Functional cortical changes of the sensorimotor network are associated with clinical recovery in multiple sclerosis

Abstract

Objective: To assess the early cortical changes following an acute motor relapse secondary to a pseudotumoral lesion in MS patients, the longitudinal cortical functional correlates of clinical recovery, and the evolution over time of cortical reorganization.

Methods: FMRI during the performance of a simple motor task were obtained from 12 MS patients (after a clinical attack involving the motor system secondary to a pseudotumoral lesion) and 15 matched controls. In six patients and five controls, a longitudinal fMRI study was also performed.

Results: In patients, at baseline, the primary sensorimotor cortex (SMC) of the ipsilateral (contralesional) hemisphere was significantly more active during task performance with the impaired than the unimpaired hand. During task performance with the unimpaired hand, the ipsilateral cerebellum and several motor areas in the contralateral hemisphere were significantly more active. Pseudotumoral lesion volume was correlated with activation of the primary SMC bilaterally (r = -0.86 and -0.85) and the nine-hole peg test score with activation of the primary SMC of the affected hemisphere (r = 0.88). A recovery of function of the primary SMC of the affected hemisphere was found in the four patients with clinical improvement. In the two patients without clinical recovery, there was a persistent recruitment of the primary SMC of the unaffected hemisphere.

Conclusions: Pseudotumoral MS lesions affecting the motor system can determine short-term cortical changes characterized by the recruitment of pathways in the unaffected hemisphere. The regain of function of motor areas of the affected hemisphere seems to be a critical factor for a favorable recovery.

Figure 1

Evolution over time (baseline and month 6) of a pseudotumoral MS lesion in one patient followed up over 6 months. On T2‐weighted images, a progressive reduction of lesion volumes over time is visible.

Figure 2

Cortical activations during right hand movement in healthy subjects (A) and during movement of unimpaired (B) and impaired (C) hand in patients in the acute‐subacute phase of a clinical relapse. In patients, scans obtained during task performance with the left hand have been flipped in order to keep the left hemisphere contralateral to movement. Images are in neurological convention. See text for further details.

Figure 3

Comparison of cortical activations between task performance with unimpaired and impaired hands. Scans obtained during task performance with the left hand have been flipped in order to keep the left hemisphere contralateral to movement. (A) During task performance with the impaired hand, the primary sensorimotor cortex (SMC) of the ipsilateral hemisphere was significantly more activated than during the unimpaired hand task. (B–D) During task performance with the unimpaired hand, several motor areas in contralateral hemisphere, including the primary SMC (B), secondary sensorimotor area, thalamus (C), and ipsilateral cerebellum (D) were significantly more active than during impaired hand task. Images are in neurological convention. See text for further details.

Figure 4

Scatterplots of the correlations between volume of the pseudotumoral lesions and the relative activations of the ipsilateral (A) and controlateral (B) primary SMC and between NHPTr and relative activation of the contralateral primary SMC (C) in patients during task performance with the impaired hand.

Figure 5

SPMt maps superimposed on high‐resolution T1‐weighted images showing relative cortical activations during task performance with the impaired hand between patients with good recovery and those with poor/absent recovery: (A) Contralateral primary SMC; (B) Bilateral SII; (C) Contralateral CMA; (D) Ipsilateral SMA.

Figure 6

Longitudinal evolution of cortical activations in the primary SMC, bilaterally, during task performance with impaired hand compared to unimpaired hand in one patient with good clinical recovery during follow up (A and B) and in one patient with poor/absent clinical recovery (C and D). Scans obtained during left hand motor task have been flipped in order to keep the left hemisphere contralateral to movement. Activations have been superimposed on a glass brain. At baseline, both patients showed an increased activation of the primary SMC of the unaffected (ipsilateral) hemisphere (A and C). During follow up, the patient with good clinical recovery showed an increased functionality of the primary SMC of the affected hemisphere (B), while the patient with poor/absent clinical recovery continued to show an recruitment of the primary SMC of the unaffected hemisphere (D).