Adaptive plasticity during the development of colour vision.
Colour vision greatly enhances the discriminatory and cognitive capabilities of visual systems and is found in a great majority of vertebrates and many invertebrates. However, colour coding visual systems are confronted with the fact that the external stimuli are ambiguous because they are subject to constant variations of luminance and spectral composition. Furthermore, the transmittance of the ocular media, the spectral sensitivity of visual pigments and the ratio of spectral cone types are also variable. This results in a situation where there is no fixed relationship between a stimulus and a colour percept. Colour constancy has been identified as a powerful mechanism to deal with this set of problems; however, it is active only in a short-term time range. Changes covering longer periods of time require additional tuning mechanisms at the photoreceptor level or at postreceptoral stages of chromatic processing. We have used the trichromatic blue acara (Aequidens pulcher, Cichlidae) as a model system and studied retinal morphology and physiology, and visually evoked behaviour after rearing fish for 1-2 years under various conditions including near monochromatic lights (spectral deprivation) and two intensities of white light (controls). In general, long-term exposure to long wavelengths light had lesser effects than light of middle and short wavelengths. Within the cone photoreceptors, spectral deprivation did not change the absorption characteristics of the visual pigments. By contrast, the outer segment length of middle and long-wave-sensitive cones was markedly increased in the blue rearing group. Furthermore, in the same group, we observed a loss of 65% short-wave-sensitive cones after 2 years. These changes may be interpreted as manifestations of compensatory mechanisms aimed at restoring the balance between the chromatic channels. At the horizontal cell level, the connectivity between short-wave-sensitive cones and the H2 cone horizontal cells, and the spinule dynamics were both affected in the blue light group. This observation rules out the role of spinules as sites of chromatic feedback synapses. The light-evoked responses of H2 horizontal cells were also sensitive to spectral deprivation showing a shift of the neutral point towards short wavelengths in the blue rearing group. Interestingly, we also found an intensity effect because in the group reared in bright white light the neutral point was more towards longer wavelength than in the dim light group. Like the changes in the cones, the reactions of horizontal cells to spectral deprivation in the long wave domain can be characterised as compensatory. We also tested the spectral sensitivity of the various experimental groups of blue acara in visually evoked behaviour using the optomotor response paradigm. In this case, the changes in the relative spectral sensitivity were more complex and could not be explained by a simple extrapolation of the adaptive and compensatory processes in the outer retina. We conclude that the inner retina, and/or the optic tectum are also involved and react to the changes of the spectral environment. In summary, we have shown a considerable developmental plasticity in the colour vision system of the blue acara, where epigenetic adaptive processes at various levels of the visual system respond to the specific spectral composition of the surroundings and provide a powerful mechanism to ensure functional colour vision in different visual environments. We suggest that processes involving an active fine-tuning of the photoreceptors and the postreceptoral processing of chromatic information during ontogenetic development are a general feature of all colour vision systems. Such mechanisms would establish a functional balance between the various chromatic channels. This appears to be an essential condition for the cognitive systems to extract the relevant and stable information from the unstable and changing stimulus situation.
Wagner
Hans-Joachim
HJ
Eberhard-Karls Universität Tübingen, Graduate School of Neural and Behavioural Sciences and Max Planck Research School, Anatomisches Institut, Osterbergstrasse 3, 72074 Tübingen, Germany. hjwagner@anatu.uni-tuebingen.de
Kröger
Ronald H H
RH
D000221:Adaptation, Ocular / Q000502:physiology*; D000818:Animals; D023681:Cichlids / Q000502:physiology; D003118:Color Perception / Q000502:physiology*; D006801:Humans; D009473:Neuronal Plasticity / Q000502:physiology*