Handedness and effective connectivity of the motor system
Introduction
Handedness is a fundamental, behavioral characteristic of the motor system that evolves even before birth and stabilizes during early childhood (Fagard, 2013). While to date a formal definition of handedness is missing, it is widely accepted that handedness includes that (i) one hand is consistently preferred for carrying out a particular task, (ii) the same hand is chosen for the majority of tasks to be performed, and (iii) this hand is more proficient than the other in task performance (Hammond, 2002, Serrien et al., 2006). Experimental evidence suggests that this intrinsic behavioral phenomenon is associated with asymmetries in the structural and functional organization of the cerebral cortex (Amunts et al., 1996, Eickhoff et al., 2008, Hammond, 2002). For example, anatomical studies revealed a deeper central sulcus in the dominant compared to the non-dominant hemisphere in both right- and left-handers (Amunts et al., 1996). Furthermore, neuroimaging studies demonstrated an influence of hand dominance on neural activity (Dassonville et al., 1997, Kim et al., 1993, Solodkin et al., 2001, Volkmann et al., 1998). In both right- and left-handers, dominant hand movements were shown to be associated with a greater volume of the hand representation in the contralateral primary motor cortex (M1) (Dassonville et al., 1997, Volkmann et al., 1998). Solodkin and colleagues mapped brain activation patterns in right- and left-handers during single and sequential finger movements and found larger volumes of activation and less hemispheric lateralization in left-handers (Solodkin et al., 2001). The latter finding is compatible with behavioral data demonstrating that hand preference in left-handers is often expressed to a lesser degree than in right-handers (Borod et al., 1984). Finally, transcranial magnetic stimulation (TMS) paradigms provided evidence for handedness-related asymmetries in cortical excitability (Brouwer et al., 2001, Ziemann and Hallett, 2001). Ziemann and Hallett (2001) demonstrated that performing a complex motor task with one hand increases the excitability of the motor cortex contralateral to the inactive hand. This increase was significantly smaller when the task was performed with the dominant (right) as opposed to the non-dominant (left) hand (Ziemann and Hallett, 2001). The authors hypothesized that the dominant (left) motor cortex exerts more inhibitory control upon the contralateral motor cortex controlling the non-dominant left hand than vice versa. Taken together, the neural mechanisms for hand dominance might rest in hemispheric-specific differences of network dynamics that govern unimanual movements.
Accordingly, we here investigated whether the preference to use the right or left hand in everyday life is reflected by systematic differences in network interactions during unimanual movements. As outlined above, structural and functional neuroimaging studies have already addressed the neural correlates of handedness (Amunts et al., 1996, Dassonville et al., 1997, Kloppel et al., 2007, Solodkin et al., 2001, Volkmann et al., 1998). However, to date little is known about hand preference and the dynamics of the motor network. To this end, we addressed in a functional magnetic resonance imaging (fMRI) study the question whether there are differences in neural activity and interregional interaction of key motor regions between right- (n = 18) and left-handers (n = 18). Dynamic causal modeling (DCM) was used to assess effective connectivity, i.e., the causal influence that one area exerts upon activity of another (Friston et al., 2003), during unimanual movements of the dominant and non-dominant hands at different frequencies for a bihemispheric network consisting of key motor areas like M1, supplementary motor area (SMA), ventrolateral premotor cortex (PMv), motor putamen (Put) and motor cerebellum (Cb) (Grefkes et al., 2008, Passingham, 1997, Witt et al., 2008). We hypothesized that higher movement speed evokes a stronger BOLD signal especially in the contralateral primary sensorimotor cortex (Jancke et al., 1998, Sadato et al., 1996). Moreover, we hypothesized that movement-related connections are differentially modulated depending on whether subjects are right-handed or left-handed (Kloppel et al., 2007, Solodkin et al., 2001).
Section snippets
Subjects
The study was approved by the local ethics committee and performed in accordance with the Declaration of Helsinki. Thirty-six subjects (18 right-handers [mean age 25.7 ± 3.0 SD; range: 22–34 years] and 18 left-handers [mean age 24.6 ± 2.6 SD; range: 19–30 years]) with no history of neurological or psychiatric disease gave written informed consent. The two groups were carefully matched for age, sex, and laterality of handedness. The fMRI and connectivity data of the right-handers were included in a
Neural activity during unilateral fist closures
Visually paced fist closures of the dominant or the non-dominant hand were associated with enhanced BOLD activity in a network of cortical and subcortical areas comprising contralateral primary motor cortex (M1), bilateral supplementary motor area (SMA), and bilateral ventral premotor cortex (PMv), bilateral motor putamen (Put), bilateral anterior lobe of the cerebellum (Cb), and bilateral primary visual (V1) and extrastriate cortex (P < 0.05, FWE-corrected, Fig. 1A). Please note that hemispheres
Discussion
We found that during dominant hand movements, neural coupling of contralateral (dominant) SMA with premotor areas, motor putamen and M1 was significantly higher in right-handers as compared to left-handers. Moreover, our results revealed a positive correlation between neural coupling strengths and the Edinburgh Handedness Inventory (EHI) scores during movements of the dominant hand. Together, our findings indicate that a stronger preference to use the right hand corresponds to stronger neural
Acknowledgments
We thank our volunteers and are grateful to Dr Marc Tittgemeyer and the MR staff for the support. CG was supported by a grant from the German Research Foundation (Deutsche Forschungsgemeinschaft GR 3285/2-1). SBE was supported by the Deutsche Forschungsgemeinschaft (DFG, EI 816/4-1; S.B.E. and LA 3071/3-1), the National Institute of Mental Health (R01-MH074457) and the Helmholtz Initiative on Systems Biology. GRF gratefully acknowledges support from the Marga and Walter Boll Stiftung.
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