Fuzziness of muscle synergies in patients with multiple sclerosis indicates increased robustness of motor control during walking

Abstract

Deficits during gait poses a significant threat to the quality of life in patients with Multiple Sclerosis (MS). Using the muscle synergy concept, we investigated the modular organization of the neuromuscular control during walking in MS patients compared to healthy participants (HP). We hypothesized a widening and increased fuzziness of motor primitives (e.g. increased overlap intervals) in MS patients compared to HP allowing the motor system to increase robustness during walking. We analysed temporal gait parameters, local dynamic stability and muscle synergies from myoelectric signals of 13 ipsilateral leg muscles using non-negative matrix factorization. Compared to HP, MS patients showed a significant decrease in the local dynamic stability of walking during both, preferred and fixed (0.7 m/s) speed. MS patients demonstrated changes in time-dependent activation patterns (motor primitives) and alterations of the relative muscle contribution to the specific synergies (motor modules). We specifically found a widening in three out of four motor primitives during preferred speed and in two out of four during fixed speed in MS patients compared to HP. The widening increased the fuzziness of motor control in MS patients, which allows the motor system to increase its robustness when coping with pathology-related motor deficits during walking.

Figure 1

Boxplots depicting the maximum Lyapunov exponent values for healthy participants (HP) and patients with Multiple Sclerosis (MSP) during walking at preferred and fixed speed. Asterisks denote significant differences between HP and MSP.

Figure 2

The average spatiotemporal spinal motor outputs (SMOs) are presented for healthy participants (HP) and patients with Multiple Sclerosis (MSP) during walking at preferred and fixed speed normalized in amplitude to the maximum of each segment. These curves were obtained by mapping each of the 13 muscle activations onto the relevant spinal segment (lumbar from L2 to L5 and sacral from S1 and S3). Asterisks denote significant differences in the full width at half maximum of the mapped EMGs between HP and MSP. The two level plots show the average alpha-motoneurons (MN) activity for each condition, giving additional information about the absolute activation level (normalization to the maximum of each condition). The stance and swing phases have been temporally normalized to the same amount of data points (100 each). Values are the means across all participants and all trials.

Figure 3

Averages and standard deviations of the motor modules as well as averaged and individual motor primitives of the four fundamental synergies for healthy participants (HP) and patients with Multiple Sclerosis (MSP) during walking at preferred speed (A, HP = 1.3 ± 0.1 m/s, MSP = 0.8 ± 0.4 m/s) and fixed speed (B, 0.7 m/s). The motor modules are presented on a normalized y-axis base (horizontal black line indicates normalized to 1). Included muscles are gluteus medius (ME), maximus (MA), tensor fasciae latae (TF), rectus femoris (RF), vastus medialis (VM), lateralis (VL), semitendinosus (ST), long head of biceps femoris (BF), tibialis anterior (TA), peronaeus longus (PL), medial (GM) and lateral (GL) gastrocnemius and soleus (SO). For the motor primitives, the x-axis full scale represents one gait cycle (stance and swing normalized to the same amount of points and divided by a vertical line) and the y-axis the normalized maximum amplitude of the individual motor primitives.

Figure 4

Average motor modules and motor primitives of the four fundamental synergies for walking at preferred and fixed speed. The motor modules are presented on a normalized y-axis base. Included muscles at the hip were gluteus medius (ME), maximus (MA) and tensor fasciae latae (TF), at the thigh rectus femoris (RF), vastus medialis (VM) and lateralis (VL), semitendinosus (ST) and the long head of biceps femoris (BF). Lower-leg muscles were tibialis anterior (TA), peronaeus longus (PL), medial (GM) and lateral (GL) gastrocnemius and soleus (SO). For the motor primitives, the x-axis full scale represents one gait cycle (stance and swing normalized to the same amount of points and divided by a vertical line) and the y-axis the normalized amplitude. Asterisks denote significant differences between healthy participants (HP) and patients with Multiple Sclerosis (MSP) for Post hoc tests in the motor modules and R² similarities within groups compared to between groups in the motor primitives.

Figure 5

Overlapping time intervals of motor primitives during preferred speed (left) and fixed speed (right). The heat maps show the individual motor primitive when exceeding half maximum activation for healthy participants (HP, blue) and MS patients (MPS, red). Darker colours indicate higher frequencies of occurrence across all 30 gait cycles per participant. At the bottom the averaged frequency of overlaps (AFO) across all gait cycles and all participants per group. For all graphs the x-axis full scale represents one gait cycle (stance and swing normalized to the same amount of points.