Abstract
Until the 1990s, the notion of brain lateralization—the division of labor between the two hemispheres—and its more visible behavioral manifestation, handedness, remained fiercely defined as a human specific trait. Since then, many studies have evidenced lateralized functions in a wide range of species, including both vertebrates and invertebrates. In this review, we highlight the great contribution of comparative research to the understanding of human handedness’ evolutionary and developmental pathways, by distinguishing animal forelimb asymmetries for functionally different actions—i.e., potentially depending on different hemispheric specializations. Firstly, lateralization for the manipulation of inanimate objects has been associated with genetic and ontogenetic factors, with specific brain regions’ activity, and with morphological limb specializations. These could have emerged under selective pressures notably related to the animal locomotion and social styles. Secondly, lateralization for actions directed to living targets (to self or conspecifics) seems to be in relationship with the brain lateralization for emotion processing. Thirdly, findings on primates’ hand preferences for communicative gestures accounts for a link between gestural laterality and a left-hemispheric specialization for intentional communication and language. Throughout this review, we highlight the value of functional neuroimaging and developmental approaches to shed light on the mechanisms underlying human handedness.
Highlights
Humans exhibit a strong right hand preference for manual actions, which is consistently observed across tasks at the population-level and is so referred as “handedness” [1,2].Recent meta-analyses assessed more precisely the strong manual bias observed for manipulating items and for different manual tasks
We present the results of studies conducted in a wide variety of species that allow us to discuss the potential mechanisms underlying human handedness by identifying three categories of “manual” actions: (1) towards inanimate targets, (2) towards animate targets—that may involve emotion processing, and (3) communicative gestures—involving language-related functions
A difference in hand preference between unimanual interactions with inanimate targets and physical contacts made toward a conspecific has been reported in ape species-chimpanzees and gorillas: in the two studies conducted by Forrester et al [136,137], while a group-level right hand preference for interaction with inanimate targets was confirmed in these species, no right-handed bias was reported toward conspecifics, further suggesting that manual lateralization reflects right- or left hemisphere processing according to the emotive or functional characteristics of the target
Summary
Humans exhibit a strong right hand preference for manual actions, which is consistently observed across tasks at the population-level and is so referred as “handedness” [1,2]. Criteria for certain categories of the population (e.g., elite athletes), as highlighted in the five meta-analyses run by Papadatou-Pastou et al [6] Even if this manual bias exhibited for reaching, grasping, and manipulating objects or even interacting and communicating with conspecifics is being better assessed, the mechanisms underlying human handedness are still widely debated on both theoretical and empirical grounds. The large corpus of studies on this topic suggests that, besides genetic factors, non-genetic environmental factors play a significant role and need further considerations [7,8,9] The presence of such a population-level right-side bias (i.e., similar proportions) has been demonstrated in hominin species prior to Homo sapiens, namely in Homo neanderthalensis [10]; as evidence of this, previous studies investigated asymmetric morphological traits of the fossil record like asymmetries in the humeral shape or dental striations, and asymmetrical retouch patterns on Paleolithic artifacts (i.e., when producing stone or bone tools [11]). Recent studies have further considered that—besides adaptive explanations—the acquisition of handedness may be related to variations in developmental trajectories in other traits across ontogeny
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