Consolidation of motor sequence learning eliminates susceptibility of SMAproper to TMS: a combined rTMS and cTBS study

Abstract

Earlier research suggested that after 210 practice trials, the supplementary motor area (SMA) is involved in executing all responses of familiar 6-key sequences in a discrete sequence production (DSP) task (Verwey, Lammens, and van Honk, 2002). This was indicated by slowing of each response 20 and 25 min after the SMA had been stimulated for 20 min using repetitive transcranial magnetic stimulation (rTMS). The present study used a similar approach to assess the effects of TMS to the more posterior SMAproper at the end of practice and also 24 h later. As expected stimulation of SMAproper with 20 min of 1 Hz rTMS and 40 s of continuous theta burst stimulation (cTBS) immediately after practice slowed sequence execution relative to a sham TMS condition, but stimulation on the day following practice did not cause slowing. This indicates that offline consolidation makes learning robust against stimulation of SMAproper. Execution of all responses in the sequence was disrupted 0, 20, and 40 min after rTMS, but after cTBS, this occurred only after 40 min. The results suggest that it is implicit sequence knowledge that is processed by the SMAproper and that consolidates.

Modulating Visuomotor Sequence Learning by Repetitive Transcranial Magnetic Stimulation: What Do We Know So Far?

“…Additionally, a PET study suggests that the SMA is involved in the execution of previously learned sequences rather than in the acquisition of sequences (Honda et al 1998). In more recent studies, the SMA was found to be involved in the automatization of sequential movements (Shimizu et al 2020) and the consolidation of implicit sequence knowledge (Verwey et al 2022). We found that only three studies have targeted the SMA.…”

“…Different stimulation protocols (i.e., conventional rTMS vs. TBS), stimulation timings (i.e., before, during, or after learning), control stimulation (i.e., no control, sham stimulation, active control), and stimulation intensities were utilized in almost all studies. Although both repetitive stimulation techniques seem to modulate visuomotor sequence learning effectively, a recent study suggests that the conventional low-frequency rTMS has a greater inhibitory effect on motor sequence learning than cTBS (Glinski 2021;Verwey et al 2022).…”

C-SMB 2.0: Integrating over 25 years of motor sequencing research with the Discrete Sequence Production task

“…Counterbalancing sequences across practice and testing ensures that across participants familiar and unfamiliar sequences comprise the same sequence sets. Multiday practice and testing on a day after practice allow for studying consolidation of sequencing skill (Kim et al, 2016 ; Verwey et al, 2022a , b ; Wright et al, 2010 ). To determine the contribution of explicit knowledge, the practice or test phase in a DSP task is usually followed by an awareness test (see section “Preparing Longer Sequences”).…”

“…In addition to unveiling the underlying processing mechanisms, the DSP task has been used to address the effectiveness of procedures to boost motor sequence learning, like using mental practice (Sobierajewicz et al, 2016 ), and increasing contextual interference by randomly varying alternative sequences in a single block of trials (Random Practice, or RP), instead of practicing different sequences in separate blocks (Blocked Practice, or BP) 3 (Cross et al, 2007 ; Immink & Wright, 1998 ; Kim et al, 2018 ; Lin et al, 2012 , 2016 ; Verwey et al, 2022b ). In addition, DSP studies explored the learning benefits of noninvasive stimulation of brain areas like M1 and prefrontal areas using transcranial magnetic brain stimulation (TMS; Cohen et al, 2009 ; Kennerley et al, 2004 ; Ruitenberg et al, 2014 ; Verwey et al, 2022a ) and transcranial direct current stimulation (tDCS; Greeley et al, 2020 , 2022 ; Kim et al, 2020 , 2021 ; Kim & Wright, 2020 ; Sobierajewicz et al, 2019 ; Waters-Metenier et al, 2014 ).…”

“…Two DSP studies involved placeholder fillings with the same luminance as the background to reduce attentional capture (Riesenbeck, 2021 ; Verwey, 2021 ). Stimulus locations were not always spatially compatible with the required responses (Ganor-Stern et al, 2013 ; Verwey et al, 2020 ) and many DSP tasks involved letters or numbers to indicate the individual responses and/or fingers to be used (e.g., Brown & Carr, 1989 ; De Kleine & Verwey, 2009 ; Ganor-Stern et al, 2013 ; Immink & Wright, 1998 ; Kornysheva et al, 2013 ; Mantziara et al, 2021 ; Verwey, 1999 , 2001 ; Verwey et al, 2002 , 2016 , 2022a ; Wiestler & Diedrichsen, 2013 ; Wright et al, 1996 ; Yokoi et al, 2017 ; Yokoi & Diedrichsen, 2019 ). These key-specific stimuli have sometimes been displayed simultaneously, after which the sequence was either immediately executed or only after onset of a ‘go’ stimulus (Schneider & Eberts, 1980 as cited and described in Schneider & Fisk, 1983 ; Wiestler & Diedrichsen, 2013 ; Wiestler et al, 2014 ; Wright & Shea, 1991 , 1994 ; Wright et al, 1996 ).…”