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

During high-speed behaviour, animals must predict, detect, process, and respond synchronously to rapid environmental changes, including those caused by their own movements. How neural systems achieve such precision remains unclear. Here, we investigate how the housefly (Musca domestica), renowned for agile aerial manoeuvres, maintains visual accuracy during ultrafast motion. Although rapid movements typically blur vision, houseflies exhibit remarkable visual acuity; their visual neurons achieve record-high rates of information sampling (~2,500 bits/s) and synaptic transmission (~4,100 bits/s), substantially surpassing previous estimates. Using intracellular and photomechanical recordings of photoreceptors exposed to rapid sequences of saccade-like stimuli, we traced information transmission to large monopolar cells (LMCs), the first interneurons in the visual pathway. We identify a previously unknown mechanism - synaptic high-frequency jumping - in which photoreceptor-LMC synapses dynamically shift transmission towards higher frequencies during saccadic input. This mechanism extends visual bandwidth to ~920 Hz, eliminates synaptic delays, and quadruples traditional flicker-fusion limits (~230 Hz). Ultrafast behavioural experiments confirm flies respond synchronously within ~13-20 ms, even while photoreceptor responses are still approaching their peak (9-16 ms), directly challenging classical sequential-processing models. Our biophysically realistic photoreceptor-LMC model demonstrates how photomechanical, quantal, and refractory sampling processes co-adapt dynamically with behaviour. Thus, flies actively shape their visual input through self-generated saccades, driving high-frequency jumping, efficient neural coding, hyperacute vision, and neural synchronisation. These findings redefine foundational principles of compound-eye function, uncovering a universal neural strategy underlying synchronous, high-speed predictive processing.