Beneficial effects of cerebellar tDCS on motor learning are associated with altered putamen-cerebellar connectivity: A simultaneous tDCS-fMRI study

• Published in: NeuroImage (Orlando, Fla.) Vol. 223; p. 117363
• Main Authors: Liebrand, Matthias, Karabanov, Anke, Antonenko, Daria, Flöel, Agnes, Siebner, Hartwig R., Classen, Joseph, Krämer, Ulrike M., Tzvi, Elinor
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.12.2020; Elsevier Limited; Elsevier
• Subjects: Adult; Brain Mapping; Cerebellum; Cerebellum - physiology; Cortex (frontal); Cortex (motor); Electrical stimulation of the brain; ESB; Explicit knowledge; Female; fMRI; Frontal gyrus; Functional magnetic resonance imaging; Humans; Learning - physiology; Magnetic Resonance Imaging; Male; Middle Aged; Motor Cortex - physiology; Motor sequence learning; Motor skill learning; Neural Pathways - physiology; Neuroimaging; Psychomotor Performance - physiology; Putamen; Putamen - physiology; Reaction Time; Reaction time task; Rehabilitation; Supplementary motor area; tDCS; Transcranial Direct Current Stimulation; Young Adult; Cerebellum; RT; M1; IPL; RmANOVA; RND; MNI; GLM; IFG; BMA; BOLD; CB; STIM; Pu; SMA; PMC; DCN; DCM; fMRI; tDCS; Motor sequence learning; SMP; SRTT; COND; SEQ
• ISSN: 1053-8119; 1095-9572
• DOI: 10.1016/j.neuroimage.2020.117363

Non-invasive transcranial stimulation of cerebellum and primary motor cortex (M1) has been shown to enhance motor learning. However, the mechanisms by which stimulation improves learning remain largely unknown. Here, we sought to shed light on the neural correlates of transcranial direct current stimulation (tDCS) during motor learning by simultaneously recording functional magnetic resonance imaging (fMRI). We found that right cerebellar tDCS, but not left M1 tDCS, led to enhanced sequence learning in the serial reaction time task. Performance was also improved following cerebellar tDCS compared to sham in a sequence production task, reflecting superior training effects persisting into the post-training period. These behavioral effects were accompanied by increased learning-specific activity in right M1, left cerebellum lobule VI, left inferior frontal gyrus and right inferior parietal lobule during cerebellar tDCS compared to sham. Despite the lack of group-level changes comparing left M1 tDCS to sham, activity increase in right M1, supplementary motor area, and bilateral middle frontal cortex, under M1 tDCS, was associated with better sequence performance. This suggests that lack of group effects in M1 tDCS relate to inter-individual variability in learning-related activation patterns. We further investigated how tDCS modulates effective connectivity in the cortico-striato-cerebellar learning network. Using dynamic causal modelling, we found altered connectivity patterns during both M1 and cerebellar tDCS when compared to sham. Specifically, during cerebellar tDCS, negative modulation of a connection from putamen to cerebellum was decreased for sequence learning only, effectively leading to decreased inhibition of the cerebellum. These results show specific effects of cerebellar tDCS on functional activity and connectivity in the motor learning network and may facilitate the optimization of motor rehabilitation involving cerebellar non-invasive stimulation.