Hoverfly responses to looming stimuli depend on elevation and speed

Abstract

Abstract An object on immediate collision course generates a rapidly expanding visual stimulus on the retina, which will typically trigger a fast reaction, such as an evasive behavior. In hoverflies, for example, visual looming stimuli may be generated if the insect is about to collide with a stationary object in the surround, by an approaching predator, or by conspecifics during territorial interactions. Supporting these behavioral responses is a diverse range of looming sensitive descending neurons that project information from the optic lobes and central brain to the motor control centers in the thoracic ganglia. We here show that the looming sensitive descending neurons are predominantly sensitive to looming stimuli located in the ventral visual field. To investigate if this is matched by behavior, we recorded how tethered hoverflies responded to looming stimuli presented dorsally or ventrally on a visual monitor, at four different speeds ( l/|v| of 10 - 667 ms), covering a naturalistic range. We found that ventral stimuli, especially at intermediate speeds ( l/|v| = 50 or 200 ms), triggered much stronger behavioral responses than dorsally displayed stimuli. The behavioral data thus not only match the receptive fields of the neurons likely to support the behavior, but also highlight that behavioral output is not entirely reflexive but is strongly modulated by stimulus speed and elevation. Significance Statement If someone throws a ball at you, this generates a rapidly expanding object across your visual field, which will make you react before you have even had time to think. You may for example duck, dip or dive to avoid the ball, or bring your hands up to grab it. Similarly, many insects respond to rapidly approaching objects. We here show that hoverfly reactions to such looming stimuli depend on stimulus speed and elevation, with the strongest response to stimuli approaching from below. We further demonstrate that the neurons likely supporting these behaviors show highest sensitivity in the ventral visual field, suggesting a close match between neural tuning and behavioral output.