Synaptic high-frequency jumping synchronises vision to high-speed behaviour

Abstract

Abstract During high-speed behaviour, animals must synchronise perception and action despite rapid environmental and self-generated motion. How neural systems achieve such precision remains unclear. Here we show how the housefly ( Musca domestica ) maintains visual accuracy during fast motion. Using intracellular and photomechanical recordings during saccade-like stimulation, we traced information flow from photoreceptors to large monopolar cells (LMCs). Visual neurons achieved record-high information sampling (~2500 bits·s -1 ) and synaptic transmission (~4100 bits·s -1 ), far exceeding previous estimates. We identify a previously unknown mechanism - synaptic high-frequency jumping - in which photoreceptor-LMC synapses dynamically shift transmission toward higher frequencies during saccades, extending visual bandwidth to ~1000 Hz, effectively eliminating synaptic delays, and quadrupling classical flicker-fusion limits (~230 Hz). Behavioural experiments show flies respond synchronously within ~13-20 ms, even before photoreceptor responses peak. A biophysically realistic model reveals how photomechanical-stochastic-refractory quantal sampling and synaptic transmission co-adapt with saccadic behaviour: through self-motion, flies efficiently translate image motion into temporally-precise, predictive high-speed vision.