Handedness and effective connectivity of the motor system

Abstract

Handedness denotes the individual predisposition to consistently use the left or right hand for most types of skilled movements. A putative neurobiological mechanism for handedness consists in hemisphere-specific differences in network dynamics that govern unimanual movements. We, therefore, used functional magnetic resonance imaging and dynamic causal modeling to investigate effective connectivity between key motor areas during fist closures of the dominant or non-dominant hand performed by 18 right- and 18 left-handers. Handedness was assessed employing the Edinburgh-Handedness-Inventory (EHI). The network of interest consisted of key motor regions in both hemispheres including the primary motor cortex (M1), supplementary motor area (SMA), ventral premotor cortex (PMv), motor putamen (Put) and motor cerebellum (Cb). The connectivity analysis revealed that in right-handed subjects movements of the dominant hand were associated with significantly stronger coupling of contralateral (left, i.e., dominant) SMA with ipsilateral SMA, ipsilateral PMv, contralateral motor putamen and contralateral M1 compared to equivalent connections in left-handers. The degree of handedness as indexed by the individual EHI scores also correlated with coupling parameters of these connections. In contrast, we found no differences between right- and left-handers when testing for the effect of movement speed on effective connectivity. In conclusion, the data show that handedness is associated with differences in effective connectivity within the human motor network with a prominent role of SMA in right-handers. Left-handers featured less asymmetry in effective connectivity implying different hemispheric mechanisms underlying hand motor control compared to right-handers.

Manual dexterity: Functional lateralisation patterns and motor efficiency

“…This observation supports data that have revealed that interactions between hemispheres underline changes in processing demands due to handedness (Pool, Rehme, Fink, Eickhoff, & Grefkes, 2014;Reid & Serrien, 2012). Here, we noticed that right-handers showed suppression during movement as compared to rest, which suggests that inhibition of the contralateral hemisphere assists functional lateralisation.…”

“…Therefore, midline circuitry represents a relevant pathway that supports functional coupling patterns when righthanders perform movements with the non-dominant hand. This observation is in line with earlier fMRI research that has revealed that handedness guides effective connectivity within the motor network, including a significant role of the SMA (Pool et al, 2014). Taking into account that the coordination of brain systems was observed for complex rather than easy movements without a behavioural handedness effect, it suggests that these widespread interactions have limited 12 influence in supporting behavioural efficiency as compared to localised interactions between leftsided brain regions.…”

Functional resting-state connectivity of the human motor network: Differences between right- and left-handers

“…Liu and colleagues found greater interhemispheric asymmetry in functional resting-state-connectivity of attention-related areas in right-handers compared to left-handers (Liu et al, 2009). We recently showed that effective connectivity, i.e., the causal influence that one area exerts over another area, between motor areas was differentially modulated in right-and left-handers depending on whether movements were performed with the dominant or non-dominant hand (Pool et al, 2014). More precisely, effective connectivity analysis revealed that in right-handed subjects movements of the dominant hand were associated with significantly stronger coupling of contralateral (left, i.e., dominant) supplementary motor area (SMA) with ipsilateral SMA, ipsilateral ventral premotor cortex (PMv), contralateral motor putamen and contralateral primary motor cortex (M1) (compared to equivalent connections in left-handers).…”

“…Thirty-six subjects [18 right-handers (10 males; 22-33 years old; mean age 26.1 ± 3.0 SD) and 18 left-handers (7 males; 19-30 years old; mean age 24.3 ± 2.6 SD)] with no history of neurological or psychiatric disease gave informed consent. Activation data of frequency-dependent modulation were previously published for this cohort of subjects (Pool et al, 2013(Pool et al, , 2014.…”

“…Based on these observations we concluded that handedness is associated with differences in effective connectivity within the human motor network with a prominent role of left SMA in righthanders. The fact that left-handers featured less asymmetry in effective connectivity strongly suggested differential hemispheric mechanisms underlying hand motor control in left-and right-handers (Pool et al, 2014). However, differences in task performance (either in absolute performance measures or in hidden parameters like attention and effort) are inherent putative confounds for all taskbased fMRI studies (Lowe et al, 1998;Yan et al, 2012).…”