Modulating Human Procedural Learning by Cerebellar Transcranial Direct Current Stimulation

Abstract

Neuroimaging studies suggest that the cerebellum contributes to human cognitive processing, particularly procedural learning. This type of learning is often described as implicit learning and involves automatic, associative, and unintentional learning processes. Our aim was to investigate whether cerebellar transcranial direct current stimulation (tDCS) influences procedural learning as measured by the serial reaction time task (SRTT), in which subjects make speeded key press responses to visual cues. A preliminary modeling study demonstrated that our electrode montage (active electrode over the cerebellum with an extra-cephalic reference) generated the maximum electric field amplitude in the cerebellum. We enrolled 21 healthy subjects (aged 20-49 years). Participants did the SRTT, a visual analogue scale and a visual attention task, before and 35 min after receiving 20-min anodal and sham cerebellar tDCS in a randomized order. To avoid carry-over effects, experimental sessions were held at least 1 week apart. For our primary outcome measure (difference in RTs for random and repeated blocks) anodal versus sham tDCS, RTs were significantly slower for sham tDCS than for anodal cerebellar tDCS (p = 0.04), demonstrating that anodal tDCS influenced implicit learning processes. When we assessed RTs for procedural learning across the one to eight blocks, we found that RTs changed significantly after anodal stimulation (interaction "time" × "blocks 1/8": anodal, p = 0.006), but after sham tDCS, they remained unchanged (p = 0.094). No significant changes were found in the other variables assessed. Our finding that anodal cerebellar tDCS improves an implicit learning type essential to the development of several motor skills or cognitive activity suggests that the cerebellum has a critical role in procedural learning. tDCS could be a new tool for improving procedural learning in daily life in healthy subjects and for correcting abnormal learning in neuropsychiatric disorders.

The impact of cerebellar transcranial direct current stimulation (tDCS) on learning fine-motor sequences

“…There was no difference in subjective ratings between the two stimulation groups, and the effects of stimulation were apparent the next day, which is unlikely to be a nonspecific enhancement of attention or arousal. This result is similar to other research indicating that the effects of tDCS are better observed at a delay [35,39,52] and to Study 1 in that no differences between the sham and anodal group were observed on the same day. It is possible that the aftereffect of cerebellar tDCS, which can last for up to 30 min after stimulation is over [33], could be directly enhancing consolidation processes.…”

“…These results together might suggest that cathodal stimulation does not lead to the exact behavioural inverse of anodal tDCS [49], and might depend on characteristics of the task. Differences in task or stimulation protocol may also explain the lack of effects of anodal tDCS on total learning during practice or sequence-specific learning, which was not consistent with the enhanced learning that Ferrucci et al [39] observed after anodal tDCS was applied after the baseline SRT task. We stimulated during practice of the sequences whereas they stimulated between two sessions of SRT task performance.…”

“…More specifically, we anticipate that anodal tDCS will lead to improvements in transfer performance, whereas cathodal tDCS will have a detrimental effect on transfer. Furthermore, as in [39], we expect to see a facilitatory effect of anodal tDCS on overall learning and sequence-specific learning, whereas cathodal tDCS would have the opposite effect. In this way, tDCS may have a facilitatory or inhibitory effect on error detection by affecting Purkinje cells [33], leading ultimately to stronger or weaker representations (internal models) in the cerebellum.…”

“…Other studies indicate that the effects of cerebellar tDCS are specific to the cerebellum, without significant spread to the occipital cortex [34][35][36] and do not significantly affect autonomic function [37,38]. It has been hypothesized that tDCS may affect Purkinje cells [33,39], which receive error signals from climbing fibres and in turn modulate deep cerebellar nuclei output to the cortex.…”

Non-invasive cerebellar stimulation in dystonia

“…Procedural learning assessed by the serial reaction time test (SRTT) can be improved in healthy adults by cerebellar TDCS [81,83].…”