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.

An Integrative Framework for the Appraisal of Coloration in Nature

“…This has provided a guiding framework for the comparative investigation of visual perception in nonhuman animals. However, the complexities of color perception have been elucidated for very few nonhuman model systems, including primates (Osorio et al 2004), goldfish (Neumeyer 1992;Gehres and Neumeyer 2007;Stojcev et al 2011), bees (von Helverson 1972Backhaus 1991;Chittka and Menzel 1992;Giurfa et al 1997;Dyer et al 2011;Dyer 2012;de Ibarra et al 2014), pigeons, and chickens (Bowmaker 1977;Bowmaker and Knowles 1977;Okano et al 1992). The sum of this work offers two important conclusions.…”

“…Analysis of achromatic information is relatively more straightforward and can be achieved by integrating across entire spectral curves or across wavelength intervals of specific interest (e.g., Andersson et al 1998;Kemp and Rutowski 2007). However, biological inference will again be limited by knowledge about how achromatic information is received and processed by the viewer(s) of interest (e.g., Schaerer and Neumeyer 1996;Lind and Kelber 2011;Stojcev et al 2011;Zhou et al 2012;Lind et al 2013). At a minimum, knowledge of the spectral range or function of achromatic sensitivity in viewers will be useful to guide how to best summarize achromatic information (see, e.g., Prudic et al 2007).…”

Spectral inputs and ocellar contributions to a pitch-sensitive descending neuron in the honeybee

“…Paulk et al (2008) showed that in bumblebees, some lobula cells were sensitive to both color and motion, which suggested that although the motion and color information pathways are initially segregated, they converge on the higher order neurons. In honeybees, the convergence of the motion and color information pathways was also proved by behavioral experiments (Stojcev et al 2011;Zhang et al 1995).…”

Honeybees (Apis mellifera) Learn Color Discriminations via Differential Conditioning Independent of Long Wavelength (Green) Photoreceptor Modulation

“…Thus, the “UV” and “blue” photoreceptor outputs project directly to the second optic ganglia of the bee brain (the outer medulla) [27]; [28], while the ‘green’ photoreceptor signal is initially processed in the first optic ganglia (the lamina) [29]–[31]. Furthermore, behavioural experiments have shown that modulation of the ‘green’ photoreceptor is responsible for stimulus detection at small visual angles [24]; [32]; [33], broad field motion processing (as measured with the optomotor response) [34], small field motion detection at high frequencies [35]; [36], and some complex pattern recognition tasks, which can be learned only through differential conditioning [37].…”