title: An Evolutionary Hypothesis of Binary Opposition in Functional Incompatibility about Habenular Asymmetry in Vertebrates.
abstract: Many vertebrates have asymmetrical circuits in the nervous system. There are two types of circuit asymmetry. Asymmetrical circuits in sensory and/or motor systems are usually related to lateralized behaviors. It has been hypothesized that spatial asymmetry in the environment and/or social interactions has led to the evolution of asymmetrical circuits by natural selection. There are also asymmetrical circuits that are not related to lateralized behaviors. These circuits lie outside of the sensory and motor systems. A typical example is found in the habenula (Hb), which has long been known to be asymmetrical in many vertebrates, but has no remarkable relationship to lateralized behaviors. Instead, the Hb is a hub wherein information conveyed to the unilateral Hb is relayed to diverging bilateral nuclei, which is unlikely to lead to lateralized behavior. Until now, there has been no hypothesis regarding the evolution of Hb asymmetry. Here, we propose a new hypothesis that binary opposition in functional incompatibility applies selection pressure on the habenular circuit and leads to asymmetry. Segregation of the incompatible functions on either side of the habenula is likely to enhance information processing ability via creating shorter circuits and reducing the cost of circuit duplication, resulting in benefits for survival. In zebrafish and mice, different evolutionary strategies are thought to be involved in Hb asymmetry. In zebrafish, which use a strategy of structurally fixed asymmetry, the asymmetrical dorsal Hb leads to constant behavioral choices in binary opposition. In contrast, in mice, which use a strategy of functionally flexible lateralization, the symmetrical lateral Hb is functionally lateralized. This makes it possible to process complicated information and to come to variable behavioral choices, depending on the specific situation. These strategies are thought to be selected for and preserved by evolution under selection pressures of rigidity and flexibility of sociability in zebrafish and mice, respectively, as they are beneficial for survival. This hypothesis is highly valuable because it explains how the Hb evolved differently in terms of asymmetry and lateralization among different species. In addition, one can propose possible experiments for the verification of this hypothesis in future research.
authors.affiliation: Department of Anatomy and Neuroscience, Graduate School of Medicine and Pharmaceutical Sciences, University of Toyama Toyama, Japan.
authors.forename: Hiroyuki
authors.initials: H
authors.lastname: Ichijo
authors.affiliation: Department of Anatomy and Neuroscience, Graduate School of Medicine and Pharmaceutical Sciences, University of Toyama Toyama, Japan.
authors.forename: Tomoya
authors.initials: T
authors.lastname: Nakamura
authors.affiliation: Department of Anatomy and Neuroscience, Graduate School of Medicine and Pharmaceutical Sciences, University of Toyama Toyama, Japan.
authors.forename: Masahumi
authors.initials: M
authors.lastname: Kawaguchi
authors.affiliation: Department of Anatomy and Neuroscience, Graduate School of Medicine and Pharmaceutical Sciences, University of Toyama Toyama, Japan.
authors.forename: Yuichi
authors.initials: Y
authors.lastname: Takeuchi
keywords: asymmetry; habenula; lateralization; mouse; natural selection; scale-eating; zebrafish