Early visual experience influences behavioral lateralization in the guppy

Abstract

Individual differences in lateralization of cognitive functions characterize both humans and non-human species. Genetic factors can account for only a fraction of the variance observed and the source of individual variation in laterality remains in large part elusive. Various environmental factors have been suggested to modulate the development of lateralization, including asymmetrical stimulation of the sensory system during ontogeny. In this study, we raised newborn guppies in an asymmetric environment to test the hypothesis that early left–right asymmetries in visual input may affect the development of cerebral asymmetries. Each fish was raised in an impoverished environment but could voluntarily observe a complex scene in a nearby compartment containing a group of conspecifics. Using asymmetric structures, we allowed some subjects to observe the complex scene with the right eye, others with the left eye, and control fish with both eyes. Among asymmetrically stimulated fish, the mirror test revealed eye dominance congruent with the direction of asymmetric stimulation, while controls showed no left–right laterality bias. Interestingly, asymmetric exposure to social stimuli also affected another aspect of visual lateralization—eye preference for scrutinizing a potential predator—but did not influence a measure of motor asymmetry. As the natural environment of guppies is fundamentally asymmetrical, we suggest that unequal left–right stimulation is a common occurrence in developing guppies and may represent a primary source of individual variation in lateralization as well as an efficient mechanism for producing laterality phenotypes that are adapted to local environmental conditions.