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Handedness and White Matter Networks NROXXX10.1177/1073858420937657The NeuroscientistBudisavljevic et al. 937657review-article2020 Review The Neuroscientist 2021, Vol. 27(1) 88 –103 Handedness and White Matter Networks © The Author(s) 2020 Article reuse guidelines: sagepub.com/journals-permissions DOI:https://doi.org/10.1177/1073858420937657 10.1177/1073858420937657 journals.sagepub.com/home/nro Sanja Budisavljevic1,2, Umberto Castiello1 , and Chiara Begliomini1 Abstract The development and persistence of laterality is a key feature of human motor behavior, with the asymmetry of hand use being the most prominent. The idea that asymmetrical functions of the hands reflect asymmetries in terms of structural and functional brain organization has been tested many times. However, despite advances in laterality research and increased understanding of this population-level bias, the neural basis of handedness remains elusive. Recent developments in diffusion magnetic resonance imaging enabled the exploration of lateralized motor behavior also in terms of white matter and connectional neuroanatomy. Despite incomplete and partly inconsistent evidence, structural connectivity of both intrahemispheric and interhemispheric white matter seems to differ between left and right-handers. Handedness was related to asymmetry of intrahemispheric pathways important for visuomotor and visuospatial processing (superior longitudinal fasciculus), but not to projection tracts supporting motor execution (corticospinal tract). Moreover, the interindividual variability of the main commissural pathway corpus callosum seems to be associated with handedness. The review highlights the importance of exploring new avenues for the study of handedness and presents the latest state of knowledge that can be used to guide future neuroscientific and genetic research. Keywords handedness, white matter, diffusion imaging, tractography, corpus callosum, corticospinal tract, superior longitudinal fasciculus Introduction dominant for hand control. However, the erroneous idea that left-handers have very different underlying neural Lateralized motor behavior represents the key feature of asymmetries, which could increase the variance in data, our daily life. In behavioral terms motor asymmetries are led to their unfortunate exclusion from many research exemplified at the level of hand and feet as well as eye studies (Willems and others 2014). A majority of left- dominance. Among these the most researched and most handed individuals have typical functional hemispheric prominent example of lateralization is the asymmetrical lateralization, and only a small minority presents with a hand use, also known as handedness (McManus 2009, reversed or atypical hemispheric dominance for lan- 2019). Handedness can be classified in terms of hand pref- guage, praxis, spatial attention, face recognition or pros- erence or hand performance, depending on the tests and ody (for a review, see Vingerhoets 2019). measures used (Box 1). Regardless of taxonomy, studies Handedness is thought to either result from or to tend to converge toward similar figures and frequencies. induce asymmetries in the functional and structural orga- Thus, most adults (around 90%) prefer to use their right nization of the human brain (Toga and Thompson 2003; hand over the left for most types of hand movements Vingerhoets 2019). Whether it is handedness or HS that (Papadatou-Pastou and others 2020; Porac and Coren came first is a matter of debate, since a point-to-point 1981), with numbers varying according to the geographi- mapping across developmental stages remains a chal- cal location (Raymond and Pontier 2004). The remaining lenge (Andersen and Siebner 2018; Buckingham and 10% consist of ambidextrous and left-handed individuals. Although the two cerebral hemispheres, just like our 1Department of General Psychology, University of Padova, Padova, two hands, seem identical at first, they show both func- Italy tional and structural hemispheric asymmetries (Box 2). 2The School of Medicine, University of St. Andrews, St. Andrews, UK This phenomenon, termed hemispheric specialization Corresponding Author: (HS), has long been thought of as a division of labor Sanja Budisavljevic, The School of Medicine, University of St. Andrews, (Vingerhoets 2019). Handedness is intimately linked to North Haugh, St Andrews KY16 9TF, United Kingdom. the notion of HS and the fact that one hemisphere seems Email: [email protected] Budisavljevic et al. 89 Box 1. Short Summary of Handedness Classification. Hand preference denotes a tendency of one hand to play a leading, manipulative role (e.g., rubbing a matchstick on the side of the matchbox or opening a jar lid) while the other hand plays a supporting, stabilizing role (e.g., holding the matchbox or the jar firmly). Hand preference can vary along two dimensions: direction (right-handedness vs. left-handedness) and degree (pure/consistent handedness vs. mixed/inconsistent handedness). It is usually assessed via experimental manipulation tasks (for infants/children) or self- reported questionnaires made by items describing everyday habits, unimanual and bimanual (for adults). The Edinburgh Handedness Questionnaire (Oldfield 1971) is the most popular assessment tool, resulting in a laterality quotient expressing the strength of the bias toward right- or left-handedness. Hand performance (also referred to as hand proficiency, manual dexterity, relative hand skill) can be assessed with motor performance tasks, such as the Annett pegboard (Annett 1970), rapid tapping (Peters 1980; Peters and Durding 1978), circle-marking (Tapley and Bryden 1985), and kinematical tasks (Begliomini and others 2008). Hand preference correlates reliably, but not perfectly, with hand performance (Todor and Doane 1977), highlighting the importance of using both measures when assessing asymmetrical hand use (Henkel and others 2001). Carey 2015). Some insights emerged from fetal ultra- and others 2011b; Fig. 1). Literature on gray matter asym- sound and gene expression studies: the right-side handed- metries and handedness reveals a plethora of equivocal ness bias was observed as early as 10 weeks gestation, or findings, and these will be briefly mentioned in the rele- as soon as fetus starts to independently move its arms (for vant sections. In general, large-scale studies using auto- a review, see Hepper 2013). This behavior was noted mated parcellation methods reported that handedness had before the maturation of the main central motor pathway, little to do with gray matter asymmetries in terms of cor- the corticospinal tract (ten Donkelaar and others 2004), tical volume, cortical thickness, surface area, and sulcal and the gene expression asymmetries in cerebral hemi- depth (Kong and others 2018, Maingault and others spheres (12 weeks of gestation; Sun and others 2005), but 2016). However, associations with handedness did some- occured around the same time as differential gene expres- times appear by lowering statistical thresholds (Guadalupe sion in the left and right segments of the spinal cord (i.e., and others 2014; Maingault and others 2016) or by using 10 weeks of gestation; Ocklenburg and others 2017). the manual gray matter parcellation approach that takes The prenatal asymmetry of hand use was found to be a into account the local brain morphology (Germann and precursor of postnatal handedness in terms of direction others 2019). (Hepper and others 2005; Parma and others 2017) but not The white matter and handedness exploration gained degree, which stabilizes only in mid-childhood (McManus momentum when the invasive “gold standard” postmor- and others 1988). The phenotypic plasticity supports the tem approach was complemented by diffusion MRI. This notion of bidirectional influence across ontogeny—the is a noninvasive, fast, repeatable, whole-brain technique neural traits influencing handedness and vice versa. This that can be used across large samples and combined with reciprocity is supported by studies showing that handed- other MRI modalities to produce blueprints of “structural ness shifts can modulate brain asymmetries (Marcori and connectivity.” The importance of studying structural con- Okazaki 2020; Marcori and others 2019; Sun and others nectivity is highlighted by a networked nature of the brain 2012) but also by studies reporting that lesions altering and the importance of interacting brain regions for brain brain structure can produce shifts in hand selection function (ffytche and Catani 2005). Up to date, both inter- (Howells and others 2020). It is in light of such bidirec- hemispheric and intrahemispheric connections have been tionality that discussion on the brain asymmetries and implicated as important factors in shaping HS (Ocklenburg handedness should be viewed. and others 2016a; Stephan and others 2007; Tzourio- Recent advances in neuroimaging methods allowed Mazoyer 2016), and hence potential neural substrates for for the measurement and the visualization of both func- lateralized motor behavior. As more and more articles tional and structural asymmetries of the human brain using various neuroimaging methods are published on (Box 2). Although anatomical factors are crucial in mod- handedness and HS, the laterality research pendulum is ulating brain’s functional organization (Rockland 2020), swinging toward the need to integrate this different infor- the relationship between the functional and structural mation. The present review aims to synthesize the current asymmetries is weak due to the absence of one-to-one
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