Brain reactions to the use of sensorized hand prosthesis in amputees

Abstract

Objective: We investigated for the first time the presence of chronic changes in the functional organization of sensorimotor brain areas induced by prolonged training with a bidirectional hand prosthesis.

Methods: A multimodal neurophysiological and neuroimaging evaluation of brain functional changes occurring during training in five consecutive amputees participating to experimental trials with robotic hands over a period of 10 years was carried out. In particular, modifications to the functional anatomy of sensorimotor brain areas under resting conditions were explored in order to check for eventual changes with respect to baseline.

Results: Full evidence is provided to demonstrate brain functional changes, and some of them in both the hemispheres and others restricted to the hemisphere contralateral to the amputation/prosthetic hand.

Conclusions: The study describes a unique experimental experience showing that brain reactions to the prolonged use of an artificial hand can be tracked for a tailored approach to a fully embedded artificial upper limb for future chronic uses in daily activities.

Keywords: advanced biotechnologies; brain function; hand prosthesis; personalized medicine.

FIGURE 1

Left lower and upper panels: the prosthetic system (the sensorized prosthesis, the EMG electrodes for the muscular activity recording, the electrical stimulator, and the TIME electrodes implanted on the nerves) and the functioning of the whole system during a grasp task (EMG from the stump muscles during voluntary contraction was recorded with surface electrodes, used to decode efferent activity, and translated into orders for movement of the hand prosthesis; the contact and force production of the prosthetic fingers against resistance triggered a rapid cascade of events within a time window of a few tens of milliseconds, generating a real‐time perception of a sensation from the phantom hand/fingers, thanks to the proportional intensity of electrical stimulation of the stump nerves with the TIME connected to the stimulator). Middle lower panels: localization of TIME electrodes into the median and the ulnar nerves above the elbow, the TIME electrode inserted in the nerve during surgery, and the transcutaneous electrodes available for the connection with the stimulator at the end of surgery. Upper right panel: structure of the TIME electrodes and procedure of their insertion via a guiding needle. Right lower panel: setting of TMS‐EEG performed with the neuronavigation system for exact positioning and repositioning

FIGURE 2

Left panel: Grand average of the TMS‐EEG responses recorded at the electrode FC3 for the left hemisphere at the baseline (black line) and T1 (red line). Middle panel: Grand average of TMS‐EEG responses recorded at the electrode FC4 in single‐pulse stimulation for the right hemisphere at baseline (black line) and T1 (red line). Right panel: trace of a normal subject (courtesy of Bonato et al., 2006). The EEG responses of left hemisphere (the spared one since the patients were all left amputees) are similar to a normal subject. The early components of EEG responses, within 50 ms, of right hemisphere (the contralateral to the amputation) are less represented and smaller in amplitude

FIGURE 3

ANOVA interaction: F (30,210) 5 p < .077) of the power density values among the factors ROIs (frontal, central, parietal, occipital, temporal, limbic), Band [delta (2–4 Hz), theta (4–8 Hz), alpha 1 (8–10.5 Hz), alpha 2 (10.5–13 Hz), beta 1 (13–20 Hz), beta 2 (20–30 Hz), and gamma (30–40 Hz)], and condition (baseline and T1). Duncan‐planned post hoc testing showed that the pattern baseline > T1 was fitted in the delta band in frontal (p < .032206) and temporal regions (p < .001632) while the opposite trend baseline < T1 was found in alpha band in central (p < .066) and parietal (p < .002682) regions (asterisks for significant difference)

FIGURE 4

EEG power density of right and left hemispheres. Upper Left and right panels: ANOVA interaction of the power density values among the factors ROIs (frontal, central, parietal, occipital, temporal, limbic), Band (delta, theta, alpha 1, alpha 2, beta 1, beta 2 and gamma), and condition (baseline; T1) in the left hemisphere (left panel) and in the right hemisphere (right panel). Lower panel: lagged linear baseline versus T1 connectivity in EEG bands (delta, theta, alpha 1, alpha 2, beta 1, beta 2 and gamma) in the left (blue lines) and in the right hemisphere (red lines)

FIGURE 5

Small‐word index of right and left hemispheres at baseline and T1. ANOVA interaction of the small‐world index among the factors Band [delta (0.5–4.5 Hz), theta (5–7.5 Hz), alpha (8–11.5 Hz), sigma (12–15.5 Hz), and beta (16–24.5 Hz)] and side (left hemisphere, right hemisphere) at baseline (left panel) and T1 (right panel). After robotic hand use and sensory feedback trials, the two hemispheres appeared less different in small‐worldness

FIGURE 6

(a) MRI tractography. Corticospinal tract reconstruction. No statistically significant changes between the two sides were observes. (b) Functional MRI. Brain activation during movement imagination task of the phantom hand before and after the training. The upper panel shows the cerebral activation during the task at baseline, while the lower panel shows the activation at the end of the trial. Activation of the occipital areas is due to visual stimulation by the virtual hand movements in a screen. Following the training trials (T1), there was a reduction of additional motor areas and cerebellum activation with a prominent and more selective activation of the contralateral M1 as a typical sign of “motor learning.” Activation maps are displayed with the same statistical threshold