(A) A classic model with (i) a symmetrical receptive field and (ii) an immobile rhabdomere leads to identical (iii) light inputs and virtually identical (iv) photoreceptor outputs (minute differences result from stochastic photon sampling), respectively, for the dots moving in the opposite directions. (B) A model with (ii) a moving rhabdomere generates both dynamic (iii) light input and (iv) photoreceptor output, which rise and decay earlier for the back-to-front moving dot (red traces) than the front-to-back moving dot (blue traces). (C) Our full model with rhabdomere contraction dynamics that move and narrow its receptive field. This makes the light input and photoreceptor output rise and decay faster than in the other two models, with the back-to-front waveforms leading the front-to-back counterparts. (D) The intracellular responses of a R1-R6 photoreceptor to the given two dot stimuli, as recorded in vivo, show similar dynamics to the full model in (C) with its back-to-front signals (red) leading the front-to-back signals (blue).