Introduction

Developmental dyslexia is a neurogenetic disorder characterized by severe difficulty in reading acquisition despite normal intelligence, education, and motivation [1]. Neuroimaging studies have revealed that developmental dyslexia is associated with dysfunctions in the left perisylvian language areas, including the left temporoparietal cortex (consisting of the posterior superior temporal gyrus, the angular gyrus, and the supramarginal gyrus), the occipital-temporal cortex, and the inferior frontal cortex. The temporoparietal cortex is assumed to support the mapping from graphemes to phonemes [2–5], whereas the occipital-temporal cortex is important for orthographic (print) processing [6]. The inferior frontal gyrus is implicated in articulatory processes and the active analysis of phonological elements of written words [7].

Besides dysfunctions in the cerebral cortex, dyslexic readers also show structural and functional abnormalities in the cerebellum [8–11]. Structural studies have revealed that dyslexic readers show decreased gray matter volume (GMV) in the cerebellar regions [9, 12–15] and atypical asymmetry of the cerebellum [16, 17]. Interestingly, the coordinates of the cerebellar abnormality reported in different studies were quite close, centering on the lobule VI of the left and right cerebellum [13, 14, 18, 19]. In a study with German-speaking dyslexics, the most significant structural abnormality was found in the bilateral anterior cerebellum (extending into lobule VI). Additionally, the GMV in this region was positively correlated with literacy skills, including reading speed, spelling, rhyme detection, and digit naming [9]. Besides, researchers found that a region of the right lobule VI of the cerebellum was the most predictive of whether an adult reader had dyslexia or not [20].

Functional neuroimaging studies have also revealed atypical cerebellar activation in individuals with dyslexia [8, 10, 11, 21–23]. However, most studies have adopted motor-related tasks [8, 21–23], probably due to the behavioral observation that some individuals with dyslexia show deficits in motor skills [24–26], along with the general opinion that the cerebellum is mainly engaged in motor processing. Nevertheless, the association between performance on motor tasks and reading or reading difficulty is still a matter of debate [27, 28] and the cerebellum is thought to be also involved in other cognitive processes, rather than confined to motor process [29, 30]. Particularly, given that the typical symptom of dyslexia is reading impairment rather than a motor deficit, using language tasks to investigate this question is reasonable. Up to now, only a few neuroimaging studies have adopted language tasks to explore the alteration of cerebellar function in dyslexic readers. One study, by Baillieux and colleagues, used a silent word generation task and found that dyslexic children showed more widespread and diffuse activations in the cerebellum compared to typically developing children [10]. Specifically, a recent fMRI study reported reduced activation in lobule VI of the right cerebellum in individuals with dyslexia. The double-deficit group (children with both rapid naming and phonological impairment) showed less cerebellar activation compared to children with only rapid naming impairment, who in turn showed less activation than the typically developing children. The reduced activation in children with dyslexia was only found in a written word rhyming task, but not in a written word semantic decision task [11]. In contrast, a meta-analysis of functional neuroimaging studies of dyslexia revealed overactivation of the cerebellum in reading tasks which, the authors suggested, was the consequence of increased effort or compensatory strategies of dyslexia during reading tasks [18]. Finally, the reciprocal connections between the right cerebellum and the phonological processing areas (the left inferior frontal gyrus and the left lateral temporal cortex) are believed to be important for fluent reading [31], but dyslexic readers showed altered cerebro-cerebellar functional connectivity during phonological tasks [32].

Despite much research, the role of the cerebellum in dyslexia is still far from clear. Although abnormal activation of the cerebellum has been observed in phonological processing during word reading, it has yet to be determined whether orthographic processing of written words, which requires an elaborate analysis of visual features, such as spatial configurations [33] and line junctions [34], also involves in altered cerebellar activity in dyslexic readers. Importantly, growing evidence suggests that the cerebellum is involved in visual and spatial processing, e.g., line bisection judgment [35], visual-perceptual learning [36], and visual-spatial rotation [37], in line with the clinical findings that visual–spatial difficulties follow cerebellar lesions [38, 39].

In the present study, we used visually-presented orthographic and phonological tasks to explore the functional activation of the cerebellum and the cerebro-cerebellar functional connectivity in children with dyslexia and in their matched typically developing children. We applied a high-resolution atlas template of the human cerebellum, which was recently developed for better normalization [40], allowing a more precise examination of the functions of the human cerebellum in young readers.

Materials and Methods

Participants

Twenty typically developing readers (13 females, mean age = 10.31 years, standard deviation [SD] = 1.0) and fourteen children with dyslexia (3 females, mean age = 10.19, SD = 0.68) were included and analyzed in the current study. Originally, twenty dyslexic children participated in the experiment but six were excluded due to excessive head motion during scanning. The participants were fourth- or fifth-grade children, screened from hundreds of children from several primary schools in Beijing. They were native Mandarin speakers and had no neurological disorders. All the participants were right-handed according to the Edinburgh Handedness Inventory [41] and had normal intelligence as assessed by Raven’s Standard Progressive Matrices [42]. In particular, parents’ reports and ratings were used to verify that children in our study had no attention deficit hyperactivity disorder (ADHD) [43]. This study was approved by the Institutional Review Board of the National Key Laboratory of Cognitive Neuroscience and Learning at Beijing Normal University, and written consent was obtained from all children and their parents.

Dyslexia Criteria and Behavioral Tests

Children were categorized as having dyslexia if they scored either (1) at least 1.5 SD below the norm in a Chinese character recognition test or (2) at least one SD below the norm in the Chinese character recognition test and at least 1.5 SD below in a Chinese phonological awareness test [44, 45]. These screening criteria for detecting Chinese children with dyslexia have also been used in previous studies [46–48]. The control group of typically developing readers all scored one SD above the norm in both the Chinese character recognition test and the Chinese phonological awareness test.

A battery of cognitive tests was also administered after the MRI scanning to evaluate children’s reading performance. This battery includes three reading tests: (1) a Chinese vocabulary test to assess the quality and breadth of children’s vocabulary [49]; (2) a reading comprehension test to assess efficiency of extracting meaning from written words and sentences [50]; and (3) a rapid digit naming test to measure automatization process [51]. We also administered a digit cancelation test to get a quantitative measure of children’s sustained attention ability [52]. The two groups of participants (14 dyslexic readers and 20 typically developing readers) were matched on age, gender, handedness, attention ability, and non-verbal IQ. The demographic information and scores on the cognitive and reading-related tests of the dyslexic readers and typically developing readers are shown in Table 1.

Table 1 Demography and performance of reading and cognitive tests
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fMRI Task and Procedure

Prior to the experimental scanning session, children underwent a 20-min training session in a mock scanner. This training session aimed to help children familiarize with the MRI environment and task instructions and to prepare them to keep their head motionless throughout the scanning. Immediately following the training session, children were tested in the actual MRI scanner.

During fMRI acquisition, participants performed an orthographic task and a phonological task. Both have been previously used to investigate the neural basis of reading as well as the neural deficits of dyslexia [50, 53–56]. There were two scanning runs, one for each task. For the orthographic task, participants read two visually presented characters and judged, as quickly and accurately as possible, whether the characters were similar in shape or not (for examples, see Fig. 1). For the phonological task, two Chinese characters were visually presented and participants were required to judge whether they rhymed or not. Participants were instructed to press a button on a response box with one index finger for “yes” responses and another for “no” responses, as determined in advance.

Fig. 1
figure 1

Task design for both tasks: orthographic (left) and phonological (right) task. Participants had to indicate whether the characters had similar shapes or whether they rhymed via a button press

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A block design was used, where four blocks of experimental trials were alternated with five blocks of control trials (a condition where participants were fixating a point centered on the screen) in each scanning run. Varying durations for experimental blocks were used to counter the potential artifact of periodic noise resulting from physiological rhythms or participants’ expectation [50]. The number of trials in each experimental block ranged from 8 to 12, and the duration for each control block of trials was fixed at 24 s. In each trial, a pair of words was displayed for 2500 ms, one to the left and one to the right of a central fixation point on the screen, followed by a 500 ms blank interval. The average duration for each experimental block was 30 s and the total time for a scanning run was 4 min.

Image Acquisition

Scans were acquired with a 3.0 T Siemens MRI scanner at the MRI center in Beijing Normal University. Functional images were acquired using a gradient-echo planar imaging sequence sensitive to brain oxygen-level dependent (BOLD) contrast. The parameters were as follows: 40 contiguous axial slices, 3 mm thickness, TR = 2400 ms, flip angle = 81°, TE = 30 ms, in-plane resolution = 3 × 3 mm, matrix = 64 × 64 [57]. High-resolution T1-weighted 3D images were acquired with following parameters: axial slices = 176, slice thickness = 1 mm, TR = 2300 ms, flip angle = 9°, TE = 4.18 ms, in-plane resolution = 1 × 1 mm, FOV = 256 × 256, matrix = 256 × 256.

fMRI Data Preprocessing

Data Preprocessing in the Cerebellum with SUIT

Given the rather small size of functional subunits in the cerebellum and the considerable anatomical variability between individuals, we conducted preprocessing with the SUIT-toolbox for SPM to improve the alignment of infra-tentorial anatomical and functional areas. SUIT is a new high-resolution atlas template of the human cerebellum and brainstem that is spatially unbiased (i.e., the location of each structure is equal to the expected location of the structure across individuals in Montreal Neurological Institute—MNI space). At the same time, the template preserves the anatomical detail of cerebellar structures through a nonlinear atlas-generation algorithm. By using automated nonlinear normalization methods, a more accurate inter-subject alignment than current whole-brain methods can be achieved [58].

Preprocessing procedure proceeded in the following steps: (1) The first five time points of each participant’s functional images were discarded to allow for equilibration of the magnetic field; (2) Slice timing correction and realignment of the functional data were performed to correct for acquisition time difference between slices and head movement, respectively; (3) The origin of the structural image to the anterior commissure was set manually and we then co-registered this high-resolution structural image to the mean functional image; (4) GLM analysis was performed to get the activation of task vs. fixation for each subject, in which a boxcar function of task was convolved with the HRF (the six head movement parameters were regarded as covariates); (5) The structural image of the cerebellum and the brainstem was isolated from the rest of the brain using the SUIT-toolbox and then normalized to the SUIT template using a nonlinear deformation; (6) The deformation parameters from the normalized step were used to warp the functional data (contrast images from the first-level GLM) to the cerebellum template with a resolution of isotropic 2*2*2 mm; (7) The normalized images were smoothed with an 6-mm FWHM Gaussian kernel.

Whole-Brain Data Preprocessing

We also conducted whole-brain analyses. Data pre-processing included slice timing, realignment, co-registration, tissue segmentation, normalization, and smoothing. Specifically, after discarding the first five time points of each participant’s functional images, the images were corrected for differences in slice-acquisition time to the middle slice and were realigned to the first volume in the scanning session. Functional images were co-registered with their corresponding anatomical volumes, and normalized to MNI stereotaxic space using parameters obtained from anatomical segmentation, and resampled to voxel size of 3*3*3 mm. Spatial smoothing was performed with a Gaussian filter (6 mm full width at half maximum).

fMRI Statistical Analyses

Group Comparisons for Cerebellar Activation

Individual subject’s activation brain maps were generated by using a general linear model in which the boxcar function of experimental condition was convolved with the canonical hemodynamic response and head movement parameters were regressed out as covariates. Then, the contrast images between experimental and fixation conditions from each subject were taken into a second-level random-effects model for group-level analysis. Whole-cerebellum activation was computed by using a one-sample t test, separately for each group and for each task (individual voxel p = 0.00001, cluster size >50 voxels, voxel size = 2*2*2, uncorrected). Then, a two-sample t test was performed to evaluate group differences in cerebellar activation between dyslexic readers and typically developing readers (individual voxel p = 0.001, cluster size >39 voxels, voxel size = 2*2*2, AlphaSim corrected to p = 0.05). A traditional whole-brain analysis was also computed to reconfirm the group differences in cerebellar activation based on the SUIT template and a new normalization technique. Additionally, the dyslexic readers in the current study exhibited a numerically higher scores on the Raven non-verbal intelligence test relative to the typically developing readers, though the group contrast was not statistically significant (t = −1.89, p = 0.07). To exclude the potential effect of non-verbal intelligence, we ran group comparisons for cerebellar activation with IQ as a covariate. We found that the results did not change so the subsequent analyses did not include IQ as a covariate.

Correlation Between Cerebellar Activation and Reading Performance

To characterize the relationship between regional activation in the cerebellum and reading performance, we further extracted and averaged the activation of all the voxels within a 6-mm sphere centered on the most significant voxel between group contrasts. The correlations between cerebellar activation and behavioral scores in each reading test were computed for each group.

ROI-Wise Cerebro-Cerebellar Functional Connectivity Analysis

The cerebro-cerebellar functional connectivity between two cerebellar seeds and 12 reading regions of interest (2*12 pairs) was computed in an ROI-wise way. We chose the 6-mm sphere centered on the most significant voxel between group contrasts in the cerebellum as cerebellar seeds. In addition, we selected 12 cortical regions of interest (ROIs), including 11 regions derived from a meta-analysis of brain activation during reading in children [59] and adults [60]. This set of seeds had been validated in previous fMRI studies [61, 62]. One additional region, the left supramarginal gyrus, was added based on a recent meta-analysis which found both structural and functional alterations in this region in dyslexia [18]. The 12 ROIs in the current study were the left inferior occipital gyrus (L.IOG), the left fusiform gyrus (L.FFG), the left posterior superior temporal gyrus (L.STG), the left temporoparietal junction (L.TPJ), the left intraparietal sulcus (L.IPS), the left supramarginal gyrus (L.SMG), the left dorsal precentral gyrus (L.PCG), the left supplementary motor area (L.SMA), the left inferior frontal gyrus pars opercularis (L.IFGop), the left inferior frontal gyrus pars triangularis (L.IFGtri), the left middle frontal gyrus (L.MFG), and the left thalamus (L.THAL). Each ROI was a sphere with a 6-mm radius, centered on the MNI coordinates listed in Table 2.

Table 2 MNI coordinates of the regions of interest
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To compute cerebro-cerebellar functional connectivity, the BOLD time series from the experimental blocks were extracted, converted into Z score, and then concatenated. For each participant, we calculated the mean time series of each ROI by averaging the signal across all voxels within the ROI. Pearson correlations were computed between cerebellar seeds and cortical ROIs, then, the correlation coefficients were converted to Z values using a Fisher’s r-to-z transformation. Finally, a random-effect group (typically developing, dyslexia) × task (orthography, phonology) ANOVA was conducted based on the Fisher’s Z scores of subject-specific cerebro-cerebellar functional connectivity.

Results

Behavioral Measures

Table 1 reports the demographic information and behavioral performance of dyslexic and typically developing readers. As can be seen in Table 1, the two groups did not differ significantly in age, non-verbal IQ, and gender. However, the typically developing readers performed significantly better than the dyslexic readers on almost all reading achievement tests, including the standardized measures of Chinese character recognition, Chinese vocabulary, reading comprehension and Chinese phonological awareness tests (Table 1; independent samples t tests, two-tailed, all ps < 0.05). We were therefore confident that the criterion of dyslexia in our study is effective. Notably, dyslexic readers in our study did not perform worse in rapid naming test, which means that dyslexic children in our study were not impaired in automatization process.

In-Scanner Performance

The inside-scanner behavioral data was partly missing due to unexpected technological problems. The in-scanner performance analysis was thus based on the remaining data of eight dyslexic readers and ten typically developing readers. Independent two sample t tests were computed separately for orthographic and phonological task to evaluate the group differences in accuracy and reaction time. In the orthographic task, there were no significant group differences in both accuracy (M = 0.95, SD = 0.07 and M = 0.94, SD = 0.05 for typically developing and dyslexic readers respectively, p > 0.45) and reaction time (M = 1083 ms, SD = 230 and M = 1195 ms, SD = 184 for typically developing and dyslexic readers respectively, p > 0.25). In the phonological task, there were also no significant group differences in both accuracy (M = 0.72, SD = 0.18 and M = 0.65, SD = 0.11 for typically developing and dyslexic readers respectively, p > 0.15) and reaction time (M = 1933 ms, SD = 228 and M = 1920 ms, SD = 319 for typically developing and dyslexic readers respectively, p > 0.30).

fMRI Results

Results for activation within each group were reported separately for the orthographic and the phonological tasks (see Table 3). In the orthographic task, both typically developing readers and dyslexic readers showed significant activation in the bilateral cerebellum Crus 1, which extended to lobule VI of the cerebellum. In the phonological task, typically developing readers activated the right cerebellum Crus 2 and bilateral Crus 1, but no cerebellar regions were significantly activated for the dyslexic readers. Independent two-sample t tests were computed to evaluate group differences in cerebellar activation between typically developing and dyslexic readers. In the orthographic task, results revealed more activation for dyslexic readers relative to typically developing readers in the bilateral lobule VI of the cerebellum (see Table 4 and Fig. 2a). However, no cerebellar regions showed significant group differences for the phonological task (see Table 4). Besides, a traditional whole-brain analysis was also conducted to reconfirm the group contrast results within the cerebellum. We found that the results in the cerebellum were validated, with a significant group difference in the bilateral cerebellum for the orthographic task (individual voxel p = 0.001, voxel size = 3*3*3, cluster size >12 voxels, AlphaSim corrected to p = 0.05), while no significant group difference in the cerebellar regions was found for the phonological task even with a lenient threshold (individual voxel p = 0.01, voxel size = 3*3*3, cluster size >30 voxels, AlphaSim uncorrected) (see the supplementary results, Table S1).

Table 3 Coordinates of activation peaks for the orthographic and phonological tasks in the cerebellum
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Table 4 Cerebellar regions showing significant group differences in group contrasts separately for the orthographic and phonological tasks
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Fig. 2
figure 2

Group differences in the cerebellar activation. a Regions in red showed significant group difference in cerebellar activation during the orthographic task. b The eigenvalue of activation in the left cerebellum VI (−26,−48,−38) in both the orthographic and phonological task. c The eigenvalue of activation in the right cerebellum VI (26, −46, −30) in both the orthographic and phonological tasks. Error bars represent the standards error (SE) of the difference between sample means. ***p < 0.005

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To illustrate the group difference within the bilateral lobule VI of the cerebellum in the phonological task, we further extracted the activation in the bilateral lobule VI of the cerebellum for each group for phonological processing. Results showed that the group difference in cerebellar activation was not significant in the phonological task, but a tendency for greater activation in dyslexic readers compared to typically developing readers was revealed (see Fig. 2b, c).

Cerebellum-Behavior Correlation

To further characterize the relationship between activation in the cerebellum and reading ability, we correlated standard score in each reading test with the eigenvalue of cerebellar activation in the orthographic task extracted from a 6-mm sphere centered on the most significant voxel in group comparisons. We found that scores in the Chinese vocabulary test were negatively correlated with the eigenvalue of activation in both the lobule VI of the left cerebellum (r = −0.54, p < 0.05, FDR uncorrected) and in lobule VI of the right cerebellum (r = −0.68, p < 0.01, FDR corrected) for the group of dyslexic readers (see Table 5, Fig. 3).

Table 5 Correlations between reading performance and bilateral cerebellar activation
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Fig. 3
figure 3

Negative correlations between bilateral cerebellar activation and Chinese vocabulary standard scores for the dyslexic readers. No significant correlation was found for typically developing readers

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ROI-Wise Cerebro-Cerebellar Functional Connectivity Analysis

We computed ROI-wise cerebro-cerebellar functional connectivity for each subject seeded in the bilateral lobule VI of the cerebellum (MNI: −26, −48, −33; 26, −46, −33) with 12 reading ROIs, and we further computed a 2 group (typically developing readers, dyslexic readers) × 2 task (orthography, phonology) mixed-model ANOVA analysis. For the seed in the right cerebellum, we found a significant interaction between group and task (F(1,32) = 5.197, p < 0.05) and a significant main effect of group (F(1,32) = 5.643, p < 0.05) in functional connectivity within the left fusiform gyrus. Specifically, in the orthographic task, dyslexic readers exhibited more functional connectivity between the right cerebellum and the left fusiform gyrus, but not in the phonological task (see Fig. 4b). For the seed of the left cerebellum, a significant interaction between group and task was revealed in the functional connectivity with the left supramarginal gyrus (F(1,32) = 5.669, p < 0.05). Specifically, dyslexic readers exhibited more functional connectivity between the left cerebellum and the left supramarginal gyrus in the phonological task than typically developing readers, but not in the orthographic task (see Fig. 4c). Note that results reported here did not survive the multiple comparisons for 2*12 pairs for functional connectivity.

Fig. 4
figure 4

Significant group × task interaction in ROI-wise cerebro-cerebellum functional connectivity. a Demonstration of cerebellar seeds and reading ROIs. b Functional connectivity between the right cerebellum and the left fusiform gyrus. c Functional connectivity between the left cerebellum and the left supramarginal gyrus. Error bars represent the SE of the difference between sample means. ***p < 0.005; **p < 0.01

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Discussion

This study investigated the cerebellar activation and cerebro-cerebellar functional connectivity in dyslexic readers in comparison with typically developing readers using basic reading tasks. We found that compared to typically developing readers, dyslexic readers showed an abnormally higher engagement of the bilateral cerebellum in the orthographic task, which was negatively correlated with literacy measures. Additionally, a tendency for higher cerebellar activation in children with dyslexia was revealed in the phonological task (the lack of significance might be a result of a fairly small sample size in the current study). For functional connectivity, during the orthographic task, stronger connections were observed in dyslexic readers compared to typically developing readers between the lobule VI of the right cerebellum and the left fusiform gyrus. On the other hand, for the phonological task, stronger functional connectivity was found in dyslexic readers relative to typically developing readers between the left lobule VI of cerebellum and the left supramarginal gyrus. These findings deepen our understanding of the role of the cerebellum in both reading and reading impairment.

Firstly, our study revealed that abnormal cerebellar activity in dyslexic readers was not specific to phonological processing but also manifested in the orthographic task. Previous studies addressing cerebellar abnormalities of dyslexia during reading mainly used phonological processing tasks [11, 32], which may be partly due to the predominant “phonological deficit” view of dyslexia [63]. The cerebellar deficit hypothesis of dyslexia postulated by Nicolson et al. proposed that a cerebellar impairment may lead to phonological deficits via an articulatory (motor) problem [64]. Our findings suggest that the role of the cerebellum in reading or in dyslexia should have to be reconsidered because it may not relate to the motor functions of the cerebellum. Interestingly, a recent meta-analysis of voxel-based morphometry (VBM) revealed that an abnormality in the bilateral lobule VI of the cerebellum may be specific to dyslexic readers, since it did not overlap with the cerebellar clusters identified in ADHD and autism spectrum disorders [19]. Our results confirmed this cerebellar abnormality from a functional perspective by revealing greater cerebellar activation in dyslexic readers when they performed our written language processing tasks. Notably, the region showed group differences was not significantly activated in typically developing readers in our study, which implies that the atypical activity observed in the lobule VI of the cerebellum is specifically related to dyslexia.

The overactivation of the bilateral lobule VI of the cerebellum may possibly be a kind of compensatory engagement of these regions during reading in dyslexic readers. Cerebellar overactivation in dyslexic readers has been reported in previous functional neuroimaging studies [65, 66]. Meanwhile, a recent meta-analysis also found overactivation of the cerebellum in dyslexic readers, and further revealed that the overactivated cerebellar region overlapped with the region manifesting structural differences between typically developing and dyslexic readers [18]. The authors proposed that cerebellar overactivation reflects the increased effort or compensatory strategies of dyslexic readers during written language processing. Our findings strongly support this proposal on account of higher engagement of the bilateral lobule VI of the cerebellum for orthographic processing and numerically greater but non-significant activation for phonological processing in dyslexic readers compared to typically developing readers. In addition, we found a negative correlation between dyslexic readers’ cerebellar activation and their reading performance. That is, with increasing reading difficulty, dyslexic readers showed more cerebellar activation. This finding indicates that as a compensatory region, the degree of engagement of the lobule VI of the cerebellum is determined by the severity of reading difficulty.

We further observed higher cerebro-cerebellum functional connectivity in dyslexic readers in both orthographic and phonological tasks. Specifically, atypically higher functional connectivity was observed between the left lobule VI of the cerebellum and the left fusiform gyrus in the orthographic task, whereas higher functional connectivity was found between the right lobule VI of the cerebellum and the left supramarginal gyrus in the phonological task. It was recently proposed that cortico-cerebellar loops are the basic neural substrate underlying the cerebellum’s cognitive role [67, 68]. Our results support this hypothesis by revealing that the cerebellum functions in combination with other cerebral regions which were critical for the current task, rather than functions alone in the implementation of compensatory processes for dyslexic readers. As a support for the existence of a compensatory cortico-cerebellar loop between the left supramarginal gyrus and the cerebellum, a diffusion-tensor imaging (DTI) study found that compared to typically developing readers, dyslexic readers have greater fractional anisotropy (FA) in white matter tracts connecting the cerebellum with the temporoparietal and inferior frontal regions (which are part of a network supporting reading processes) [69]. Greater FA in dyslexic readers has been hypothesized to be related to compensatory mechanisms leading to extra recruitment of neural resources, which consequently contribute to increased myelination or axonal packing [69]. The higher cerebro-cerebellar connections we found may serve as the basic neural substrates underlying the compensatory function of the cerebellum in dyslexic readers. More importantly, we found that the compensatory cerebro-cerebellum connections were dynamically modulated by the on-going reading tasks. Note that the left fusiform gyrus and the left supramarginal gyrus are critical regions for orthographic [6, 70] and phonological [71–73] processing, respectively. It seems that the role of the lobule VI of the cerebellum in dyslexic readers is flexible. The cerebellum works with the cerebral regions responsible for the on-going task and shifts the connection to other relevant cerebral regions when the task changes. An interesting issue is whether the cerebellum is left-lateralized for orthographic processing and right-lateralized for phonological processing in dyslexic readers. Indeed, for this group of readers, we found stronger connectivity on opposite sides of the lobule VI of the cerebellum in our orthographic and phonological tasks. Future studies are required to clarify this issue. Regardless, our findings offer novel information on how cerebellum is incorporated with cerebral regions for compensatory processing during reading in dyslexic readers.

In this study, we suggested the abnormality of cerebellum in dyslexia as a compensatory system, but we cannot exclude other hypotheses. For example, the increased activation and connectivity of cerebellum might be just a concomitant phenomenon of reading impairment. Contrary to our findings of cerebellar overactivation in dyslexic readers, some studies reported cerebellar deactivation in dyslexic readers [11, 74]. However, the cerebellar coordinates reported in these studies were various and not confined to the lobule VI of the cerebellum. This inconsistency probably results from the heterogeneity of dyslexia and the different inclusion criteria across studies. Besides, the inconsistencies across studies may also be due to different cognitive components or task demands and it suggests that the function of specific cerebellar subregions should be taken into consideration when interpreting cerebellar abnormality in dyslexia. It is important to note that the sample size of the current study is not very large and that the participants were native Chinese speakers. Thus, it is unclear whether our findings can be generalized to other linguistic populations. Though cerebellar abnormality has been found in dyslexic readers from both alphabetic [11, 14] and logographic writing systems [15, 75], direct comparisons of cerebellar activation and cerebro-cerebellum functional connectivity between dyslexic readers from different writing systems should be conducted to clarify this point in the future.

Conclusion

In the current study, we found that dyslexic readers showed higher bilateral engagement of the lobule VI of the cerebellum during reading tasks. This activation was negatively correlated with reading ability. In addition, the atypical cerebro-cerebellar functional connectivity in dyslexic readers was dynamically modulated by real-time tasks which might reflect the basic neural substrates for a compensatory role of the cerebellum in dyslexic readers. This suggests that cerebellar abnormalities in dyslexic readers could be better understood with an examination of the functional connectivity between the cerebellum and cerebral regions.