Protection and expression of human motor memories

SE Pekny, SE Criscimagna-Hemminger, and R Shadmehr (2011) Journal of Neuroscience.

Abstract When we adapt our movements to a perturbation, and then adapt to another perturbation, is the initial memory destroyed, or is it protected? Despite decades of experiments, this question remains unresolved. The confusion, in our view, is due to the fact that in every instance the approach has been to assay contents of motor memory by re-testing with the same perturbations. When performance in re-testing is the same as naïve, this is usually interpreted as the memory being destroyed. However, it is also possible that the initial memory is simply masked by the competing memory. We trained humans in a reaching task in field B, and then in field A (or washout) over an equal number of trials. To assay contents of motor memory, we used a new tool: after completion of training in A, we withheld reinforcement (i.e., reward) for a brief block of trials and then clamped movement errors to zero over a long block of trials. We found that this led to spontaneous recovery of B. That is, withholding reinforcement for the current motor output resulted in the expression of the competing memory. Therefore, adaptation followed by washout or reverse-adaptation produced competing motor memories. The protection from unlearning was unrelated to sudden changes in performance errors that might signal a contextual change, as competing memories formed even when the perturbations were introduced gradually. Rather, reinforcement appears to be a critical signal that affords protection to motor memories, and lack of reinforcement encourages retrieval of a competing memory.