Quantifying the link between retinal performance and the optomotor response

Visually driven behaviors continuously adjust as the animal experiences different external environments or internal states. To understand the neural basis of this plasticity, we must quantify the relation between changes in the operation of circuits in the visuo-motor pathway and the behavioral output. Here, we use larval zebrafish to measure how modulation of the retina impacts the optomotor response (OMR). We find that diurnal changes in the contrast dependence of the OMR are linearly dependent on changes in the rate at which information about contrast is transmitted across the population of bipolar cells: when synaptic information rates increased 4-fold, the contrast gain of the behavior increased 2.4-fold. The energetic cost of the improvement in retinal performance was offset by the circuit switching to a state in which each vesicle transmitted 2-4 times as much information at any given release rate. These results demonstrate that retinal noise limits a behavior driven by cone photoreceptors, not just at threshold but also across a range of contrasts found in natural stimuli. Adjustment of the retinal circuit between operating regimes of higher and lower information efficiency also demonstrates a previously unrecognized aspect of modulation by internal state that we propose reflects a trade-off between the energetic cost of retinal computation and the ecological benefits of visually driven behaviors at different stages of the solar cycle. This study supports the idea that information measures will be useful in investigating links between the operation of neural circuits and behavior.