LAUSR

Significance Animal visual systems are typically thought of by analogy to cameras—sensory systems providing continuous information streams that are processed through fixed algorithms. However, studies in flies and mice have shown that visual neurons are dynamically and adaptively retuned by the behavioral state of the animal. In Drosophila, prominent higher-order neurons in the visual system respond more strongly to fast-moving stimuli once the animal starts walking or flying. In this study, we systematically investigated the neurobiological mechanism governing the behavioral-state modulation of directionally selective neurons in Drosophila. We show that behavioral activity modifies the physiological properties of critical neurons in this visual motion circuit and that neuromodulation by central feedback neurons recapitulates these effects. The behavioral state of an animal can dynamically modulate visual processing. In flies, the behavioral state is known to alter the temporal tuning of neurons that carry visual motion information into the central brain. However, where this modulation occurs and how it tunes the properties of this neural circuit are not well understood. Here, we show that the behavioral state alters the baseline activity levels and the temporal tuning of the first directionally selective neuron in the ON motion pathway (T4) as well as its primary input neurons (Mi1, Tm3, Mi4, Mi9). These effects are especially prominent in the inhibitory neuron Mi4, and we show that central octopaminergic neurons provide input to Mi4 and increase its excitability. We further show that octopamine neurons are required for sustained behavioral responses to fast-moving, but not slow-moving, visual stimuli in walking flies. These results indicate that behavioral-state modulation acts directly on the inputs to the directionally selective neurons and supports efficient neural coding of motion stimuli.