Where next for laterality research? Looking back and looking forward

ABSTRACT

While paying attention to the recommendations of Ocklenburg, Berretz, Packheiser, and Friedrich (2020) in the target article, researchers in the field of laterality should attempt to: (1) solve the long-standing puzzle of the relationship between handedness and language lateralization; (2) further explore the genetic bases of manual and cerebral asymmetry and of their associations with psychiatric and neurodevelopmental conditions; (3) explore the adaptive significance of laterality for humans and non-humans and elucidate the relationships of asymmetry across species; and (4) embrace developing technologies to investigate the interaction between the hemispheres during the performance of everyday tasks.

KEYWORDS:

• Laterality
• Handedness
• Speech dominance

We concur with the views expressed by Ocklenburg et al. (2020) in the target article. In particular, we agree that the cross-species study of laterality should be a major topic of research in the next decade. One aim might be to compare different primate species and humans, preferably from non-industrialized societies, on the same behavioural task to ascertain how manual preference and skill asymmetry vary within and between species. In addition, it would be instructive to look at task-related brain activation in different species performing the same task (Thiebaut de Schotten, Croxson, & Mars, 2019). A programme of comparative neuroimaging would help to identify the organizational principles whereby brains have adapted through convergent and divergent evolutionary processes (see Friedrich et al., 2021).

We distinguish between two classes of challenge for the future. One is to solve those long-outstanding problems that seem resistant to solution; the other is to tackle new problems arising from the development of new techniques.

Among the first category is “the puzzling relationship between language dominance and dominant hand” (Carey & Johnstone, 2014, p. 1). Estimates of the frequency of atypical (right or bilateral) speech representation as a function of handedness have varied widely (Coppens, Hungerford, Yamaguchi, & Yamadori, 2002). Two studies, each with samples of 100 or more participants (Mazoyer et al., 2014; Springer et al., 1999), reported very low incidences of right hemisphere speech. Springer et al. (1999, p. 2040) stated that “fMRI in 100 right-handed, neurologically normal individuals failed to identify a single person with clear right hemisphere dominance”, though 6% had “symmetric language representation”. Similarly, Mazoyer et al. (2014) claimed not to find a single case of right-sided speech among 144 right-handers but they too observed cases of “atypical” speech in 8 of these right-handers. They concluded that right hemisphere speech occurred only in left-handers and estimated a 0.6% prevalence for right hemisphere lateralization in the general population. Compare this with the proposal (based on consideration of the brain damage literature) that almost 10% of the general population has right cerebral dominance (Annett, 2002).

Mazoyer et al. (2014, p. 13) refer to “the dogma of the existence of a correlation between hemispheric dominance for language and handedness”. They point out that the prevalence of right-handedness is approximately 90%, as is the prevalence of left hemisphere speech. As a result, a close correspondence between the two is to be expected by chance alone. They argue that their results (see also Packheiser et al., 2020) suggest that, if individuals with strongly atypical language lateralization are excluded, “the agreement between hemispheric dominance for hand preference and for language was barely above the chance level” (p. 8).

Does any link with language lateralization relate to degree as well as direction of handedness? Functional transcranial Doppler sonography (Knecht et al., 2000) and fMRI (Somers et al., 2015) studies have reported a relationship between direction and degree of handedness and an index of speech lateralization. However, to date, it has been difficult to investigate the distribution of laterality indices of a truly representative sample of the population within a single study.

A common procedure has been to study only right-handers (e.g., Knecht et al., 2000), only left-handers (e.g., Szaflarski et al., 2002) or to take two groups from opposite extremes of the laterality continuum (e.g., Mazoyer et al., 2014). As a consequence, individuals of intermediate hand preference, who comprise up to one-third of the population (Annett, 2002), are excluded.

Rather than compute a correlation coefficient between indices of brain asymmetry and laterality quotients reflecting summed scores derived from a hand preference questionnaire (for critique, see Beaton, 2003), it would be preferable in our view to use a measure of hand skill asymmetry. By dividing the laterality distribution into bins, one could examine the distribution of speech lateralization of participants across bins. Neuroanatomical asymmetries could be related to handedness in an analogous manner.

Given modern imaging methods, it should be possible in the next decade to derive sufficient data from neurologically healthy representative samples of the general population, along with adequate testing of handedness, to finally answer the question of precisely how, if at all, handedness and language lateralization are related. This will necessitate a concerted effort towards large-scale collaboration between research groups (see Kong et al., 2020). It is important to determine the nature of any relationship between handedness and speech dominance since the absence of an association would imply that handedness and language lateralization are two independent characteristics with separate genetic underpinnings.

Within our second category of challenge, future research should continue the attempt to unravel the shared or independent genetic bases of cerebral and manual asymmetry (Cuellar-Partida et al., 2020; de Kovel & Franks, 2019), and of the associations between perturbations of laterality and psychiatric (Wiberg et al., 2019) and neurodevelopmental (Brandler & Paraschini, 2014) conditions. We see this as the major challenge for laterality research during the next decade.

A further challenge is to determine the extent (if any) to which an asymmetrical brain is of fundamental importance for humans—as a species, and at an individual level. The purported advantages of having an asymmetrical brain have been widely discussed (Levy, 1974; Vallortigara & Rogers, 2020). We believe that developments in comparative neuroanatomy and comparative neuroimaging (Friedrich et al., 2021) will help shed light on the emergence of brain lateralization and thereby determine its significance for our own species.

At the level of the individual, both human and infrahuman, many studies have attempted to relate aspects of asymmetry (including handedness) to levels of cognitive ability (Ntolka & Papadatou-Pastou, 2018) or to performance on specific tasks (Hirnstein, Leask, Rose, & Hausmann, 2010). However, the possible implications of variation in direction and degree of multiple asymmetries for individual differences in cognition have barely been considered (but see Labache et al., 2020).

The wider question of whether there are any reproductive advantages associated with individual differences in cerebral lateralization has been deliberated in a few studies looking at Darwinian fitness in relation to handedness (see Faurie et al., 2006; Zickert, Geuze, van der Feen, & Groothuis, 2018). Might individuals with differing patterns of cerebral lateralization have developed different mating strategies, perhaps related to subtle differences in personality traits or abilities, and/or to aspects of female (McKeever, Cerone, Suter, & Wu, 2000; Zhu et al., 2009) or even male reproductive biology?

Our final proposed challenge for laterality researchers during the next decade is to understand more fully how the two hemispheres of the asymmetric brain interact to produce an exquisitely co-ordinated unity of behaviour and a unified (if not unity of) conscious experience (Pinto et al., 2017). We still have little idea how the two limbs are controlled from moment to moment when, for example, someone ties their shoelace, knots a tie, or swings a golf club. And how are the activities of the two sides of the brain co-ordinated in tasks which apparently require the specialized abilities of the two hemispheres acting in concert (think, for example, of reading sheet music while concentrating on getting right the rhythm, tempo, timbre, volume and emotional register of a piece of music)?

Despite the decline of so-called split-brain surgery, a focus on hemispheric interaction should be maintained. This will require novel ways of thinking how this might be explored in both humans and other species. Studies showing increased connectivity between and within the hemispheres in cases of agenesis of the corpus callosum (Mancuso, Uddin, Nania, Costa, & Cauda, 2019) and application of dynamic network theory to neuroimaging studies (Doron, Bassett, & Gazzaniga, 2012) represent significant moves in this direction.

Disclosure statement

No potential conflict of interest was reported by the authors.