Visual Coding in Locust Photoreceptors

Information capture by photoreceptors ultimately limits the quality of visual processing in the brain. Using conventional sharp microelectrodes, we studied how locust photoreceptors encode random (white-noise, WN) and naturalistic (1/f stimuli, NS) light patterns in vivo and how this coding changes with mean illumination and ambient temperature. We also examined the role of their plasma membrane in shaping voltage responses. We found that brightening or warming increase and accelerate voltage responses, but reduce noise, enabling photoreceptors to encode more information. For WN stimuli, this was accompanied by broadening of the linear frequency range. On the contrary, with NS the signaling took place within a constant bandwidth, possibly revealing a ‘preference’ for inputs with 1/f statistics. The faster signaling was caused by acceleration of the elementary phototransduction current - leading to bumps - and their distribution. The membrane linearly translated phototransduction currents into voltage responses without limiting the throughput of these messages. As the bumps reflected fast changes in membrane resistance, the data suggest that their shape is predominantly driven by fast changes in the light-gated conductance. On the other hand, the slower bump latency distribution is likely to represent slower enzymatic intracellular reactions. Furthermore, the Q10s of bump duration and latency distribution depended on light intensity. Altogether, this study suggests that biochemical constraints imposed upon signaling change continuously as locust photoreceptors adapt to environmental light and temperature conditions

On the Origin and the Signal-Shaping Mechanism of the Fast Photosignal in the Vertebrate Retina

Fast photosignals (FPS) with R(1) and R(2) components were measured in retinas of cattle, rat, and frog within a temperature range of 0° to 60°C. Except for temperatures near 0°C the signal rise of the R(1) component was determined by the duration of the exciting flash. The kinetics of the R(2) component and the meta transition of rhodopsin in the cattle and rat retina were compared. For the analysis of the FPS it is presupposed that the signal is produced by light-induced charges on the outer segment envelope membrane that spread onto the whole plasma membrane of the photoreceptor cell. To a good approximation, this mechanism can be described by a model circuit with two distinct capacitors. In this model, the charging capacitance of the pigmented outer segment envelope membrane and the capacitance of the receptor's nonpigmented plasma membrane are connected via the extra- and intracellular electrolyte resistances. The active charging is explained by two independent processes, both with exponential rise (R(1) and R(2)), that are due to charge displacements within the pigmented envelope membrane. The time constant τ(2) of the R(2) membrane charging process shows a strong temperature dependence that of the charge redistribution, τ(r), a weak one. In frog and cattle retinas the active charging is much slower within a large temperature range than the passive charge redistribution. From the two-capacitor model it follows for τ(r) « τ(2) that the rise of the R(2) component is determined by τ(r), whereas the decay is given by τ(2). For the rat retina, however, τ(2) approaches τ(r) at physiological temperatures and becomes <τ(r) above 45°C. In this temperature range where τ(2) ≈ τ(r), both processes affect rise and decay of the photosignal. The absolute values of τ(r) are in good accordance with the known electric parameters of the photoreceptors. At least in the cattle retina, the time constant τ(2) is identical with that of the slow component of the meta II formation. The strong temperature dependence of the meta transition time gives rise to the marked decrease of the R(2) amplitude with falling temperature. As the R(1) rise could not be fully time resolved the signal analysis does not yield the time constant τ(1) of the R(1) generating process. It could be established, however, within the whole temperature range that the decay of the R(1) component is determined by τ(r). Using an extended model that allows for membrane leakage, we show that in normal ringer solution the membrane time constant does not influence the signal time-course and amplitude