Pre-supplementary motor cortex mediates learning transfer from perceptual to motor timing

Abstract

When we intensively train a timing skill, such as learning to play the piano, we not only produce brain changes associated with task-specific learning but also improve our performance in other temporal behaviors that depend on these tuned neural resources. Since the neural basis of time learning and generalization is still unknown, we measured the changes in neural activity associated with the transfer of learning from perceptual to motor timing in a large sample of subjects (n=65; 39 women). We found that intense training in an interval discrimination task increased the acuity of time perception in a group of subjects that also exhibited learning transfer, expressed as a reduction in inter-tap interval variability during an internally driven periodic motor task. In addition, we found subjects with no learning and/or generalization effects. Notably, functional imaging showed an increase in pre-supplementary motor area and caudate-putamen activity between the post- and pre-training sessions of the tapping task. This increase was specific to the subjects that generalized their timing acuity from the perceptual to the motor context. These results emphasize the central role of the cortico-basal ganglia circuit in the generalization of timing abilities between tasks.Significance statementIntensive training in a task can lead to improvements in other behaviors when the neural resources are shared between conditions. Hence, the learning-generalization strategy is now actively used in interventions to improve timing behaviors across tasks. Here we show that timing-precision enhancement after interval discrimination training can be transferred as a decrease in temporal variability during a tapping task in a subgroup of subjects. Crucially, the generalization from perceptual to motor timing increased activity in the pre-supplementary motor area and caudate-putamen in that subgroup. These findings support the notion that magnified recruitment occurs in the cortico-basal-ganglia circuit when an acquired perceptual-timing ability is transferred to a motor-timing task.