Electricity has been used in medicine for over 100 years. Today, brain stimulation is becoming more frequently used in various labs and clinics as a research tool for testing hypotheses about how motor and cognitive functions are performed by the cerebrum and the cerebellum, and how connections between these two brain regions support these functions. With regards to the cerebellum, this is partly because the lateral cerebellar hemispheres, which are thought to be involved in cognition (see below), are accessible to transcranial electrical stimulation, are sensitive to the effects of polarizing currents, and because the procedure is relatively inexpensive and easy to perform in human participants. The brain stimulation procedure described in the present article demonstrates how cognitive processes such as working memory and attention can be facilitated during tasks that are 'more' rather than 'less' cognitively demanding1. The interpretation of these task-specific results, are firmly constrained by an understanding of the physiology of the cerebro-cerebellar pathway. Neuro-enhancement effects, even when tasks are difficult, are also observed after electrical stimulation of the prefrontal cortex2,3,4,5.

The cerebellum plays an important role in predicting, timing and executing movements6. However, various lines of research now suggest that the cerebellum may influence cognitive processes. In the anatomical domain, for example, numerous studies have suggested that reciprocal connections between regions of the prefrontal cortex and the cerebellum (i.e., the cerebro-cerebellar pathway) might support cognition7,8,9,10,11,12. In the clinical domain, some patients with damage to specific parts of the posterior cerebellum present with intellectual and emotional problems whose symptoms are conceptualized in the 'dysmetria of thought' hypothesis, and clinically termed the 'cerebellar cognitive affective syndrome (CCAS), while those with damage to anterior portions of the cerebellum, present with motor impairments (e.g., ataxia) and conceptualized as 'dysmetria of movement'13,14,15. In the brain imaging domain, Schmahmann and colleagues16,17 have used functional magnetic resonance imaging (fMRI) and functional connectivity to map task-specific regions of the cerebellum and the connections these areas make with the prefrontal lobe during motor and cognitive tasks.

The cognitive tasks presented in this study were selected because they have previously been shown to activate so-called non-motor regions of the cerebellum. But they also enabled us to partition out motor and cognitive task components, which was achieved by varying the level of cognitive relative to motor demands that are required to perform them correctly, and the intervention of a brain stimulation procedure that has previously been shown to modulate brain-behaviour relationships. Recent attempts to modulate brain function and behaviour have included the use of polarizing currents across the scalp, termed, transcranial direct current stimulation (tDCS). In fact, clinicians have been stimulating the cerebellar cortex with implanted electrodes in patient populations since the 1970's with encouraging therapeutic results18. Today, stimulating the brain across the scalp is realised to be useful for studying brain-behaviour relationships in healthy participants.

TDCS in humans normally involves delivering a low (1-2 mA) direct current (DC) continuously through a pair of saline-soaked electrodes for 15-20 min. A typical electrode montage for stimulating the brain might involve one (anodal) electrode being placed on the head (over the brain region of interest), and the other (cathodal) electrode being placed on the cheek (cephalic) or shoulder (non-cephalic) on the contralateral side of the body. In the case of stimulating the cerebellum, intracerebral current flow between the two electrodes has relatively little functional spread to nearby regions (e.g., visual cortex19) and is thought to excite or depress Purkinje cells in the cerebellar cortex20, producing both neurophysiological and behavioural changes. The spread of current and effects of cerebellar-tDCS in humans are inferred from modelling data or from animal studies, and from indirect effects on the motor cortex. In the motor domain, the effects are also shown to be polarity-specific as evidenced by the consequences of cerebellar stimulation on motor cortex excitability20. For example, anodal stimulation generally has an excitatory effect and increases the output of Purkinje cells; increasing inhibition of the facilitatory pathway from the cerebellar nuclei to the cerebral cortex, while cathodal stimulation generally has an opposite effect i.e., dis-inhibition of the cerebral cortex by reducing Purkinje cell inhibition of the cerebellar nuclei. Anatomical studies in primates reveal how Purkinje cells could exert a facilitatory drive onto both motor and cognitive circuits, via a synaptic relay in the ventral-lateral thalamus21. However, recent tDCS studies in humans suggest that the anodal-cathodal distinction may not be clear cut. For example, the after-effects of tDCS over motor cortex are highly variable between individuals, and are not always polarity-specific22. Similar criticisms are also levied towards results in the cognitive domain23. This may help to explain why effects on cognitive functions are more difficult to detect and to interpret than the direct effects of the cerebellum on motor areas due to cerebellar-brain inhibition (CBI20). Such observations highlight the need to better understand individual factors that determine the efficacy of brain stimulation, and to develop improved protocols for stimulating the brain.

Changes in both motor and cognitive functions are physiologically plausible via electrical stimulation of the cerebello-thalamo-cortical pathway24. With regards to cognitive functions, a modulatory effect of cerebellar-tDCS on verbal working memory has been reported25,26. And lasting effects on cognition from stimulating regions of the prefrontal cortex are also observed2,3,4,5. However, the physiological effects of brain stimulation on neurons are different depending on whether behaviour is tested during (on-line effects) or after (off-line effects) the stimulation period27. It has been suggested that on-line effects may include changes in the intracellular environment (e.g., ion concentrations) and the electrochemical gradient (e.g., membrane potentials), while off-line effects might include longer lasting changes in neural activity due to altered intracellular processes (e.g., receptor plasticity)27. The present study investigates off-line effects, whereby tDCS is applied in-between two sessions of cognitive testing, and behaviour is compared between the two sessions.

Investigating a role for the cerebellum in cognition is assisted by the use of tasks that have previously been shown to involve cerebellar functioning. One particular task involves arithmetic reasoning and divided attention and is called the Paced Auditory Serial Addition Task (PASAT28). It has been used extensively to assess various cognitive functions in both healthy and patient populations. The test typically involves participants listening to numbers presented every 3 sec, and adding the number they hear to the number they heard before (rather than giving a running total). It is a challenging task and imposes a high degree of WM, attention and arithmetic ability. It also involves activity in the cerebrum and the cerebellum associated with these particular elements of the task as revealed on PET29 and MRI30. To make the task more cognitively difficult and attentionally demanding (as confirmed by others in a recent study31, the original instructions were changed so that participants were required to subtract the number they hear from the number they heard before. We call this new task the Paced Auditory Serial Subtraction Task (PASST1), and it is more difficult to perform than the PASAT as evidenced by subjective ratings of task difficulty and significantly longer reaction times1. Both versions of the task were included so that one was more cognitively difficult and attentionally demanding to perform than the other, while motor demands (covert speech operations) were comparable between tasks. If the cerebellum is involved in cognition, then perturbing its function with tDCS might interfere with the role of this structure during performance on the PASST, but not necessarily on the PASAT.

Another task used extensively to investigate a role for the cerebellum during speech and language aspects of cognition is the Verb Generation Task (VGT32,33,34,35,36,37). Like the PASAT, it has been used extensively to test verbal working memory in healthy and patient populations. Basically, the VGT requires participates to say aloud a verb (e.g., drive) in response to a visually presented noun (e.g., car), compared with performance on a control task whereby participants read nouns aloud. Generating verbs and reading nouns have similar perceptual and motor demands, but different verbal WM demands (i.e., greater semantic analysis). And greater activity in a cerebro-cerebellar network is associated with generating verbs compared with reading of nouns34,35,36. Words are also generated more quickly (an effect of priming) when the tasks are repeated using the same words (in a random order) across blocks, and cerebro-cerebellar activity increases as observed on PET33 and fMRI37.

In this article, a procedure is described for applying tDCS over the cerebellum to investigate a role for this brain structure in cognition, together with two arithmetic (experiment one) and three language tasks (experiment two) of varying difficulty, which three separate groups of participants performed before and after the stimulation period. We hypothesized, given a role for the cerebellum in cognition, that performance on the more demanding tasks (i.e., PASST and verb generation) would be affected more by tDCS (off-line effects) than performance on the less demanding tasks (PASAT and noun/verb reading).