Tonic Pain Experienced during Locomotor Training Impairs Retention Despite Normal Performance during Acquisition

Abstract

Many patients are in pain when they receive gait training during rehabilitation. Based on animal studies, it has been proposed that central sensitization associated to nociception (maladaptive plasticity) and plasticity related to the sensorimotor learning (adaptive plasticity) share similar neural mechanisms and compete with each other. The aim of this study was to evaluate whether experimental tonic pain influences motor learning (acquisition and next-day retention) of a new locomotor task. Thirty healthy human subjects performed a locomotor adaptation task (perturbing force field applied to the ankle during swing using a robotized orthosis) on 2 consecutive days. Learning was assessed using kinematic measures (peak and mean absolute plantarflexion errors) and electromyographic (EMG) activity. Half of the participants performed the locomotor adaptation task with pain on Day 1 (capsaicin cream around the ankle), while the task was performed pain-free for all subjects on Day 2 to assess retention. Pain had no significant effect on baseline gait parameters nor on performance during the locomotor adaptation task (for either kinematic or EMG measures) on Day 1. Despite this apparently normal motor acquisition, pain-free Day 2 performance was markedly and significantly impaired in the Pain group, indicating that pain during training had an impact on the retention of motor memories (interfering with consolidation and/or retrieval). These results suggest that the same motor rehabilitation intervention could be less effective if administered in the presence of pain.

Pain Induced during Both the Acquisition and Retention Phases of Locomotor Adaptation Does Not Interfere with Improvements in Motor Performance

“…While several studies have described the immediate effect of pain on motor performance [2], its effect on motor learning has been less investigated [3–10]. Among the studies who did look at the effect of pain on motor learning, only a few have considered its impact on the retention of new motor skills [8–10], rather than simply looking at improvement during practice (i.e., skill acquisition).…”

“…The only study so far that has looked at the effect of pain on a locomotor learning task showed that cutaneous pain induced by topical application of capsaicin (an experimental model of neuropathic pain) impairs the retention of motor learning despite normal performance during the acquisition phase [8]. In this study, pain was applied only during initial training (motor acquisition) and subjects were pain-free when retested for retention on the following day [8]. Based on these results, it has been suggested that cutaneous pain could interfere with neural processes associated with consolidation of motor learning.…”

What Is Being Trained? How Divergent Forms of Plasticity Compete To Shape Locomotor Recovery after Spinal Cord Injury

“…82 A recent clinical case study has similarly shown that healthy human subjects given brief peripheral nociceptive input are unable to retain a locomotor learning task. 114 Together these observations suggest that peripheral nociceptive stimulation early after SCI produces lasting changes within the spinal cord circuitry that undermine future neurorehabilitation efficacy. Targeting the synaptic mechanisms of these intraspinal changes has the potential to reverse maladaptive plasticity for improved locomotor recovery.…”

Virtual feedback for motor and pain rehabilitation after spinal cord injury

“…8 In addition, pain has been shown to directly interfere with sensorimotor functions, such as the capacity to learn locomotor 9 and upper limb motor 10 tasks. As such, simultaneous treatment of motor functions and pain would be preferred over conventional treatment, that is suboptimal as evidenced by the high prevalence of chronic pain.…”