Generalized role for the cerebellum in encoding internal models: evidence from semantic processing

Abstract

The striking homogeneity of cerebellar microanatomy is strongly suggestive of a corresponding uniformity of function. Consequently, theoretical models of the cerebellum's role in motor control should offer important clues regarding cerebellar contributions to cognition. One such influential theory holds that the cerebellum encodes internal models, neural representations of the context-specific dynamic properties of an object, to facilitate predictive control when manipulating the object. The present study examined whether this theoretical construct can shed light on the contribution of the cerebellum to language processing. We reasoned that the cerebellum might perform a similar coordinative function when the context provided by the initial part of a sentence can be highly predictive of the end of the sentence. Using functional MRI in humans we tested two predictions derived from this hypothesis, building on previous neuroimaging studies of internal models in motor control. First, focal cerebellar activation-reflecting the operation of acquired internal models-should be enhanced when the linguistic context leads terminal words to be predictable. Second, more widespread activation should be observed when such predictions are violated, reflecting the processing of error signals that can be used to update internal models. Both predictions were confirmed, with predictability and prediction violations associated with increased blood oxygenation level-dependent signal in the posterior cerebellum (Crus I/II). Our results provide further evidence for cerebellar involvement in predictive language processing and suggest that the notion of cerebellar internal models may be extended to the language domain.

Keywords: cerebellum; cognition; fMRI; internal models; language.

Figures

Figure 1.

Schematic of the trial structure for a trial in the Incongruent condition.

Figure 2.

BOLD activations in control analyses. a, Regions showing a positive correlation between RT and BOLD response. b, Sensorimotor activations, revealed by the contrast of Letter Strings > implicit experimental baseline. The cerebellar template has been oriented to reveal the peak activation in the superior cerebellum (lobule V). c, Regions involved in word processing, revealed by the contrast of Scrambled > Letter Strings. Images are thresholded at p < 0.005 (uncorrected) and show clusters surviving cluster-level FDR correction for multiple comparisons (q < 0.05). Cerebral activations are displayed on semi-inflated brain templates using the Caret software package (Van Essen, 2012), while cerebellar activations are displayed on the SUIT template (Diedrichsen, 2006) using MRIcron (Rorden et al., 2007). Complete unthresholded t-maps from all reported analyses can be downloaded from http://neurovault.org/collections/25/.

Figure 3.

Cerebellar regions sensitive to contextual predictability. a, Activations related to contextually predictable words revealed by the contrast of Congruent > Scrambled. b, Activations related to violations of predictability, revealed by the contrast of Incongruent > Congruent. c, Activations revealed by the contrast of Incongruent > Scrambled. d, Secondary tests for areas sensitive to prediction based on the contrasts of Incongruent > Scrambled (red), Congruent > Scrambled (green), and their overlap (yellow). e, Axial slice showing the activation patterns attributed by Imamizu et al. (2000) to error processing (red), an acquired internal model of a new tool (blue), and their overlap (orange). Reprinted with permission.

Figure 4.

Cerebral regions sensitive to contextual predictability.