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.

Keywords: Dynamic causal modeling; Left-handers; Motor putamen; Premotor cortex; Right-handers.

Fig. 1

Neural activity for A visually paced fist closures (main effect “hand”) and B the parametric modulation of “frequency” (n = 2 × 18; P < 0.05, FWE-corrected).

Fig. 2

A Bayesian model selection and B the winner model.

Fig. 3

Endogenous connectivity (DCM A-matrix; n = 2 × 18; P < 0.05, FDR-corrected). Green arrows = positive coupling rates, red arrows = negative coupling rates. The width of each arrow corresponds to the coupling strength. In left-handers, the inhibitory connection ndSMA ➔ dM1 is significant at an uncorrected threshold (P < 0.05). For mean coupling parameters and P-values (one-sample t-test against zero) see Supplemental Table II.

Fig. 4

Modulatory effects on effective connectivity (main effect “hand”) during right and left hand fist closures (DCM B-matrix; n = 2 × 18; P < 0.05, FDR-corrected). Green arrows = positive coupling rate, red arrows = negative coupling rates. The width of each arrow corresponds to the coupling strength. For mean coupling parameters and P-values (one-sample t-test against zero) see Supplemental Tables IIIa and IIIb.

Fig. 5

Differences between right- and left-handers when performing dominant hand movements (* P < 0.05, FDR-corrected).