Fronto-Parietal Networks are Associated with Multi-Day Savings in Visuomotor Adaptation

Humans are able to adapt their behavior to changing environmental or internal demands, enabling us to engage in appropriate sensorimotor performance. Mechanisms underlying such adaptation learning to e.g., force field or visual perturbations have been investigated extensively at both the behavioral and neural level, revealing important insights into how people adaptively modify motor control. Interestingly, several studies have shown that retention of the learned information can outlast the training session, and that adaptation learning can lead to the formation of long-term memories (i.e., those lasting 24h or more). However, not much is known about the neural mechanisms that are involved in multi-day adaptation and retention. The present study therefore aimed to I) identify changes in neural activation that occur over the time course of multi-day adaptation learning, and II) identify individual neural predictors of sensorimotor memory retention. We collected functional magnetic resonance imaging (fMRI) data from 16 participants (12 males; mean age 40 years) while they performed a manual adaptation task, in which they moved a joystick to hit targets presented on a screen. Initially, they performed the task under normal visual feedback, but then had to adapt to 45 degree clockwise rotated feedback. Participants performed the task during four separate test sessions over a three-month period, allowing us to examine adaptation rates and savings at subsequent sessions (which were completed on average 11 days, 48 days and 86 days after the first session). At the behavioral level, participants' performance improved within each test session and learning rates increased over the sessions. Participants were less perturbed by the rotated feedback in later sessions compared to the initial test session, which reflects savings of adaptation learning. At the neural level, results showed that activation changed over the four test sessions in a variety of frontal, parietal, cingulate, and temporal cortical areas, as well as various subcortical areas. Interestingly, these areas mostly showed activation increases rather than decreases. Furthermore, we found that retention of adaptation learning was associated with the extent of activation in frontal cortical areas including the bilateral middle, medial and superior frontal gyri, as well as parietal and cingulate cortical areas including the bilateral precuneus and anterior cingulate gyrus. These findings suggest that participants may be learning how to better engage cognitive processes across days, potentially reflecting the improvements in action selection that have been shown to occur with savings.