Collision avoidance and a looming sensitive neuron: size matters but biggest is not necessarily best

Locusts possess visual neurons that can be uniquely identified in each locust and that respond selectively to looming stimuli, giving the animal a warning of impending collision. It has been suggested that one such neuron, the lobula giant movement detector (LGMD), issues this warning by generating a peak in its response that occurs ca. 25 ms after a looming object reaches a subtense of 17 degrees on the eye. This peak is proposed to be a trigger for escape behaviour. We use both modelling and electrophysiological techniques to show that this early peak in LGMD response is not the 'essential functional variable' used naturally by the locust to trigger escape, but rather results from the unnaturally large stimulus used in the previous experimental work. The natural predators of Locusta in Africa, where the locust evolved, are small birds such as the fiscal shrike Lanius collaris humeralis and the carmine bee-eater Merops nubicus, with pectoral diameters of 40-45 mm (measurements from museum specimens). Locusta in flight are less than 100 mm wing tip to wing tip. When a locust views small approaching objects, the response of the LGMD continues to increase throughout the object's approach and the locust is able to trigger escape behaviours without the LGMD response peaking prior to collision.