Dorsal ocelli set the luminance-dependent operating state of the bumblebee visual system

Abstract

Despite long-standing hypotheses that insect dorsal ocelli modulate compound-eye processing to support flight stabilization, dim-light navigation, and locomotor speed, the neurophysiological basis of these functions remains unclear. Combining behavioural assays with multi-site local field potential recordings in bumblebees, we tested how ocellar input affects compound-eye processing. Ocellar occlusion impaired orientation precision at dusk, supporting a role for ocelli in dim-light navigation. Under bright daytime skies, occlusion did not affect orientation but reduced flight speed, consistent with a role in locomotor control under high illumination. Neurophysiologically, ocellar occlusion disrupted luminance-dependent scaling across the visual system, most prominently in the medulla. In intact bees, broadband neural power scaled inversely with luminance, decreasing under bright and increasing under dim conditions. When ocellar input was blocked, this relationship reversed, leaving visual-system activity in a high-power, dark-like state even under bright illumination. Ocellar modulation was particularly evident in the green-sensitive pathway, implicated in optic-flow processing and flight-speed regulation, providing a neural correlate of the behavioural speed reduction while UV-sensitive responses remained largely invariant following ocellar occlusion. These findings reconcile disparate views of ocellar function and identify ocelli as regulators of the neural dynamic range supporting orientation in low light and movement control in bright conditions.