Abstract
The alignment of visceral and brain asymmetry observed in some vertebrate species raises the question of whether this association also exists in humans. While the visceral and brain systems may have developed asymmetry for different reasons, basic visceral left–right differentiation mechanisms could have been duplicated to establish brain asymmetry. We describe the main phenotypical anomalies and the general mechanism of left–right differentiation of vertebrate visceral and brain laterality. Next, we systematically review the available human studies that explored the prevalence of atypical behavioral and brain asymmetry in visceral situs anomalies, which almost exclusively involved participants with the mirrored visceral organization (situs inversus). The data show no direct link between human visceral and brain functional laterality as most participants with situs inversus show the typical population bias for handedness and brain functional asymmetry, although an increased prevalence of functional crowding may be present. At the same time, several independent studies present evidence for a possible relation between situs inversus and the gross morphological asymmetry of the brain torque with potential differences between subtypes of situs inversus with ciliary and non-ciliary etiologies.
Highlights
Vertebrates’ visceral and central nervous systems demonstrate a strikingly asymmetric organization with a strong population bias toward a prototypical left–right configuration [1,2]. As both systems serve fundamentally different biological functions, it seems plausible to assume that the reasons behind their asymmetry may be entirely different and that their left–right differentiation evolved independently. While this may be true, it does not preclude the possibility that basic mechanisms for establishing left–right differentiation of the viscera have been reused to establish central nervous system laterality and that there may be a link between both manifestations of asymmetry
In the absence of striking relations, small samples limit the statistical power to detect more subtle differences between typical and atypical groups in particular when only a subsample of participants shows a relation and others do not. This brings us to the second limitation of this approach, the heterogeneity of factors that contribute to brain and visceral asymmetries
Two broad categories of anomalies are generally distinguished, situs inversus characterized by a complete or near-complete mirror reversal of typical visceral asymmetry, and heterotaxy described as a duplication of one of either asymmetric sides
Summary
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. Vertebrates’ visceral and central nervous systems demonstrate a strikingly asymmetric organization with a strong population bias toward a prototypical left–right configuration [1,2] As both systems serve fundamentally different biological functions, it seems plausible to assume that the reasons behind their asymmetry may be entirely different and that their left–right differentiation evolved independently. The typical asymmetrical position of the internal organs in vertebrates is an example of directional asymmetry, and the equal number of male fiddler crabs with a larger left or right claw is the prototypical example of antisymmetry The latter two types of asymmetry have been proposed as informative traits to investigate evolution mechanisms as they are easy to define, easy to compare, and have evolved multiple times independently [9]. A comparison of the key nodal cascade genes in lower chordates and vertebrates surprisingly suggests that the ancestral target of the nodal cascade might have been brain asymmetry [9]
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