Neural Summation in the Hawkmoth Visual System Extends the Limits of Vision in Dim Light

Abstract

Most of the world’s animals are active in dim light and depend on good vision for the tasks of daily life. Many have evolved visual adaptations that permit a performance superior to that of manmade imaging devices [1]. In insects, a major model visual system, nocturnal species show impressive visual abilities ranging from flight control [2, 3], to color discrimination [4, 5], to navigation using visual landmarks [6, 7, 8] or dim celestial compass cues [9, 10]. In addition to optical adaptations that improve their sensitivity in dim light [11], neural summation of light in space and time—which enhances the coarser and slower features of the scene at the expense of noisier finer and faster features—has been suggested to improve sensitivity in theoretical [12, 13, 14], anatomical [15, 16, 17], and behavioral [18, 19, 20] studies. How these summation strategies function neurally is, however, presently unknown. Here, we quantified spatial and temporal summation in the motion vision pathway of a nocturnal hawkmoth. We show that spatial and temporal summation combine supralinearly to substantially increase contrast sensitivity and visual information rate over four decades of light intensity, enabling hawkmoths to see at light levels 100 times dimmer than without summation. Our results reveal how visual motion is calculated neurally in dim light and how spatial and temporal summation improve sensitivity while simultaneously maximizing spatial and temporal resolution, thus extending models of insect motion vision derived predominantly from diurnal flies. Moreover, the summation strategies we have revealed may benefit manmade vision systems optimized for variable light levels [21].