Movement chunking during sequence learning is a dopamine-dependant process: a study conducted in Parkinson’s disease

Abstract

Chunking of single movements into integrated sequences has been described during motor learning, and we have recently demonstrated that this process involves a dopamine-dependant mechanism in animal (Levesque et al. in Exp Brain Res 182:499-508, 2007; Tremblay et al. in Behav Brain Res 198:231-239, 2009). However, there is no such evidence in human. The aim of the present study was to assess this question in Parkinson's disease (PD), a neurological condition known for its dopamine depletion in the striatum. Eleven PD patients were tested under their usual levodopa medication (ON state), and following a 12-h levodopa withdrawal (OFF state). Patients were compared with 12 healthy participants on a motor learning sequencing task, requiring pressing fourteen buttons in the correct order, which was determined by visual stimuli presented on a computer screen. Learning was assessed from three blocks of 20 trials administered successively. Chunks of movements were intrinsically created by each participant during this learning period. Then, the sequence was shuffled according to the participant's own chunks, generating two new sequences, with either preserved or broken chunks. Those new motor sequences had to be performed separately in a fourth and fifth blocks of 20 trials. Results showed that execution time improved in every group during the learning period (from blocks 1 to 3). However, while motor chunking occurred in healthy controls and ON-PD patients, it did not in OFF-PD patients. In the shuffling conditions, a significant difference was seen between the preserved and the broken chunks conditions for both healthy participants and ON-PD patients, but not for OFF-PD patients. These results suggest that movement chunking during motor sequence learning is a dopamine-dependent process in human.

Chunking improves symbolic sequence processing and relies on working memory gating mechanisms

“…While the overlap between the neural correlates of chunking and WM gating (Graybiel 1998;Bor et al 2003;Gruber et al 2006;Tremblay et al 2010;Murty et al 2011;D'Ardenne et al 2012;Wymbs et al 2012;Jin et al 2014) was considered as indirect evidence of their possible interactions, in accordance with the computational models (O'Reilly and Frank 2006; Grossberg and Kazerounian 2011), we provide here, for the first time, behavioral evidence that chunking is linked to WM gating processes. This suggests that, in accordance with our prediction, chunking during sequence performance relies on the same mechanisms as in WM updating tasks, i.e., presumably the capacity to gate the access of information to WM while filtering irrelevant distractors (Gruber et al 2006;O'Reilly and Frank 2006;D'Ardenne et al 2012).…”

Role of Broca's Area in Implicit Motor Skill Learning: Evidence from Continuous Theta-burst Magnetic Stimulation

“…Among the other structures found activated in SRTT, it has been suggested that the BG are involved in the chunking process as demonstrated in both animals (Levesque et al, 2007;Jog, Kubota, Connolly, Hillegaart, & Graybiel, 1999;Aldridge & Berridge, 1998;Graybiel, 1998;Cromwell & Berridge, 1996;Berridge & Whishaw, 1992) and humans (Tremblay et al, 2010;Boyd et al, 2009). A similar assumption has been made for the hippocampus, because its lesion impairs associative learning in SRTT (Curran, 1997), a finding confirmed in rodents (Ergorul & Eichenbaum, 2006).…”

The Striatum: Where Skills and Habits Meet

“…This manipulation does not interfere with well-learned sequences, but disrupts the formation of new chunks (Levesque et al 2007). Chronic dopamine denervation in patients with Parkinson's disease can also lead to an impairment of chunking for new sequences of movement (Tremblay et al 2010). There is also emerging evidence from human neuroimaging that the strength of activity in the associative striatum varies on a trial-by-trial basis with the degree to which subjects put together elements of motor sequences into chunks, the concatenation aspect of chunking (Wymbs et al 2012).…”