Nurture versus nature: long-term impact of forced right-handedness on structure of pericentral cortex and basal ganglia

Abstract

Does a conflict between inborn motor preferences and educational standards during childhood impact the structure of the adult human brain? To examine this issue, we acquired high-resolution T1-weighted magnetic resonance scans of the whole brain in adult "converted" left-handers who had been forced as children to become dextral writers. Analysis of sulcal surfaces revealed that consistent right- and left-handers showed an interhemispheric asymmetry in the surface area of the central sulcus with a greater surface contralateral to the dominant hand. This pattern was reversed in the converted group who showed a larger surface of the central sulcus in their left, nondominant hemisphere, indicating plasticity of the primary sensorimotor cortex caused by forced use of the nondominant hand. Voxel-based morphometry showed a reduction of gray matter volume in the middle part of the left putamen in converted left-handers relative to both consistently handed groups. A similar trend was found in the right putamen. Converted subjects with at least one left-handed first-degree relative showed a correlation between the acquired right-hand advantage for writing and the structural changes in putamen and pericentral cortex. Our results show that a specific environmental challenge during childhood can shape the macroscopic structure of the human basal ganglia. The smaller than normal putaminal volume differs markedly from previously reported enlargement of cortical gray matter associated with skill acquisition. This indicates a differential response of the basal ganglia to early environmental challenges, possibly related to processes of pruning during motor development.

Figure 1.

Areas showing significant changes related to handedness (image threshold for display purposes: p < 0.001, uncorrected). Results overlaid on a single subject T1-weighted MRI scan in MNI-space. Right panel, Local gray matter volume in left putamen (at x, y, z = −28, 2, 6). Error bars represent 90% confidence intervals of the mean.

Figure 2.

Scatter plot revealing that a greater right-hand lateralization of writing significantly correlates with a relatively larger volume of the left middle putamen (left panel) and the right-lateralization of cortical surface area size in the central sulcus (right panel) in converted left-handers with a first-degree left-handed family member. a.u., Arbitrary units.

Figure 3.

Left panel, Central sulcus surface area for each group, separately for each hemisphere. Right panel, Illustration of lateralization of the central sulcus surface area. Error bars represent 90% confidence intervals of the mean. a.u., Arbitrary units.