Descending premotor target tracking systems in flying insects

The control of behaviour in all animals requires efficient transformation of sensory signals into the task-specific activation of muscles. Predation offers an advantageous model behaviour to study the computational organisation underlying sensorimotor control. Predators are optimised through diverse evolutionary arms races to outperform their prey in terms of sensorimotor coordination, leading to highly specialised anatomical adaptations and hunting behaviours, which are often innate and highly stereotyped. Predatory flying insects present an extreme example, performing complex visually-guided pursuits of small, often fast flying prey over extremely small timescales. Furthermore, this behaviour is controlled by a tiny nervous system, leading to pressure on neuronal organisation to be optimised for coding efficiency. In dragonflies, a population of eight pairs of bilaterally symmetric Target Selective Descending Neurons (TSDNs) relay visual information about small moving objects from the brain to the thoracic motor centres. These neurons encode the movement of small moving objects across the dorsal fovea region of the eye which is fixated on prey during predatory pursuit, and are thought to constitute the commands necessary for actuating an interception flight path. TSDNs are characterised by their receptive fields, with responses of each TSDN type spatially confined to a specific portion of the dorsal fovea visual field and tuned to a specific direction of object motion. To date, little is known about the descending representations mediating target tracking in other insects. This dissertation presents a comparative report of descending neurons in a variety of flying insects. The results are organised into three chapters: Chapter 3 identifies TSDNs in demoiselle damselflies and compares their response properties to those previously described in dragonflies. Demoiselle TSDNs are also found to integrate binocular information, which is further elaborated with prism and eyepatch experiments. Chapter 4 describes TSDNs in two dipteran species, the robberfly Holcocephala fusca and the killerfly Coenosia attenuata. Chapter 5 describes an interaction between small- and wide-field visual features in TSDNs of both predatory and nonpredatory dipterans, finding functional similarity of these neurons for prey capture and conspecific pursuit. Dipteran TSDN responses are repressed by background motion in a direction dependent manner, suggesting a control architecture in which target tracking and optomotor stabilization pathways operate in parallel during pursuit.

Name dc:type.qualificationname

Doctor of Philosophy (PhD)

Level dc:type.qualificationlevel

Doctoral

Grantor dc:publisher.institution

University of Cambridge

Year dc:date.issued

2019

Author dc:creator

• Supple, Jack

Advisor dc:contributor.advisor

• Franze, Kristian

• neuroethology
• descending neurons
• vision
• insect
• predation
• neuroscience

Licence

• https://apollo8-f-pro.lib.cam.ac.uk/bitstreams/962d0844-cd8a-4118-9866-a80cbab9217c/download
• https://creativecommons.org/licenses/by-nc-sa/4.0/

Language dc:language

eng

Author Identifier

0000-0002-8425-7297

OAI identifier oai:identifier

oai:www.repository.cam.ac.uk:1810/314894