Department of Exercise Sciences


Primary motor and premotor cortex in implicit sequence learning – evidence for competition between implicit and explicit human motor memory systems

Shailesh S. Kantak, Chaithanya K. Mummidisetty and James W. Stinear.  Published in European Journal of Neuroscience, 36, 2710-2715 (2012).

Introduction

Acquisition of serial (or sequential) behaviour is critical to activities of daily living. Motor sequence acquisition through practice involves at least two distinct, yet interrelated processes in the nervous system: online processes leading to improvements in skill performance during practice (involves the explicit memory system), and offline processes that lead to either stabilization of the skill performance over time or improvement in skill performance between training sessions (involves the implicit memory system). Implicit and explicit memory systems are complex and often compete to mediate task performance. Also, anatomically distinct networks associated with implicit and explicit sequence learning (contralateral sensory and primary motor cortex (M1)) are known to be engaged during implicit motor learning, while dorsal premotor cortex (PMd), dorsolateral prefrontal cortex and supplementary motor area are critical for explicit learning. To elucidate the neural substrates underlying the interaction between implicit and explicit memory systems, adults underwent a randomized crossover experiment of anodal transcranial direct current stimulation (AtDCS) applied over M1, PMd or sham stimulation during practice of an implicit motor sequence (serial reaction time task, SRTT).

Aim

We investigated the neural basis of competition between the implicit and explicit systems during implicit motor sequence learning. We hypothesized that compared with sham stimulation, AtDCS over M1 will enhance online and offline learning of the implicit motor sequence. In contrast, because PMd is known to be engaged in explicit knowledge of motor sequences, upregulating PMd with AtDCS during practice will attenuate online and offline learning of the implicit motor sequence.

Method

  • Participants: thirteen right-handed healthy adults. None of the participants had any history of neurological, psychiatric illness or any contraindications to transcranial magnetic stimulation (TMS) or transcranial direct current stimulation (tDCS). All participants used their non-dominant (left) hand for practice of the sequences. Each participant attended three experimental seesions separated by at least 8 days (Fig. 1).
  • We used AtDCS to modulate the excitability of distinct neural structures known to be engaged in implicit (primary motor cortex, M1) and explicit (PMd) memory system during implicit motor sequence practice. The order of PMd, M1 and sham tDCS was counterbalanced across the three experimental sessions and across participants.
  • The effect of AtDCS on M1 and PMd was assessed with online and offline changes in motor performance, a serial reaction time task (SRTT).
  • Implicit sequence performance was assessed at baseline, at the end of acquisition (EoA), and 24 h after practice (retention test, RET).
Kantak 2012 Fig 1 (insert after methods)

Results

  • AtDCS applied over M1 enhanced practice performance compared with sham stimulation (Fig. 2) and also supported offline stabilization of the motor sequence (Fig. 2).
  • In contrast, PMd stimulation with AtDCS during practice attenuated offline stabilization of the motor sequence compared with sham and M1 stimulation (Fig 3).
Kantak 2012 Fig 2 (insert after results)
Kantak 2012 Fig 3 (insert after results)

Interpretation

We assessed the role of M1 and PMd in implicit motor learning using AtDCS employed to enhance activity within the neural substrates during motor practice. Our results indicate that M1 is a critical neural substrate that implements online improvements in performance and offline stabilization for implicit motor sequence learning. In contrast, enhanced PMd activity during practice may be detrimental to offline stabilization of implicit motor sequence learning. These results support the distinction between performance and learning mechanisms. In addition, they indicate a differential engagement of M1 and PMd for practice and retention of an implicit motor sequence. Finally, our results add further support to the notion of competition between the implicit and explicit motor memory systems specifically during the post-practice consolidation phase. More research is needed to elucidate the time course and differential role of specific neural substrates during implicit and explicit motor learning.