Physics and Engineering in the Life Sciences and Experimental Biology (CoMPLEX), University College LondonLondon, UK; Department of Biomedical Science, University of SheffieldSheffield, UK.
authors.forename: Zhuoyi
authors.initials: Z
authors.lastname: Song
authors.affiliation: School of Engineering, College of Science and Technology, University of Central Lancashire Preston, UK.
authors.forename: Yu
authors.initials: Y
authors.lastname: Zhou
authors.affiliation: Department of Biomedical Science, University of SheffieldSheffield, UK; State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal UniversityBeijing, China.
authors.forename: Mikko
authors.initials: M
authors.lastname: Juusola
keywords: Random Photon Absorption Model (RandPAM); light adaptation; multi-photon-hits; photon sampling; photoreceptor; quantum-gain-nonlinearity; sublinear summation