Changes in Functional and Structural Brain Connectivity Following Bilateral Hand Transplantation

Abstract

As a surgical treatment following amputation or loss of an upper limb, nearly 200 hand transplantations have been completed to date. We report here a magnetic resonance imaging (MRI) investigation of functional and structural brain connectivity for a bilateral hand transplant patient (female, 60 years of age), with a preoperative baseline and three postoperative testing sessions each separated by approximately six months. We used graph theoretical analyses to estimate connectivity within and between modules (networks of anatomical nodes), particularly a sensorimotor network (SMN), from resting-state functional MRI and structural diffusion-weighted imaging (DWI). For comparison, corresponding MRI measures of connectivity were obtained from 10 healthy, age-matched controls, at a single testing session. The patient's within-module functional connectivity (both SMN and non-SMN modules), and structural within-SMN connectivity, were higher preoperatively than that of the controls, indicating a response to amputation. Postoperatively, the patient's within-module functional connectivity decreased towards the control participants' values, across the 1.5 years postoperatively, particularly for hand-related nodes within the SMN module, suggesting a return to a more canonical functional organization. Whereas the patient's structural connectivity values remained relatively constant postoperatively, some evidence suggested that structural connectivity supported the postoperative changes in within-module functional connectivity.

Keywords: amputation; neuroplasticity; vascularized composite allograft.

Fig. 1

Module partition. Four data-driven modules were derived from the patient's preoperative resting-state fMRI data, using Brainnetome Atlas nodes (Fan et al., 2016) and the Brain Connectivity Toolbox (Rubinov and Sporns, 2010), with the Louvain algorithm and consensus clustering.

Fig. 2

Resting-state functional connectivity of sensorimotor network (SMN) nodes and non-SMN nodes, at each testing session. Panel A = within-module connectivity; Panel B = between-module connectivity. Session 0 was approximately four months preoperative, and each subsequent session occurred at approximately six-month intervals (see Patient and Control Participants).

Fig. 3

Resting-state functional connectivity of hand and non-hand nodes within the sensorimotor network, at each testing session. Panel A = within-module connectivity; Panel B = between-module connectivity. n = 15 hand nodes and 28 non-hand nodes. Session 0 was approximately four months preoperative, and each subsequent session occurred at approximately six-month intervals (see Patient and Control Participants).

Fig. 4

Diffusion-weighted imaging (DWI) structural connectivity of sensorimotor network (SMN) nodes and non-SMN nodes, at each testing session. Panel A = within-module connectivity; Panel B = between-module connectivity. Session 0 was approximately four months preoperative, and each subsequent session occurred at approximately six-month intervals (see Patient and Control Participants).

Fig. 5

Diffusion-weighted imaging (DWI) structural connectivity of hand and non-hand nodes within the sensorimotor network, at each testing session. Panel A = within-module connectivity; Panel B = between-module connectivity. n = 15 hand nodes and 28 non-hand nodes. Session 0 was approximately four months preoperative, and each subsequent session occurred at approximately six-month intervals (see Patient and Control Participants).