Consolidation of human somatosensory memory during motor learning

Abstract

Sensorimotor learning is a bidirectional process associated with concurrent neuroplastic changes in the motor and somatosensory system. While motor memory consolidation and retention have been extensively studied during skill acquisition, little is known about the formation and consolidation of somatosensory memory associated with motor learning. Using a robotic exoskeleton, we tracked markers of somatosensory and motor learning while healthy participants trained to make goal-directed wrist reaching movements over five days and evaluated retention for up to 10 days after practice. Markers of somatosensory learning were changes in wrist position sense bias (systematic error) and precision (random error). The main results are as follows: First, somatosensory (proprioceptive) memory consolidation shows signs of cost savings with repeated sensorimotor training - the same feature is known for motor memory formation. Moreover, somatosensory learning generalized to untrained workspace. Second, somatosensory learning over days can be characterized as an early improvement in sensory precision and a later improvement in sensory bias. Third, the time course of learning gains in position sense acuity coincided with improvements in spatial movement accuracy. Finally, the gains of somatosensory learning were retained for several days. Improvements in position sense bias were still visible up to 3 days after the end of practice for the trained workspace positions, but decayed faster in the untrained workspace. Improvements in position sense precision were retained for up to 10 days and were workspace independent. The findings are consistent with the view that an internal model of somatosensory joint space is formed during motor learning.

Perspectives and Challenges in Robotic Neurorehabilitation

“…Based on these findings, action observation and passive proprioceptive training have been performed together, introducing here an additional point to discuss: The role of proprioceptive learning (or more generally, sensory learning) in the recovery process. Sensory learning is closely related to motor learning in the way in which motor learning shapes sensory networks in the brain and sensory learning changes motor areas [145,146]. In particular, sensory learning results in changes to motor networks in the brain and is also associated with plasticity in sensory systems that is determined by afferent inputs from the periphery and cortical projections from motor areas.…”

“…In particular, sensory learning results in changes to motor networks in the brain and is also associated with plasticity in sensory systems that is determined by afferent inputs from the periphery and cortical projections from motor areas. Limited to proprioception, the idea to use robots to improve the recovery of this sensory channel has been extensively tested [145,146], in addition with supplementary vibro-tactile feedback [147].…”

Somatosensory versus cerebellar contributions to proprioceptive changes associated with motor skill learning: A theta burst stimulation study

“…Given anatomical, functional, and physiological evidence suggesting reciprocal links between sensory and motor processes (Ostry & Gribble, 2016), consolidation of sensory memories may also play a role in motor learning. We and others have shown that motor skill learning is associated with improvements in body position sense (proprioception) that are retained at least 24 hours after practice ends (Cuppone et al, 2018;Mirdamadi & Block, 2020).…”

A Neuromorphic Prosthesis to Restore Communication in Neuronal Networks

“…This approach has the main advantage of informing both brain regions (i.e., neuronal modules, in our case) that an event occurred in the other region, given that interaction in the brain is intrinsically bidirectional (Roelfsema and Holtmaat, 2018). For example, in the sensorimotor system, sensory simulation can help motor recovery (Cuppone et al, 2018) and motor learning can enhance sensory functions (Ostry et al, 2010;Takeuchi and Izumi, 2013). Applications of our neuroprosthetic systems to conditions where the sensorimotor interaction is impaired would allow restoration of both communication channels, suggesting improvements in current rehabilitation therapies.…”