Closed-loop behavioral control increases coherence in the fly brain

Abstract

A crucial function of the brain is to be able to distinguish whether or not changes in the environment are caused by one’sownactions. Even the smallest brains appear to be capable of making this distinction, as has been shown by closed-loop behavioral experiments in flies controlling visual stimuli in virtual reality paradigms. We questioned whether activity in the fruit fly brain is different during such closed-loop behavior, compared with passive viewing of a stimulus. To address this question, we used a procedure to record local field potential (LFP) activity across the fly brain while flies were controlling a virtual object through their movement on an air-supported ball. The virtual object was flickered at a precise frequency (7 Hz), creating a frequency tag that allowed us to track brain responses to the object while animals were behaving. Following experiments under closed-loop control, we replayed the same stimulus to the fly in open loop, such that it could no longer control the stimulus. We found identical receptive fields and similar strength of frequency tags across the brain for the virtual object under closed loop and replay. However,whencomparing central versus peripheral brain regions,wefound that brain responses were differentially modulated depending on whether flies were in control or not. Additionally, coherence of LFP activity in the brain increased when flies were in control, compared with replay, even if motor behavior was similar. This suggests that processes associated with closed-loop control promote temporal coordination in the insect brain.