In this study we explored the role of the cerebellum in ToM. We found that a lesion to the left cerebellum, and more specifically to the left Crus I and lobule VI, led to a deficit in cognitive ToM but not affective ToM. We also found that disconnection of the cerebello-cortical pathways through the left fronto-striatal tract and the left thalamic projection were more likely to result in cognitive ToM deficits.
Overall, these findings suggest that the left cerebellum contributes to the cognitive processes of mental state attribution.
The difference between cognitive and affective Theory of Mind
To our knowledge, our study is the first to report that the cerebellum is an important node in the Cognitive but not in the Affective ToM network. This is in line with previous findings suggesting a distinct neural network for each ToM process 33. Our study adds a novel region to these networks.
The role of the cerebellum in Theory of Mind neural network
The role of the cerebellum in social cognition emerged in the last decade. In a first meta-analysis, Van Overwall et al reported that cerebellar “social” clusters overlapped with nonsocial function clusters 13. Therefore, they argued that the cerebellum provides a domain-general support of social cognition 13. However, after reporting that their mentalizing clusters were located mostly within the default network9, they concluded that the cerebellum provides a domain-specific process for social cognition 10.
Regarding the anatomical localization of cerebellar regions that are associated with mentalism, we found a ToM cluster only for the cognitive task, and only in the left cerebellar hemisphere. Our clusters were more lateral than previously described. When compared to the ToM activation map of King et al, our clusters are outside the ToM map and are all within region 6 (Active maintenance, divided attention, verbal fluency) 20. Also, when compared to the Buckner et al 7 network map, our clusters are not within the default network but within the ventral attention network and the executive/cognitive network 9. These differences may be related to the difference in the subject sample, the tasks used and our analytic approach. However, even in the previous studies, there were inconsistencies regarding which cerebellar lobules were involved and if a laterality effect existed. Van Overwall et al reported that person mentalizing clusters were associated with the right Crus I, left and right lobule VI and right lobule IV 13. But when using another type of analysis, the clusters were encompassed in left and right Crus II 8. Moreover, King et al reported that most of the ToM activations were within left and right Crus I and II (with a larger lateral spread on the right side) but with extension to right lobule VI and IX and to the midline (vermis) 20. However, in a recent functional neuroimaging study, it was reported that impairment on a complex ToM task was associated with decreased volume of the left lobule VI 34. Our results corroborate these latter findings.
The role of the cerebellum in cognitive Theory of Mind
It is widely accepted that the cerebellum has a role in predicting motor outcome and signaling the cortex when errors are detected, in order to update the motor signal and reduce errors in future movements 35. Similarly to motor activity, social behavior also require anticipation and adaptation 36, 37. Motor and space processing may help characterize environmental constraints on social behavior by processing of physical boundaries, agent sequences, and coordination. In particular, adaptation and prediction of the behavior of the self and others could be a very specific contribution that the Cerebellum makes to understanding the intent of others 14,38. This idea supports previous arguments claiming that the cerebellum regulates cortical functions for complex social behaviors by enhancing the feedforward control that is necessary to perform these functions correctly 39,40. One hypothesis why the cerebellum may be involved in cognitive but not affective ToM results follows directly from this interpretation. Cognitive ToM is a more complex form of ToM compared to affective ToM because it subserves higher-order cognitive and metacognitive processes 34. Affective ToM tasks would require less prediction and therefore, would not tax the cerebellum as much as cognitive ToM. The Clausi et al findings support this by reporting no impairment in a task that assesses the ability to attribute emotions to others in a social context and argue that it was because the task requires reduced prediction and interplay between cognitive and emotional aspects 41.
Another hypothesis is that the role of the cerebellum in the cognitive ToM task is in controlling the sensorimotor aspects of ToM. Indeed, it was reported that Cognitive but not affective ToM deficit was also related to working memory performance 42. Our group has shown that the role of the cerebellum in executive function is supportive since it appears to primarily compute the motor component of working memory 26. Also, in patients with cervical dystonia, it was reported that only cognitive ToM was impaired in those with tremor compared to those without motor impairment 43. Therefore, one could hypothesize that cognitive ToM tasks rely more upon sensorimotor control than affective ToM tasks.
The role of the white matter tracts
The cerebellum is interconnected with the cerebrum via cerebello-cortical WM loops. In our study, the WM disconnection analysis revealed that damage to the WM pathways that include the “relay” structures of the cerebello-cortical WM connection, namely the thalamus and the striatum, were associated with poor performance in cognitive ToM. This finding suggests an important role for the cerebellum in the neural network that supports cognitive ToM and that integrity of the cerebello-cortical tracts is essential for cognitive ToM.
Limitations
All participants were male veterans and mostly Caucasian, therefore this limit our ability to generalize the results to other populations. Moreover, there are documented sex differences in ToM 44 which could not be addressed. As happens in longitudinal studies, participants in the current phase of the study are likely to have recovered better from their injury than patients who would be assessed shortly after their injury. Yet, our ability to identify impairments in this set of patients suggest that cerebellar damage can lead to poorer ToM ability even after several decades. Finally, as noted in the methods section, only CT images were used, but MRI and DTI tractography should also be used for white matter pathways identification in future studies with other patient populations.