Random Photon Absorption Model Elucidates How Early Gain Control in Fly Photoreceptors Arises from Quantal Sampling

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

Early visual encoding of Musca domestica

Fly vision has often been considered to be quite poor, both temporally and spatially, as it is limited by numerous different factors (i.e. number of sampling units, lens dimensions, photoreceptors’ slow integration time, ambient light level as well as flies’ own speed when in motion) (Mallock, 1894; Fermi and Richardt, 1963; Srinivasan and Bernard, 1975; Warrant and McIntyre, 1992; Land, 1997; Warrant, 1999). Some studies have challenged these views and found that flies have evolved to partially overcome these constraints (i.e. via acute zones, head/thorax and body movements) (van Hateren and Schilstra, 1999; Hornstein et al., 2000; Burton, Tatler and Laughlin, 2001; Burton and Laughlin, 2003). One recent example from Juusola et al. (2017) showed that Drosophila photoreceptors contract to light and these photomechanical contractions coupled with refractory sampling enable the fly to overcome motion blur even to objects smaller than their optical limit. Following on from this work, my aim was to test whether different aspects of a fast-flying housefly (Musca domestica) would also have enhanced spatial and temporal vision beyond our current understanding. If slow-flying Drosophila with its optically poorer vision has evolved to compensate for its limitations, then in theory we should see similar, or better, improvements in a faster flying fly such as Musca. Additionally, working with Musca created the opportunity to investigate any presence of sexual dimorphism, as males have "love spots", which Drosophila males lack (GonzalezBellido, Wardill and Juusola, 2011; Perry and Desplan, 2016). My work focussed on examining via in vivo intracellular recordings visual encoding of Musca photoreceptors (R1-R6) and what happens to that information when passed downstream to large monopolar cells (LMCs, L1-L3). In total, this examination resulted in three separate studies: (i) early temporal encoding during body saccades, (ii) R1- R6 and L1-L3 cells' response properties during light adaptation and its impact on underlying quantum bumps (QBs) and (iii) hyperacuity of photoreceptors and LMCs. I found that temporal encoding of Musca early vision was better than previously thought, especially in male flies. Additionally, both photoreceptors' and LMCs’ signalling performance to different stimulus statistics improved when brightening mean light levels. However, when looking at spatial encoding, both male and female photoreceptors were in general not able to resolve details finer than their optical limit i.e. they were not hyperacute. LMCs may have this ability but further investigations are required