Figure 1.

Each Microvillus Is a Stochastically Operating Transduction Unit that Produces Bumps

(A) Drosophila compound eyes (left) are composed of lens-capped ommatidia (center), each of which contains eight photoreceptors (R1–R8). Right shows schematic of the light-insensitive soma and light-sensitive rhabdomere of an outer photoreceptor (R1–R6). Rhabdomere is made out of 30,000 microvilli.

(B) Schematic of phototransduction reactions inside each microvillus. M^∗, metarhodopsin; C^∗, Ca²⁺-calmodulin complex, which acts as negative feedback to multiple targets; D^∗, DAG; P^∗, G protein-PLC complex.

(C) These reactions can be modeled in a stochastic framework, with known molecular interactions, using physiologically measured parameters. Simulated reactions show how a microvillus generates elementary responses (bumps) to captured photons; after a “dead time,” 5-15 TRP-channels open, mediating Ca²⁺ and Na⁺ influx into the microvillus. Ca²⁺-calmodulin complex (red) provides negative feedback, which prevents new bumps until the feedback is low. ^∗ = G^∗ activation failed; ^∗∗ = negative feedback blocked two photon activations. [C^⋆]_i decay phase is longer than the real refractory period, which represents a balance between the feedbacks; the positive feedback can outgrow the negative one in the middle of [C^⋆]_i decay. Thus, a bump can be generated without C^⋆ being zero (e.g., the third bump).

(D) Average bumps from seven photoreceptors (whole-cell voltage clamped currents) and an average simulated bump are similar (currents are actually inward: plotted here as outward for consistency). The bump current is computed by equation 11 (Supplemental Experimental Procedures).

(E) Latency distributions, including ∼10 ms “dead time,” of simulated and real bumps (data from six wild-type cells) are similar.