Dichromatic Colour Vision in Wallabies as Characterised by Three Behavioural Paradigms

Despite lacking genetic evidence of a third cone opsin in the retina of any Australian marsupial, most species tested so far appear to be trichromatic. In the light of this, we have re-examined colour vision of the tammar wallaby which had previously been identified as a dichromat. Three different psychophysical tests, based on an operant conditioning paradigm, were used to confirm that colour perception in the wallaby can be predicted and conclusively explained by the existence of only two cone types. Firstly, colour-mixing experiments revealed a Confusion Point between the three primary colours of a LCD monitor that can be predicted by the cone excitation ratio of the short- and middle-wavelength sensitive cones. Secondly, the wavelength discrimination ability in the wallaby, when tested with monochromatic stimuli, was found to be limited to a narrow range between 440 nm and 500 nm. Lastly, an experiment designed to test the wallaby’s ability to discriminate monochromatic lights from a white light provided clear evidence for a Neutral Point around 485 nm where discrimination consistently failed. Relative colour discrimination seemed clearly preferred but it was possible to train a wallaby to perform absolute colour discriminations. The results confirm the tammar wallaby as a dichromat, and so far the only behaviourally confirmed dichromat among the Australian marsupials

Diversity of Color Vision: Not All Australian Marsupials Are Trichromatic

Color vision in marsupials has recently emerged as a particularly interesting case among mammals. It appears that there are both dichromats and trichromats among closely related species. In contrast to primates, marsupials seem to have evolved a different type of trichromacy that is not linked to the X-chromosome. Based on microspectrophotometry and retinal whole-mount immunohistochemistry, four trichromatic marsupial species have been described: quokka, quenda, honey possum, and fat-tailed dunnart. It has, however, been impossible to identify the photopigment of the third cone type, and genetically, all evidence so far suggests that all marsupials are dichromatic. The tammar wallaby is the only Australian marsupial to date for which there is no evidence of a third cone type. To clarify whether the wallaby is indeed a dichromat or trichromatic like other Australian marsupials, we analyzed the number of cone types in the “dichromatic” wallaby and the “trichromatic” dunnart. Employing identical immunohistochemical protocols, we confirmed that the wallaby has only two cone types, whereas 20–25% of cones remained unlabeled by S- and LM-opsin antibodies in the dunnart retina. In addition, we found no evidence to support the hypothesis that the rod photopigment (rod opsin) is expressed in cones which would have explained the absence of a third cone opsin gene. Our study is the first comprehensive and quantitative account of color vision in Australian marsupials where we now know that an unexpected diversity of different color vision systems appears to have evolved

Perturbation of leg protraction causes context-dependent modulation of inter-leg coordination, but not of avoidance reflexes

All animals capable of legged locomotion execute fast, adaptive compensatory movements in response to perturbation of a step cycle. In terms of motor control, such adaptive behaviour typically involves changes in the kinematics of the perturbed limb as well as changes in coordination between legs. Moreover, the unpredictable variety of real life situations implies that compensatory responses should be sensitive to the behavioural context of the animal. We have investigated the extent to which the compensatory response of a walking stick insect (Carausius morosus) adapts in parallel to strong context-dependent adaptation of step kinematics and inter-leg coordination. The behavioural contexts we chose were straight walking and visually induced curve walking, for both of which the steady state limb kinematics and inter-leg coupling strengths were known. In case of curve walking, we further distinguished contexts according to whether the inner or the outer leg was perturbed. The three contexts differed strongly with respect to the set of joint actions before perturbation. Upon mechanical perturbation of front leg protraction, we studied context-dependent differences in a local avoidance reflex of the perturbed leg, as well as in coordination mechanisms that couple the step cycles of the perturbed leg to its unperturbed neighbours. In all three walking contexts, obstacle contact caused an avoidance movement of the front leg that deviated from the unperturbed swing trajectory. Swing duration was increased while step distance was decreased; however, both effects vanished in the subsequent unperturbed step. The prevailing immediate reaction of the three leg joints were retraction of the coxa (>76%), levation of the femur (>80%), and flexion of the tibia (>80%), regardless of the behavioural context and, therefore, joint action prior to perturbation. Moreover, activation of each one of these joint actions was shown to be independent of the other two. Thus, local avoidance reflexes are not modulated by the descending visual information that causes transition from straight to curve walking, but are composed of context-independent joint actions. Perturbation of the front leg also caused significant shifts of the touch-down position of the perturbed leg and of its unperturbed neighbours. If the inner front leg was perturbed, this shift could persist until the subsequent step. Perturbation affected both the spatial location and the timing of touch-down and lift-off transitions in unperturbed neighbouring legs. These effects on inter-leg coordination were context-dependent. For example, time delay to lift-off of the contralateral neighbour was shortened in inner and straight walking legs, but not in outer legs. Finally, a targeting mechanism that determines foot placement in stick insects was shown to be affected by perturbation in a context-dependent manner. We conclude that the immediate compensatory response of the perturbed leg is not adapted to the behavioural context in spite of strongly differing step kinematics, whereas the compensatory effect on inter-limb coupling is context-dependent

Perturbation of leg protraction causes context-dependent modulation of inter-leg coordination, but not of avoidance reflexes

Ebeling W, Dürr V. Perturbation of leg protraction causes context-dependent modulation of inter-leg coordination, but not of avoidance reflexes. J. Exp. Biol. 2006;209(11):2199-2214.All animals capable of legged locomotion execute fast, adaptive compensatory movements in response to perturbation of a step cycle. In terms of motor control, such adaptive behaviour typically involves changes in the kinematics of the perturbed limb as well as changes in coordination between legs. Moreover, the unpredictable variety of real life situations implies that compensatory responses should be sensitive to the behavioural context of the animal. We have investigated the extent to which the compensatory response of a walking stick insect (Carausius morosus) adapts in parallel to strong context-dependent adaptation of step kinematics and inter-leg coordination. The behavioural contexts we chose were straight walking and visually induced curve walking, for both of which the steady state limb kinematics and inter-leg coupling strengths were known. In case of curve walking, we further distinguished contexts according to whether the inner or the outer leg was perturbed. The three contexts differed strongly with respect to the set of joint actions before perturbation. Upon mechanical perturbation of front leg protraction, we studied context-dependent differences in a local avoidance reflex of the perturbed leg, as well as in coordination mechanisms that couple the step cycles of the perturbed leg to its unperturbed neighbours.In all three walking contexts, obstacle contact caused an avoidance movement of the front leg that deviated from the unperturbed swing trajectory. Swing duration was increased while step distance was decreased; however, both effects vanished in the subsequent unperturbed step. The prevailing immediate reaction of the three leg joints were retraction of the coxa (>76%), levation of the femur (>80%), and flexion of the tibia (>80%), regardless of the behavioural context and, therefore, joint action prior to perturbation. Moreover, activation of each one of these joint actions was shown to be independent of the other two. Thus, local avoidance reflexes are not modulated by the descending visual information that causes transition from straight to curve walking, but are composed of context-independent joint actions.Perturbation of the front leg also caused significant shifts of the touch-down position of the perturbed leg and of its unperturbed neighbours. If the inner front leg was perturbed, this shift could persist until the subsequent step. Perturbation affected both the spatial location and the timing of touch-down and lift-off transitions in unperturbed neighbouring legs. These effects on inter-leg coordination were context-dependent. For example, time delay to lift-off of the contralateral neighbour was shortened in inner and straight walking legs, but not in outer legs. Finally, a targeting mechanism that determines foot placement in stick insects was shown to be affected by perturbation in a context-dependent manner.We conclude that the immediate compensatory response of the perturbed leg is not adapted to the behavioural context in spite of strongly differing step kinematics, whereas the compensatory effect on inter-limb coupling is context-dependent

The Journal of Experimental Biology 209, 2199-2214 Published by The Company of Biologists 2006

doi:10.1242/jeb.02251 Perturbation of leg protraction causes context-dependent modulation of inter-leg coordination, but not of avoidance reflexe

The Journal of Experimental Biology 208, 2237-2252 Published by The Company of Biologists 2005

doi:10.1242/jeb.01637 The behavioural transition from straight to curve walking: kinetics of leg movement parameters and the initiation of turning The control of locomotion requires the ability to adapt movement sequences to the behavioural context of the animal. In hexapod walking, adaptive behavioural transitions require orchestration of at least 18 leg joints and twice as many muscle groups. Although kinematics of locomotion has been studied in several arthropod species and in a range of different behaviours, almost nothing is known about the transition from one behavioural state to another. Implicitly, most studies on context-dependency assume that all parameters that undergo a change during a behavioural transition do so at the same rate. The present study tests this assumption by analysing th

Minimum Delta Lambda functions for five mammalian species show differences between dichromats and trichromats.

<p>Trichromatic primates (triangles: <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0086531#pone.0086531-Jacobs2" target="_blank">[21]</a>) exhibit good colour discrimination ability across a wide wavelength range. In contrast, the data from the wallaby (crosses) much more closely match the discrimination abilities of dichromatic mammals with good performance only over a narrow range of wavelengths (squares: tree squirrel <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0086531#pone.0086531-Blakeslee1" target="_blank">[19]</a>; diamonds: dog <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0086531#pone.0086531-Neitz1" target="_blank">[20]</a>).</p

Colour-mixing experiments yielded Confusion Points for various RGB colour combinations.

<p>Choice frequencies of the reference stimulus (red in Test 1, A and D; red in Test 2, B and E; green in Test 3, C and F) are presented as a function of a gradually varied colour composition of a test stimulus (green in Test 1, A and D; blue in Test 2, B and E; blue in Test 3, C and F). (A–C) The animals’ stimulus preference reversed, intersecting the 50% mark which was defined as the Confusion Point. (D–E) Converted into excitation ratios of M/S-cones, the data reveal a match between CER for both test and reference stimulus at the Confusion Point (dashed vertical lines).</p

Wallabies readily used the automated operant conditioning setup for colour vision experiments.

<p>Light stimuli were projected onto diffuser flaps that also served as the trigger when the animal pushed to indicate a stimulus choice. If correct, a food reward was delivered into a feeder bowl under the stimuli. Photo copyright: W. Ebeling.</p