General principles in motion vision: Color blindness of object motion depends on pattern velocity in honeybee and goldfish

Abstract

Visual systems can undergo striking adaptations to specific visual environments during evolution, but they can also be very "conservative." This seems to be the case in motion vision, which is surprisingly similar in species as distant as honeybee and goldfish. In both visual systems, motion vision measured with the optomotor response is color blind and mediated by one photoreceptor type only. Here, we ask whether this is also the case if the moving stimulus is restricted to a small part of the visual field, and test what influence velocity may have on chromatic motion perception. Honeybees were trained to discriminate between clockwise- and counterclockwise-rotating sector disks. Six types of disk stimuli differing in green receptor contrast were tested using three different rotational velocities. When green receptor contrast was at a minimum, bees were able to discriminate rotation directions with all colored disks at slow velocities of 6 and 12 Hz contrast frequency but not with a relatively high velocity of 24 Hz. In the goldfish experiment, the animals were trained to detect a moving red or blue disk presented in a green surround. Discrimination ability between this stimulus and a homogenous green background was poor when the M-cone type was not or only slightly modulated considering high stimulus velocity (7 cm/s). However, discrimination was improved with slower stimulus velocities (4 and 2 cm/s). These behavioral results indicate that there is potentially an object motion system in both honeybee and goldfish, which is able to incorporate color information at relatively low velocities but is color blind with higher speed. We thus propose that both honeybees and goldfish have multiple subsystems of object motion, which include achromatic as well as chromatic processing.