Does Ipsilateral Remapping Following Hand Loss Impact Motor Control of the Intact Hand?

• Published in: The Journal of neuroscience 2024-01, Vol.44 (4), p.e0948232023
• Main Authors: Tucciarelli, Raffaele, Ejaz, Naveed, Wesselink, Daan B, Kolli, Vijay, Hodgetts, Carl J, Diedrichsen, Jörn, Makin, Tamar R
• Format: Article
• Language: English
• Subjects: Amputation; Amputation, Surgical; Amputees; Brain mapping; Brain Mapping - methods; Female; Fingers; Functional Laterality; Functional magnetic resonance imaging; Hand; Humans; Magnetic Resonance Imaging - methods; Male; Motor task performance; Multivariate analysis; Neural networks; Representations; Substantia alba; Task Performance and Analysis
• ISSN: 0270-6474; 1529-2401; 1529-2401
• DOI: 10.1523/JNEUROSCI.0948-23.2023

What happens once a cortical territory becomes functionally redundant? We studied changes in brain function and behavior for the remaining hand in humans (male and female) with either a missing hand from birth (one-handers) or due to amputation. Previous studies reported that amputees, but not one-handers, show increased ipsilateral activity in the somatosensory territory of the missing hand (i.e., remapping). We used a complex finger task to explore whether this observed remapping in amputees involves recruiting more neural resources to support the intact hand to meet greater motor control demands. Using basic fMRI analysis, we found that only amputees had more ipsilateral activity when motor demand increased; however, this did not match any noticeable improvement in their behavioral task performance. More advanced multivariate fMRI analyses showed that amputees had stronger and more typical representation-relative to controls' contralateral hand representation-compared with one-handers. This suggests that in amputees, both hand areas work together more collaboratively, potentially reflecting the intact hand's efference copy. One-handers struggled to learn difficult finger configurations, but this did not translate to differences in univariate or multivariate activity relative to controls. Additional white matter analysis provided conclusive evidence that the structural connectivity between the two hand areas did not vary across groups. Together, our results suggest that enhanced activity in the missing hand territory may not reflect intact hand function. Instead, we suggest that plasticity is more restricted than generally assumed and may depend on the availability of homologous pathways acquired early in life.