Research report
Roots of brain specializations: preferential left-eye use during mirror-image inspection in six species of teleost fish

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Abstract

It has recently been reported that predator inspection is more likely to occur when a companion (i.e. the mirror image of the test animal) is visible on the left rather than on the right side of mosquitofish Gambusia holbrooki. This very unexpected outcome could be consistent with the hypothesis of a preferential use of the right eye during sustained fixation of a predator as well as of a preferential use of the left eye during fixation of conspecifics. We measured the time spent in monocular viewing during inspection of their own mirror images in females of six species of fish, belonging to different families—G. holbrooki, Xenotoca eiseni, Phoxinus phoxinus, Pterophyllum scalare, Xenopoecilus sarasinorum, and Trichogaster trichopterus. Results revealed a consistent left-eye preference during sustained fixation in all of the five species. Males of G. holbrooki, which do not normally show any social behaviour, did not exhibit any eye preferences during mirror-image inspection. We found, however, that they could be induced to manifest a left-eye preference, likewise females, if tested soon after capture, when some affiliative tendencies can be observed. These findings add to current evidence in a variety of vertebrate species for preferential involvement of structures located in the right side of the brain in response to the viewing of conspecifics.

Introduction

The different involvement of the right and left side of the brain (lateralization) in a variety of cognitive and emotional functions has long been considered unique to the human species. In the last few years, however, we have come to realize that the origins of brain lateralization should be traced down to the most ancient past of vertebrates. Apart from birds and mammals, for whom a large body of evidence was already available [9], more recently data have been progressively accumulating for the presence of a variety of structural and functional asymmetries among fishes, amphibians and reptiles [6].

An aspect of lateralization in non-mammal species is the presence of systematic preferences in eye use. This is particularly clear in birds, fishes and reptiles, which have laterally placed eyes and complete decussation at the optic chiasma, but it has also been demonstrated in animals with larger binocular overlap, such as toads, at least for the most lateral parts of their visual fields [33]. Unlike those perceptual asymmetries observed in humans and other primates under very unnatural testing conditions, such as tachistoscopic viewing or dichotic listening, preferences in eye use are evident (actually quite ubiquitous) in the everyday behaviour of animals with laterally placed eyes and deeply influence their social interactions. One noteworthy example is provided by a recent study investigating predator-inspection responses in the mosquitofish Gambusia holbrooki [3].

The use of a mirror image was introduced by behavioural ecologists [21] as an experimental method to test the hypothesis that fish would be more likely to show predator-inspection responses when sharing with a social partner (the mirror reflection) the risk of being predated upon. Surprisingly, we found that predator inspection is more likely to occur when the mirror image is visible on the left rather than on the right side of mosquitofish [3]. The most likely explanation for this asymmetry is that mosquitofish tend to use the lateral (monocular) parts of their right and left visual fields for different purposes. In fact, when faced with a vertical-bar barrier through which a biologically-relevant target was visible, female mosquitofish showed a consistent bias to turn towards the left when the target was a predator and towards the right when the target was a group of conspecifics of the same sex [4], [5], [8]. Interestingly, this rightward bias was evident in females but not in males. Motor asymmetries related to the so-called C-start reaction (a C-shaped bending of the fish’s body which initiates a fast turn away from a predator or other noxious stimulus; [10]) are likely to play a part in detour responses to predators [11]. The C-start reaction is mediated by the Mauthner cells, a pair of giant reticulospinal neurons, and evidence for disproportionately larger Mauthner cells in the left than in the right brain stem has been reported for the goldfish [22]. However, direct evidence for asymmetries in eye use which depend on the type of stimulus to be scrutinized have been reported by Miklosi et al. [20] for zebrafish (Brachidanio rerio). Moreover, evidences that asymmetries in the detour test depend, at least in part, on asymmetries in eye use have recently been provided. Measurements of the angle of viewing in the fish Girardinus falcatus revealed that those animals which tended to detour the barrier on the left side used the right eye to scrutinise a dummy predator and the left eye to scrutinise a neutral stimulus, whereas those animals which tended to detour the barrier on the right side showed the reverse pattern of eye use; fish that did not show any consistent bias in the detour test did not reveal any significant preference in the viewing test [14].

Considering that during predator-inspection tests mosquitofish typically swam very close to the mirror, it seems likely that positioning the mirror on the left side produced the best arrangement of lateral (monocular) stimulation, with the right eye fixating the predator and the left eye monitoring the companion. However, no data to disentangle the roles played by right-eye use in fixation of the predator and (possibly) left-eye use in fixation of the companion are available; in principle, either of the two effects would suffice for producing the reported asymmetry.

The aim of our first experiment was thus to verify whether in the absence of any confounding factor related to predator-inspection responses, a preferential use of the left eye during sustained viewing of their mirror images could be observed in fish.

Section snippets

Experiment 1

Two species of fish belonging to the same Order (Cyprinodontiformes) were used, G. hoolbroki (the species already used in the detour test and in the predator-inspection test in presence of a mirror) and Xenotoca eiseni.

The eastern mosquitofish, G. holbrooki (Family Poeciliidae) is a small livebearing fish native of North America and introduced in Europe at the beginning of this century. X. eiseni (Family Goodeidae) is a livebearing fish native of Mesa Central plateau of Mexico.

As mentioned

Experiment 2

Comparative work using the detour test has revealed that inspection responses to a dummy predator were lateralized in a variety of species of fish [5], [7]. The direction of lateralization tends to be the same within the most closely related species but could vary between phylogenetically-unrelated species [7]. The two species employed in Exp. 1 showed lateralization in the same direction; they belong to different families (Poeciliidae and Goodeidae) but to the same order (Cyprinodontiformes).

General discussion

Six species of fish, some of which were phylogenetically very disparate, showed an identical pattern of eye lateralization during inspection of their mirror images, namely a consistent preference for using the left eye. In fish, optic nerve axons, originating in retinal ganglion cells, cross completely at the optic chiasm. Visual fibres from each eye project mainly to the optic tectum (actually, other distinct nuclear groups, nucleus geniculatus lateralis, nucleus praetectalis and nucleus

Acknowledgements

We wish to thank Lucia Regolin for thoughtful comments on the manuscript. The research was funded by Italian MURST 40% and 60% grants.

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