Consensus paper: Language and the cerebellum: an ongoing enigma

Abstract

In less than three decades, the concept "cerebellar neurocognition" has evolved from a mere afterthought to an entirely new and multifaceted area of neuroscientific research. A close interplay between three main strands of contemporary neuroscience induced a substantial modification of the traditional view of the cerebellum as a mere coordinator of autonomic and somatic motor functions. Indeed, the wealth of current evidence derived from detailed neuroanatomical investigations, functional neuroimaging studies with healthy subjects and patients and in-depth neuropsychological assessment of patients with cerebellar disorders shows that the cerebellum has a cardinal role to play in affective regulation, cognitive processing, and linguistic function. Although considerable progress has been made in models of cerebellar function, controversy remains regarding the exact role of the "linguistic cerebellum" in a broad variety of nonmotor language processes. This consensus paper brings together a range of different viewpoints and opinions regarding the contribution of the cerebellum to language function. Recent developments and insights in the nonmotor modulatory role of the cerebellum in language and some related disorders will be discussed. The role of the cerebellum in speech and language perception, in motor speech planning including apraxia of speech, in verbal working memory, in phonological and semantic verbal fluency, in syntax processing, in the dynamics of language production, in reading and in writing will be addressed. In addition, the functional topography of the linguistic cerebellum and the contribution of the deep nuclei to linguistic function will be briefly discussed. As such, a framework for debate and discussion will be offered in this consensus paper.

Fig. 1

Effective connectivity of overt speech production (modified after [56]). Dynamic causal modeling of data from a meta-analysis of 18 functional imaging studies of overt speaking (including 261 normal subjects) and from an fMRI study of word generation (including 20 participants). According to this model, the cerebellum is part of a sub-cortical pathway receiving input from Broca's area (BA 44) via the left anterior insula and projecting onto left primary motor cortex (M 1) via the (left) ventral premotor cortex (PMC). This model suggests that cerebellar involvement in speech is located hierarchically lower than the motor planning centers of left anterior cerebral cortex

Fig. 2

Average syllabic cycle rates of /pa/, /ta/, and /ka/ (per second) in the context of a sentence production task (filled circles) and a syllable repetition (DDK) task (open circles; adapted from [67]). In sentence production, the target syllables were in the stressed position of an embedded pseudoword. In the DDK condition, subjects were instructed to produce the target syllables as fast as possible. Error bars represent one standard deviation. NOR normal participants (N =32), ATX patients with hereditary cerebellar ataxias (N =15), AOS patients with apraxia of speech after stroke (N =15). The ATX and AOS groups were matched for speaking rates. While normal subjects and AOS patients were able to increase their production rates in the DDK condition, cerebellar patients failed to accelerate their syllable productions. This was ascribed to a failure of cerebellar patients to adapt to the novel and highly specific requirements of the task of repeating a syllable at maximum rate

Fig. 3

The cerebellum is selectively involved in the articulatory control process within the phonological loop of verbal working memory. a Schematic of the phonological loop according to Baddeley [79]. Visual input is translated into a phonological representation prior to entering storage. Auditory input has direct access into storage, and no translation is required. Subvocal repetition refreshes the phonological storage information so that it can be maintained. b Evidence from neuroimaging data shows that the superior (Lobules VI/Crus I) and inferior (Lobules VIIb/VIII cerebellum make separate contributions to articulatory control. Column (1): a conjunction analysis identified regions of activation during working memory and motoric rehearsal (shown in red) vs. working memory but not motoric rehearsal (shown in blue) [104]. The superior cerebellum was involved in both tasks, supporting a motor-related translation function that supports working memory. The inferior cerebellum (shown in blue) was specifically involved in the working memory task separate from motor demands. Column (2): a temporal analysis of verbal working memory revealed superior cerebellar activity specifically during translation, and inferior cerebellar activity specifically during storage [99]. Column (3): a visual vs. auditory working memory study revealed modality-specific cerebellar regions [105]. Red regions in the superior cerebellum represent greater activity for visual stimuli than auditory stimuli, consistent with the notion that visual information requires translation, whereas auditory information does not. There was an absence of visual vs. auditory activation differences in the inferior cerebellum (area shown in stippled red circle), indicating that both modalities relied equally on this region to maintain information once entered into phonological storage

Fig. 4

Event-related potentials (ERP) demarking a sparse syntactic positivity shift (SPS) to morphological syntax violations in patients with ischemic cerebellar lesions in opposite to healthy controls. On the left, the grand average of ERP response (black dotted line correct syntax; red line syntax violation) of the patient as well as the healthy control group is depicted. As displayed on the right, source analysis found increased activities of homologous Broca and left supramarginal area, suggesting aberrant syntax processing in terms of compensating lack of cerebellar feed forwarding contributions

Fig. 5

Handwriting sample of the Dutch target sentence (Het is vandaag een mooie dag.) demonstrating some of the characteristic features of apraxic agraphia

Fig. 6

Quantified Tc-99m-ethyl cysteinate dimer SPECT showing a significant hypoperfusion in the right cerebellar hemisphere associated with decreased perfusion in the medial and lateral regions of the prefrontal language dominant hemisphere (crossed cerebello-cerebral diaschisis)

Fig. 7

Cerebellar involvement in reading skill development. Figure 7 is our attempt to represent developmental changes in reading, with later skills “scaffolded” by earlier skills, and the roles of these two cerebellar-cortical networks

Fig. 8

Topographic arrangement in cerebellum of speech versus language representation. Functional MRI localizes articulation (a) to medial parts of lobule VI bilaterally, whereas verb generation (b) activates lateral regions of lobule VI and Crus I on the right [259]. In a meta-analysis of functional imaging studies [34] higher level language tasks engage the right lateral posterior cerebellum, lobules VI and Crus I (c) according to the lobule identification in (d) [260]. Case studies of cerebellar stroke patients reveal topography for articulation vs. higher-level language tasks. A patient with stroke in the territory of the right superior cerebellar artery (e, black shading) involving lobules I–VI was dysarthric; whereas a patient with stroke in the territory of the right posterior inferior cerebellar artery (f, black shading) involving lobules VII–IX was not dysarthric but performed poorly on the Boston Naming Test [261]

Fig. 9

Activation of the cerebellar cortex in a verb generation task [228]. a Cerebellar cortical activations of the contrasts aloud reading MINUS silent reading, and b (silent) verb generation MINUS silent reading. Activations of the cerebellar cortex are mapped onto coronal sections of the SUIT maximum probability template [262]. A t value of 7.75 represents the threshold of p <0.05 (FWE corrected). The positions of the coronal slices are shown in the sagittal view from y =−79 to −53 mm. L left, R right

Fig. 10

Activation of the dentate nuclei in a verb generation task [220]. Dentate nucleus activations of the contrasts aloud reading MINUS silent reading on the right (A) and left (B), and (silent) verb generation MINUS silent reading on the right (C) and left (D). Activations are mapped onto axial slices of the dentate template [262]. Color coding represents associated t values (threshold p <0.05, Bootstrap corrected, t =3.72)