Neuromodulation of reinforced skill learning reveals the causal function of prefrontal cortex

Abstract

Accumulating evidence has suggested functional interactions between prefrontal cortex (PFC) and dissociable large-scale networks. However, how these networks interact in the human brain to enable complex behaviors is not well-understood. Here, using a combination of behavioral, brain stimulation and neuroimaging paradigms, we tested the hypothesis that human PFC is required for successful reinforced skill formation. We additionally tested the extent to which PFC-dependent skill formation is related to intrinsic functional communication with this region. We report that inhibitory noninvasive transcranial magnetic stimulation over lateral PFC, a hub region with a diverse connectivity profile, causally modulated effective reinforcement-based motor skill acquisition. Furthermore, PFC-dependent skill formation was strongly related to the strength of functional connectivity between the PFC and regions in the sensorimotor network. These results point to the involvement of lateral PFC in the neural architecture that underlies the acquisition of complex skills, and suggest that, in relation to skill acquisition, this region may be involved in functional interactions with sensorimotor networks.

Prefrontal stimulation prior to motor sequence learning alters multivoxel patterns in the striatum and the hippocampus

“…In contrast to previous studies applying disruptive prefrontal stimulation prior or during MSL 69–72 our results did not reveal any significant effects of stimulation on motor performance. These discrepancies might arise from several differences in methodology, such as the presence of reward during task practice, the awareness of the sequential material to learn (implicit / explicit learning), the task features (e.g., unimanual / bimanual) or the specific stimulation patterns used (1Hz, 5Hz rTMS and single pulse TMS / TBS).…”

Reward boosts reinforcement-based motor learning

“…Based on these elements and on the causal role of the striatum in reinforcement-based adjustments in motor commands ( Nakamura and Hikosaka, 2006 ; Williams and Eskandar, 2006 ), we suspect that this region may be crucial for the beneficial effect of reward observed in the present study. Notably, the cerebellum ( Carta et al., 2019 ; Heffley et al., 2018 ; Sendhilnathan et al., 2020 ; Vassiliadis et al., 2019 ; Wagner et al., 2017 ) and frontal areas ( Dayan et al, 2014 , 2018 ; Hamel et al., 2018 ; Palidis et al., 2019 ; Ramakrishnan et al., 2017 ; Sidarta et al., 2016 ) are also likely to contribute to reward-based motor learning. Further investigations are required to better delineate the neurophysiological bases of reward-related improvements in motor learning.…”

Reward boosts reinforcement-based motor learning

“…Based on these elements and on the causal role of the striatum in reinforcement-based adjustments in motor commands (Nakamura and Hikosaka, 2006; Williams and Eskandar, 2006), we suspect that this region may be crucial for the beneficial effect of reward observed in the present study. Notably, the cerebellum (Carta et al, 2019; Heffley et al, 2018; Sendhilnathan et al, 2020; Vassiliadis et al, 2019; Wagner et al, 2017) and frontal areas (Dayan et al, 2018, 2014; Hamel et al, 2018; Palidis et al, 2019; Ramakrishnan et al, 2017; Sidarta et al, 2016) are also likely to contribute to reward-based motor learning. Further investigations are required to better delineate the neurophysiological bases of reward-related improvements in motor learning.…”