Desert locusts Schistocerca gregaria exist in a range of forms between two morphologically and behaviourally distinct extremes, the solitarious and gregarious phases. One marked difference in behaviour is that solitarious animals fly individually, whereas gregarious locusts fly in dense swarms. We show that there are changes in identified visual neurones that can be related to this change in behaviour.

Touching hairs on the hindlegs of a solitarious locust can within 4 h transform that animal’s behaviour so that it acts gregariously (Rogers et al. 2001). We can also drive this change by electrically stimulating a leg sensory nerve.

We have analysed the responses of a visual interneurone, the descending contralateral motion detector (DCMD), and the properties of its output connections onto a leg motor neurone, the fast extensor tibiae (FETi) that is important in escape jumping. DCMD responds maximally to the sight of an object looming towards the locust on a collision course.

The responses of DCMD were tested using simulated looming objects of various sizes and velocities, presented at 1 min intervals. DCMD in gregarious locusts showed little adaptation to repeated stimulation, but in solitarious locusts it showed a pronounced adaptation to 30 % of the value recorded in gregarious locusts.

A spike in DCMD elicited a monosynaptic excitatory postsynaptic potential in the metathoracic FETi, the amplitude of which was approximately 150 % larger in solitarious locusts than in gregarious locusts. Thus although fewer action potentials were elicited in DCMD by visual stimuli in solitarious locusts, each carried a far greater weight at this output synapse. This tunes the visual pathway in solitarious animals so that it is maximally sensitive to infrequent visual stimuli (which is likely to be the normal situation for these animals living singly in large expanses of desert). The same visual pathway of gregarious locusts is tuned by virtue of its resistance to adaptation but weaker synaptic strength so that it continues to function effectively even when the visual environment surrounding the locust contains moving objects. This may help gregarious locusts avoid collisions with conspecifics when they walk or fly in large swarms, or it may serve to maintain the sensitivity of the escape circuit to the sight of an approaching predator even when surrounded by many other locusts.

This work was supported by the BBSRC.