Information-based rhythmic transcranial magnetic stimulation to accelerate learning during auditory working memory training: a proof-of-concept study

Heather T Whittaker; Lina Khayyat; Jessica Fortier-Lavallée; Megan Laverdière; Carole Bélanger; Robert J Zatorre; Philippe Albouy

doi:10.3389/fnins.2024.1355565

Information-based rhythmic transcranial magnetic stimulation to accelerate learning during auditory working memory training: a proof-of-concept study

Front Neurosci. 2024 Apr 4:18:1355565. doi: 10.3389/fnins.2024.1355565. eCollection 2024.

Authors

Heather T Whittaker^{1

2}, Lina Khayyat¹, Jessica Fortier-Lavallée³, Megan Laverdière³, Carole Bélanger³, Robert J Zatorre^{1

2}, Philippe Albouy^{1

2

3}

Affiliations

¹ Cognitive Neuroscience Unit, Montreal Neurological Institute, McGill University, Montréal, QC, Canada.
² International Laboratory for Brain, Music and Sound Research (BRAMS) - Centre for Research on Brain Language and Music (CRBLM), Montreal, QC, Canada.
³ CERVO Brain Research Centre, School of Psychology, Université Laval, Québec City, QC, Canada.

Abstract

Introduction: Rhythmic transcranial magnetic stimulation (rhTMS) has been shown to enhance auditory working memory manipulation, specifically by boosting theta oscillatory power in the dorsal auditory pathway during task performance. It remains unclear whether these enhancements (i) persist beyond the period of stimulation, (ii) if they can accelerate learning and (iii) if they would accumulate over several days of stimulation. In the present study, we investigated the lasting behavioral and electrophysiological effects of applying rhTMS over the left intraparietal sulcus (IPS) throughout the course of seven sessions of cognitive training on an auditory working memory task.

Methods: A limited sample of 14 neurologically healthy participants took part in the training protocol with an auditory working memory task while being stimulated with either theta (5 Hz) rhTMS or sham TMS. Electroencephalography (EEG) was recorded before, throughout five training sessions and after the end of training to assess to effects of rhTMS on behavioral performance and on oscillatory entrainment of the dorsal auditory network.

Results: We show that this combined approach enhances theta oscillatory activity within the fronto-parietal network and causes improvements in auditoryworking memory performance. We show that compared to individuals who received sham stimulation, cognitive training can be accelerated when combined with optimized rhTMS, and that task performance benefits can outlast the training period by ∼ 3 days. Furthermore, we show that there is increased theta oscillatory power within the recruited dorsal auditory network during training, and that sustained EEG changes can be observed ∼ 3 days following stimulation.

Discussion: The present study, while underpowered for definitive statistical analyses, serves to improve our understanding of the causal dynamic interactions supporting auditory working memory. Our results constitute an important proof of concept for the potential translational impact of non-invasive brain stimulation protocols and provide preliminary data for developing optimized rhTMS and training protocols that could be implemented in clinical populations.

Keywords: EEG; TMS; cognition; fronto-parietal network; memory; theta oscillations.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by a CIHR Foundation grant to RJZ; by NSERC Discovery grants to PA and RJZ; and by a grant from the Healthy Brains for Healthy Lives initiative of McGill University under the Canada First Research Excellence Fund to RJZ. HTW is supported by CIHR via a Vanier Canada Graduate Scholarship. RJZ is a fellow of the Canadian Institute for Advanced Research and is funded via the Canada Research Chair Program and by FPA RD-2021-6 Scientific Grand Prize from the Fondation pour l’Audition (Paris). PA was supported by FRQS Junior 1 grant and is now supported by FRQS Junior 2 grant.