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The central complex, a group of midline neuropils in the insect brain, plays a key role in spatial orientation and navigation. Work in locusts, crickets, dung beetles, bees and butterflies suggests that it harbors a network of neurons which determines the orientation of the insect relative to the pattern of polarized light in the blue sky. In locusts, these 'compass cells' also respond to simulated approaching objects. Here, we investigated in the locust Schistocerca gregaria whether compass cells change their activity when the animal experiences large-field visual motion or when the animal is engaged in walking behavior. We recorded intracellularly from these neurons while the tethered animals were allowed to perform walking movements on a slippery surface. We concurrently presented moving grating stimuli from the side or polarized light through a rotating polarizer from above. Large-field motion was combined with simulation of approaching objects to evaluate whether responses differed from those presented on a stationary background. We show for the first time that compass cells are sensitive to large-field motion. Responses to looming stimuli were often more conspicuous during large-field motion. Walking activity influenced spiking rates at all stages of the network. The strength of responses to the plane of polarized light was affected in some compass cells during leg motor activity. The data show that signaling in compass cells of the locust central complex is modulated by visual context and locomotor activity.

Responses of compass neurons in the locust brain to visual motion and leg motor activity