Lower limb amputees undergo long-distance plasticity in sensorimotor functional connectivity

Ivanei E Bramati,Sebastian Höfle,Elington L Simões,Roberto Lent,Fernanda Tovar-Moll,Jorge Moll,Erika C Rodrigues,Bruno Melo

doi:10.1038/s41598-019-39696-z

Abstract

Amputation in adults is associated with an extensive remapping of cortical topography in primary and secondary sensorimotor areas. Here, we used tactile residual limb stimulation and 3T functional magnetic resonance imaging in humans to investigate functional connectivity changes in the sensorimotor network of patients with long-term lower limb traumatic amputations with phantom sensation, but without pain. We found a pronounced reduction of inter-hemispheric functional connectivity between homologous sensorimotor cortical regions in amputees, including the primary (S1) and secondary (S2) somatosensory areas, and primary (M1) and secondary (M2) motor areas. We additionally observed an intra-hemispheric increased functional connectivity between primary and secondary somatosensory regions, and between the primary and premotor areas, contralateral to amputation. These functional connectivity changes in specialized small-scale sensory-motor networks improve our understanding of the functional impact of lower limb amputation in the brain. Our findings in a selective group of patients with phantom limb sensations, but without pain suggest that disinhibition of neural inputs following traumatic limb amputation disrupts sensorimotor topology, unbalancing functional brain network organization. These findings step up the description of brain plasticity related with phantom sensations by showing that pain is not critical for sensorimotor network changes after peripheral injury.

Highlights

Amputation in adults is associated with the remapping of sensorimotor cortical representations
Gray matter reduction within the hand representation in upper limb amputees as well as white matter changes in the corpus callosum in lower limb amputees were identified[12,15]
This decreased functional connectivity was found for all the inter-hemispheric connections between the homotopic regions: S1 (T = −2.98, PFDR = 0.008), M1 (T = −3.71, PFDR = 0.001), M2 (T = −3.73, PFDR = 0.001), and S2 (T = −6.52, PFDR = 0.000) (Table 2)

Summary

Introduction

Amputation in adults is associated with the remapping of sensorimotor cortical representations. About 90% of individuals suffering amputation report “phantom sensations”, the term used to define the perception that the missing part is still present[6,7,8,9] Gray matter reduction within the hand representation in upper limb amputees as well as white matter changes in the corpus callosum in lower limb amputees were identified[12,15]. Taken together, these functional and structural findings suggest that limb amputation lead to marked changes of sensorimotor network as a whole, potentially unbalancing its functional organization[16]

Objectives

Methods

Results

Conclusion