Increased functional connectivity between cortical hand areas and praxis network associated with training-related improvements in non-dominant hand precision drawing

Abstract

Chronic forced use of the non-dominant left hand yields substantial improvements in the precision and quality of writing and drawing. These changes may arise from increased access by the non-dominant (right) hemisphere to dominant (left) hemisphere mechanisms specialized for end-point precision control. To evaluate this prediction, 22 healthy right-handed adults underwent resting state functional connectivity (FC) MRI scans before and after 10 days of training on a left hand precision drawing task. 89% of participants significantly improved left hand speed, accuracy, and smoothness. Smoothness gains were specific to the trained left hand and persistent: 6 months after training, 71% of participants exhibited above-baseline movement smoothness. Contrary to expectations, we found no evidence of increased FC between right and left hemisphere hand areas. Instead, training-related improvements in left hand movement smoothness were associated with increased FC between both sensorimotor hand areas and a left-lateralized parieto-prefrontal network implicated in manual praxis. By contrast, skill retention at 6 months was predicted by changes including decreased FC between the representation of the trained left hand and bilateral sensorimotor, parietal, and premotor cortices, possibly reflecting consolidation and a disengagement of early learning processes. These data indicate that modest amounts of training (<200min total) can induce substantial, persistent improvements the precision and quality of non-dominant hand control in healthy adults, supported by strengthened connectivity between bilateral sensorimotor hand areas and a left-lateralized parieto-prefrontal praxis network.

Keywords: FMRI; Humans; Laterality of motor control; Learning; Movement; Training.

Figure 1

Flow chart of participants at each stage of analysis. Numbers in each box indicate participants used; numbers at arrow indicate participants lost.

Figure 2

Sample PDT stimuli, showing 4 out of 15 possible shapes. A: 90 mm drawing length, 5 mm width. B: 135 mm drawing length, 3 mm width. C: 135 mm drawing length, 5 mm width. D: 180 mm drawing length, 3 mm width. E: 180 mm drawing length, 4 mm width.

Figure 3

PDT behavior. A: Increased speed, smoothness, and success rate across training, as well as persistence/retention during follow-up sessions. Group means ± SEM. Speed and smoothness in Z_NDH, success rate in %. B: Hand differences (NDH – DH) pre-training and post-training, demonstrating significant NDH-specific learning for smoothness and trend for speed. *: p < .001. †: p = .069. C: Hand-specificity of NDH smoothness learning confirmed by near-zero correlation between NDH smoothness gains and DH smoothness gains. D: Long-term changes in NDH smoothness, measured as % of participants at each follow-up session. “Retention” defined as significantly increased from pre-training baseline. “Persistence” defined as no significant change from post-training peak.

Figure 4

Changes in functional connectivity with normative hand seeds, across training and correlated with smoothness learning. Green outlines indicate bilateral seed regions. White outlines indicate areas that changed connectivity with both seeds (i.e., significant in both A and B). A: Changed connectivity with trained left hand’s (right hemisphere) seed, including increased connectivity with left SMg and SPL, bilateral S1, vPMC, dlPFC, and superior cerebellum; and decreased connectivity with right S2, precentral sulcus, temporal pole, bilateral occipital cortex, and SMA. B: Changed connectivity with untrained right hand’s (left hemisphere) seed, including increased connectivity with left SMG and vPMC, bilateral dlPFC, cerebellar hemispheres, and precuneus; and decreased connectivity with right S1, S2, anterior SMg, and bilateral occipital cortex.

Figure 5

Changes in functional connectivity with normative hand seeds, across training and correlated with smoothness retention at 6 months post-training. Green outlines indicate bilateral seed regions. A: Changed connectivity with trained left hand’s (right hemisphere) seed, including decreased connectivity with bilateral PMd and S1, right M1, bilateral SPL, and SMA. B: Changed connectivity with untrained right hand’s (left hemisphere) seed, including increased connectivity with dlPFC, anterior cingulate gyrus, and cerebellum; and decreased connectivity with precuneus, bilateral SPL, and left S1 and S2.