Effect of Error Augmentation on Brain Activation and Motor Learning of a Complex Locomotor Task

Abstract

Up to date, the functional gains obtained after robot-aided gait rehabilitation training are limited. Error augmenting strategies have a great potential to enhance motor learning of simple motor tasks. However, little is known about the effect of these error modulating strategies on complex tasks, such as relearning to walk after a neurologic accident. Additionally, neuroimaging evaluation of brain regions involved in learning processes could provide valuable information on behavioral outcomes. We investigated the effect of robotic training strategies that augment errors—error amplification and random force disturbance—and training without perturbations on brain activation and motor learning of a complex locomotor task. Thirty-four healthy subjects performed the experiment with a robotic stepper (MARCOS) in a 1.5 T MR scanner. The task consisted in tracking a Lissajous figure presented on a display by coordinating the legs in a gait-like movement pattern. Behavioral results showed that training without perturbations enhanced motor learning in initially less skilled subjects, while error amplification benefited better-skilled subjects. Training with error amplification, however, hampered transfer of learning. Randomly disturbing forces induced learning and promoted transfer in all subjects, probably because the unexpected forces increased subjects' attention. Functional MRI revealed main effects of training strategy and skill level during training. A main effect of training strategy was seen in brain regions typically associated with motor control and learning, such as, the basal ganglia, cerebellum, intraparietal sulcus, and angular gyrus. Especially, random disturbance and no perturbation lead to stronger brain activation in similar brain regions than error amplification. Skill-level related effects were observed in the IPS, in parts of the superior parietal lobe (SPL), i.e., precuneus, and temporal cortex. These neuroimaging findings indicate that gait-like motor learning depends on interplay between subcortical, cerebellar, and fronto-parietal brain regions. An interesting observation was the low activation observed in the brain's reward system after training with error amplification compared to training without perturbations. Our results suggest that to enhance learning of a locomotor task, errors should be augmented based on subjects' skill level. The impacts of these strategies on motor learning, brain activation, and motivation in neurological patients need further investigation.

The effectiveness of robotic training depends on motor task characteristics

“…As hypothesized, we found that training with error amplification resulted in better motor learning than haptic guidance. This is in line with previous studies that found that training with error amplification outperforms training with haptic guidance when the task difficulty is appropriate for subjects' initial skill level (Milot et al 2010;Marchal-Crespo et al 2014a;Duarte and Reinkensmeyer 2015;Marchal-Crespo et al 2017). This can be explained by the Challenge Point Theory, which states that optimal learning is achieved when the difficulty of the task is appropriate for the individual subject's level of expertise (Guadagnoli and Lee 2004).…”

“…playing a pinballlike game (Milot et al 2010)-but limited transfer of learning in a continuous task -e.g. tracking a Lissajous figure (Marchal-Crespo et al 2017). In the current study, all training strategies generalized learning of the continuous task game, but only subjects trained with haptic guidance generalized the continuous task game, although no significant differences between strategies were found.…”

“…Augmenting errors with forces proportional to errors did not enhance learning to track a 2D figure (Lee and Choi 2010). Amplifying errors during training how to synchronize the legs to track a Lissajous figure resulted in better learning in initially more skilled subjects, but limited transfer of learning (Marchal-Crespo et al 2014a, 2017. These contradictory results suggest that error amplification might limit learning of some specific motor tasks, such as figure tracking.…”

Error variability affects the after effects following motor learning of lateral balance control during walking in people with spinal cord injury

“…Thus, the CNS of people with SCI may be faster in returning to the baseline state of the MoS_Min to reduce the energy cost, resulting in a faster decline of the after effect for the varied force condition. A recent imaging study in healthy controls also indicated that different brain activation patterns were observed for the abrupt and random perturbations (Marchal‐Crespo, Michels, Jaeger, Lopez‐Oloriz, & Riener, ). Along this line of thinking, we speculate that the motor memory produced by errors with varied size and errors with consistent size may be stored in different regions of the brain, which may be a cause for the different levels of lasting of the after effect of MoS_Min.…”

Effects of Robot Viscous Forces on Arm Movements in Chronic Stroke Survivors: A Randomized Crossover Study

“…Stroke neurorehabilitation often uses the unique aspects of technology to improve motor recovery. While some researchers endeavored to simply assist movement to more closely resemble healthy patterns [1,2,3], others have attempted to exploit unique capabilities of robotics or graphic feedback to encourage neuroplasticity by augmenting error [4,5,6,7,8]. Even some traditional physical therapy exercises use mirrors to get the paretic side of the body to imitate the non-paretic side [9].…”