Latency of phototransduction limits transfer of higher-frequency signals in cockroach photoreceptors

Visual transduction in rhabdomeric photoreceptors is compartmentalized and discretized. Signals of individual microvilli, the quantum bumps, are electrotonically summed, producing a graded response. Intrinsic dispersion of quantum bump latencies is thought to introduce noise and degrade signal transfer. Here, we found profound differences in the information rate and signaling bandwidth between in vitro patch-clamp and in vivo intracellular recordings of Periplaneta americana photoreceptors and traced them to the properties of quantum bumps and membrane resistance. Comparison of macroscopic and elementary light responses revealed differences in quantum bump summation and membrane resistance in vivo versus in vitro. Modeling of voltage bumps suggested that current bumps in vivo should be much bigger and faster than those actually recorded in vitro. Importantly, the group-average latency of dark-adapted photoreceptors was 30 +/- 8 ms in intracellular (n = 34) versus 70 +/- 19 ms in patch-clamp (n = 57) recordings. Duration of composite responses increased with mean latency because bump dispersion depended on mean latency. In vivo, latency dispersion broadened the composite response by 25% on average and slowed its onset. However, in the majority of photoreceptors, the characteristic durations of multiphoton impulse responses to 1-ms stimuli did not exceed the durations of mean voltage bumps. Consistently, we found strong associations between the latency and onset kinetics of the macroscopic response, on the one hand and the higher-frequency signal gain and information rate of the photoreceptor, on the other hand, indicating a direct connection between quantum bump latency and its dispersion and the signaling bandwidth. NEW & NOTEWORTHY When stimulated by light, microvilli of rhabdomeric photoreceptors produce discrete signals characterized by variable latencies. We show that this intrinsic latency dispersion restricts signaling bandwidth and information rate of photoreceptors in Periplaneta americana. Profound differences are found between the properties of photoreceptor responses in vivo and in vitro.