Neuronal mechanisms of integrated flight control and goal-directed behaviour in butterfly

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How are reflexes that stabilise posture integrated with voluntary behaviours? During locomotion, all animals, including humans, maintain a default body orientation under various environmental conditions. When walking on uneven terrain, flying in turbulent air, or swimming through water currents, powerful inner-loop control systems constantly measure external perturbations and generate negative feedback signals to stabilise locomotion. But what happens if an animal wants to change its trajectory, for instance to avoid collisions or to turn towards attractive targets? Movements to those effects would immediately trigger reflexes stabilizing the original body orientation. As a result, the animal would be trapped by its own reflexes.As a solution to this problem, von Holst and Mittelstaedt (1950) proposed that animals generate an 'efference copy' that predicts the sensory response to self-generated movements. The efference copy neutralizes 'reafferent' sensory signals caused by the voluntary movement, thus preventing stabilization reflexes from kicking in. The advantage of using efference copies is that rather than being blocked altogether, the inner-loop continues to stabilise against unwanted perturbations during volitional behaviours.Although efference copies have been suggested to aid sensory processing in vertebrates and invertebrates, experimental evidence demonstrating their use in neural circuits for locomotor control was obtained only recently in fruitflies. Visual interneurons sensing wide-field optic flow (LPTCs) were found to modulate their activity whenever the fly made a volitional turn, either spontaneously, or in response to a threatening object. These modulations were of the appropriate sign and timing to function as efference copies, cancelling reafferent signals experienced during a turn. However, it remains unknown how these neurons are targeted by efference copies, how efference copies are calculated within the brain, and whether they reflect a general mechanism applicable for other behavioural contexts.Ultimately, any information in the brain that is used to coordinate behavioural action must be relayed to motor systems in the body, which in insects is done by descending neurons. In flies, a small number of descending neurons form bi-directional synapses with LPTCs and are sensitive to specific patterns of wide-field optic flow (WFDNs). Positioned between the visual system and motor systems in the thorax, WFDNs are strategically placed for efference copy modulation by central brain regions involved in generating volitional behaviour. Evidence is also emerging of crosstalk between inner- and outer-loop pathways at the level of descending neurons. Thus, WFDNs may represent a pathway for efference copy transmission to LPTCs at a more peripheral stage of the sensorimotor pathway.Recently, we have discovered a multitude of WFDNs in the butterfly, which may function to stabilise specific components of self-motion experienced during the erratic flight characteristic of these creatures. Butterflies are agile fliers equipped with a visual system exquisitely tuned to colour vision and, in some species, to solve navigational outer-loop tasks using various skylight cues. In this project, we aim to understand how inner- and outer-loop behaviours are integrated in butterfly WFDNs. To this end we will characterise the relationship between the butterfly WFDN neurophysiology and free-flight kinematics, and directly probe their function during inner- and outer-loop behaviours in tethered flight. Overall, this project will provide the conceptual framework to advance our understanding of how small circuits of neurons solve the reflex trap in insects, leading us towards more generalisable design principles for integrated sensorimotor control.