Abstract
One of the most striking demonstrations of plasticity in the adult human brain follows peripheral injury, such as amputation. In the primary sensorimotor cortex, arm amputation results in massive local remapping of the missing hands' cortical territory. However, little is known about the consequences of sensorimotor deprivation on global brain organisation. Here, we used resting-state fMRI to identify large-scale reorganisation beyond the primary sensorimotor cortex in arm amputees, compared with two-handed controls. Specifically, we characterised changes in functional connectivity between the cortical territory of the missing hand in the primary sensorimotor cortex (‘missing hand cortex’) and two networks of interest: the sensorimotor network, which is typically strongly associated with the hand cortex, and the default mode network (DMN), which is normally dissociated from it. Functional connectivity values between the missing hand cortex and the sensorimotor network were reduced in amputees, and connectivity was weaker in individuals amputated for longer periods. Lower levels of functional coupling between the missing hand cortex and the sensorimotor network were also associated with emerged coupling of this cortex with the DMN. Our results demonstrate that plasticity following arm amputation is not restricted to local remapping occurring within the sensorimotor homunculus of the missing hand but rather produces a cascade of cortical reorganisation at a network-level scale. These findings may provide a new framework for understanding how local deprivation following amputation could elicit complex perceptual experiences of phantom sensations, such as phantom pain.
Highlights
Our brain's ability to reorganise itself throughout life is a key mechanism that enables adjustment to novel situations, as well as compensation for injury
Arm amputation is a powerful driver of brain plasticity, as it combines sensorimotor deprivation with profound behavioural changes, encompassing both acquisition of compensatory motor skills and coping with a chronic pain condition
For the default mode network (DMN), the most parsimonious model relied on functional connectivity between the sensorimotor network and the missing hand cortex, and phantom pain magnitude as independent variables (R2 = 0.34, F(2,15) = 3.89, p = 0.044.; adjusted R2 = 0.254). These results suggest that the main driver for decoupling from the sensorimotor cortex may be time since amputation, whereas coupling with the DMN depends on both dissociation from the network of origin and increased phantom pain, the contribution of phantom pain to the final model was only marginally significant (t = 2.00, p = 0.064), and should be interpreted with caution
Summary
Our brain's ability to reorganise itself throughout life is a key mechanism that enables adjustment to novel situations, as well as compensation for injury. Arm amputation is a powerful driver of brain plasticity, as it combines sensorimotor deprivation with profound behavioural changes, encompassing both acquisition of compensatory motor skills and coping with a chronic pain condition (phantom limb pain which is a common consequence of arm amputation Weeks et al, 2010). Despite these global consequences on perception and action, amputation has been primarily used as a model for studying local plasticity, consequential to focal input loss. The mechanisms linking local remapping with complex phenomenology such as chronic phantom pain, as well as other sensations arising from the “phantom hand” are still largely unknown
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