The costs of hemispheric specialization in a fish

Abstract

Laboratory and field studies have documented better cognitive performance associated with marked hemispheric specialization in organisms as diverse as chimpanzees, domestic chicks and topminnows. While providing an evolutionary explanation for the emergence of cerebral lateralization, this evidence represents a paradox because a large proportion of non-lateralized (NL) individuals is commonly observed in animal populations. Hemispheric specialization often determines large left-right differences in perceiving and responding to stimuli. Using topminnows selected for a high or low degree of lateralization, we tested the hypothesis that individuals with greater functional asymmetry pay a higher performance cost in situations requiring matching information from the two eyes. When trained to use the middle door in a row of a nine, NL fish correctly chose the central door in most cases, while lateralized fish showed systematic leftward or rightward biases. When choosing between two shoals, each seen with a different eye, NL fish chose the high-quality shoal significantly more often than the lateralized fish, whose performance was affected by eye preference for analysing social stimuli. These findings suggest the existence of a trade-off between computational advantages of hemispheric specialization and the ecological cost of making suboptimal decisions whenever relevant information is located on both sides of the body.

Figure 1.

(a) Apparatus used in the bisectioning task. (b) Subjects were required to use the middle door in a row of nine.

Figure 2.

(a) Apparatus used in the bilateral information processing task. (b) Once outside the small corridor, the focal female simultaneously saw two stimulus shoals, each visible in a different visual hemifield.

Figure 3.

Proportion of correct choices (mean ± s.e.) of central door during the six trials of the bisectioning task in lateralized and NL topminnows. Filled circles, lateralized; open circles, non-lateralized.

Figure 4.

Bilateral information processing task. Lateralized and NL topminnows were given the choice between two different social groups each seen by a different eye. Bars represent the number of individuals choosing the normally preferred shoal in both trials, in one trial or in none. In variant A, the choice was between four (preferred stimulus) and two females. In variant B, the choice was between similar-sized (preferred stimulus) and smaller females. Black bars, variant A; white bars, variant B.