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

Reference	BB/X002276/1
Principal Investigator / Supervisor	Professor Holger Krapp
Co-Investigators / Co-Supervisors
Institution	Imperial College London
Department	Bioengineering
Funding type	Research
Value (£)	452,512
Status	Current
Type	Research Grant
Start date	17/10/2022
End date	16/10/2025
Duration	36 months

Abstract

To study the integration of visuomotor reflexes with goal-directed behaviours in butterflies we will combine state-of-the-art experimental and data analysis methods. Our hypothesis-driven systems approach focuses on optic-flow-sensitive, wide-field descending neurons (WFDNs) which link the motion vision pathway to motor centres in the thoracic ganglion. We will quantify free flight head and body kinematics using a high-resolution motion capture system. Next, we reconstruct the optic flow input to the motion vision pathway based on the results of a dynamic mode decomposition applied to our kinematic data and predict the receptive field properties of premotor WFDNs. We will also characterize the receptive field organization and morphology of WFDNs using electrophysiological recordings in combination with specialized visual stimulation devices. The vector format of WFDN receptive field data will allow us to identify specific optic flow fields, and thus self-motion components, individual descending neurons encode. Measuring the torque butterflies generate in a customized virtual reality setup we will apply systems analysis methods to quantify the performance of reflex and goal-directed behaviours under open-, closed- and semi-open-loop conditions. The setup allows us to project stimuli inducing visuomotor reflexes and polarotactic behaviour onto task-specific functional regions of the butterfly compound eye. Stimuli can be delivered separately or in combination to quantify the integration principles of reflex and goal-directed behaviours. The same setup and stimuli will be used to study WFDN responses in immobilized or tethered flying animals and to test whether the integration both functional pathways involves the use of efference copies. Our work will provide a general conceptual and experimental framework to study neuronal mechanisms and functional design principles underlying the integrated control of reflex and goal-directed behaviours.

Summary

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 ageneral 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.

Committee	Research Committee A (Animal disease, health and welfare)
Research Topics	X – not assigned to a current Research Topic
Research Priority	X – Research Priority information not available
Research Initiative	X - not in an Initiative
Funding Scheme	X – not Funded via a specific Funding Scheme

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