Differential Behavioral and Neural Effects of Regional Cerebellar tDCS

Abstract

The human cerebellum contributes to both motor and non-motor processes. Within the cerebellum, different subregions support sensorimotor and broader cognitive functions, due to regional patterns in anatomical connectivity with the cerebral cortex and spinal and vestibular systems. We evaluated the effects of transcranial direct current stimulation (tDCS) targeting different cerebellar regions on language task performance and whole-brain functional activation patterns. Functional MRI data were acquired while 43 healthy young adults (15 males, 28 females; 23.3 ± 3.0 years) performed a sentence completion task before and after 20 min of 1.5 mA anodal tDCS. Participants received tDCS targeting either the anterior sensorimotor cerebellum (n = 11; 3 cm right of inion, over lobule V); the right posterolateral cerebellum (n = 18; 1 cm down and 4 cm right of inion, over lobule VII); or sham tDCS (n = 14). TDCS targeting the right posterolateral cerebellum improved task accuracy relative to the sham condition (p = 0.04) and increased activation in left frontal and temporal cortices relevant to task performance (post-tDCS > pre-tDCS; T 3.17, FDR p < 0.05 cluster correction). The regions of increased BOLD signal after right posterolateral cerebellar tDCS fell within the network showing functional connectivity with right cerebellar lobule VII, suggesting specific modulation of this network. In contrast, tDCS targeting the sensorimotor cerebellum did not impact task performance and increased BOLD signal only in one cluster extending into the precentral gyrus. These findings indicate that sensorimotor and cognitive functional cerebellar subregions differentially impact behavioral task performance and task-relevant activation patterns, further contributing to our understanding of the cerebellar modulation of motor and non-motor functions.

Keywords: cerebellum; cognition; functional MRI; language; motor; neuromodulation.

Figure 1.. Cerebellar anatomy.

Lobules I-IV = green, V = red / superior, VI = cyan, VII = blue, VIII = red / inferior, IX = yellow, X = light blue (from the Spatially Unbiased Infratentorial [SUIT] atlas of the cerebellum; Diedrichsen et al., 2009). Left, lateral view; middle, posterior view; right, superior view.

Figure 2.. Sentence completion task.

The target word was highly predictable for predictive trials, less predictable for non-predictive trials, and not predictable for scrambled trials (see D’Mello et al., 2017).

Figure 3.. Electrode montage used for electric field modeling in SimNIBS.

Active electrode (anode) was positioned based on individual participant MRI scans and the return electrode (cathode) was positioned over the right jaw bone to approximate the right clavicle.

Figure 4.. Active electrode placement and estimated electric fields for active tDCS groups.

Electrode positions for two representative participants with the electrode targeting the sensorimotor (top; red – centered 3 cm lateral to inion) and cognitive (bottom; blue – centered 4 cm lateral and 1 cm inferior to inion) cerebellum, and the position of the center of the electrode relative to the underlying brain anatomy. Estimated electric field maps (right, thresholded from −3.0 to −6.0) for the sensorimotor (red-yellow) and cognitive (blue-green) target groups reveal both overlapping and distinct electric fields.

Fig 5.. Mean accuracy across groups, sentence type, and time point.

The violin plots show the distribution of the data, black dots represent individual participants, and white diamonds indicate mean accuracy.

Fig 6.. Mean accuracy across groups and time point.

The violin plots show the distribution of the data, black dots represent individual participants, and white diamonds indicate mean accuracy.

Fig 7.. Median response times (msec) across groups, sentence type, and time point.

The violin plots show the distribution of the data, black dots represent individual participants, and white diamonds indicate median response times.

Fig 8.. Median response times (msec) across groups and time point.

The violin plots show the distribution of the data, black dots represent individual participants, and white diamonds indicate median response times.

Fig 9.. Pre-tDCS task activation across all groups.

Results thresholded at peak FWE p<0.05, FDR cluster p<0.05. IFG = inferior frontal gyrus; IOG = inferior occipital gyrus; medSFG = medial superior frontal gyrus; MOG = middle occipital gyrus; MTG = middle temporal gyrus; PostCG = postcentral gyrus; PreCG = precentral gyrus; SFG = superior frontal gyrus; SMG = supramarginal gyrus; STG = superior temporal gyrus

Figure 10.

Increased activation after tDCS. Post > pre comparisons within groups. Light blue = sham post > pre; red = sensorimotor post > pre; blue = cognitive post > pre.

Figure 11.

Decreased activation following tDCS. Pre > post comparisons within groups. Light blue = sham pre > post; green = sensorimotor pre > post.

Fig 12.. Cognitive post > pre-tDCS activation in the context of resting state connectivity of right cerebellar lobule VII.

Pre-tDCS resting state connectivity from right VII seed in all participants is shown in orange-yellow (p<0.001, FDR p<0.05 cluster correction; n=44 participants). Blue = Cognitive group post > pre-tDCS (t 3.17, FDR p<0.05 cluster correction).