The Cerebellar Predictions for Social Interactions: Theory of Mind Abilities in Patients With Degenerative Cerebellar Atrophy

Abstract

Recent studies have focused on the role of the cerebellum in the social domain, including in Theory of Mind (ToM). ToM, or the “mentalizing” process, is the ability to attribute mental states, such as emotion, intentions and beliefs, to others to explain and predict their behavior. It is a fundamental aspect of social cognition and crucial for social interactions, together with more automatic mechanisms, such as emotion contagion. Social cognition requires complex interactions between limbic, associative areas and subcortical structures, including the cerebellum. It has been hypothesized that the typical cerebellar role in adaptive control and predictive coding could also be extended to social behavior. The present study aimed to investigate the social cognition abilities of patients with degenerative cerebellar atrophy to understand whether the cerebellum acts in specific ToM components playing a role as predictive structure. To this aim, an ad hoc social cognition battery was administered to 27 patients with degenerative cerebellar pathology and 27 healthy controls. In addition, 3D T1-weighted and resting-state fMRI scans were collected to characterize the structural and functional changes in cerebello-cortical loops. The results evidenced that the patients were impaired in lower-level processes of immediate perception as well as in the more complex conceptual level of mentalization. Furthermore, they presented a pattern of GM reduction in cerebellar portions that are involved in the social domain such as crus I-II, lobule IX and lobule VIIIa. These areas showed decreased functional connectivity with projection cerebral areas involved in specific aspects of social cognition. These findings boost the idea that the cerebellar modulatory function on the cortical projection areas subtends the social cognition process at different levels. Particularly, regarding the lower-level processes, the cerebellum may act by implicitly matching the external information (i.e., expression of the eyes) with the respective internal representation to guarantee an immediate judgment about the mental state of others. Otherwise, at a more complex conceptual level, the cerebellum seems to be involved in the construction of internal models of mental processes during social interactions in which the prediction of sequential events plays a role, allowing us to anticipate the other person's behavior.

Structural brain morphometry associated with theory of mind in bipolar disorder and schizophrenia

“…While unexpected, these results are consistent with previous studies indicating that the fusiform gyrus processes dynamic and static (including identity, gender) aspects of faces (Kawasaki et al, ), whereas the cerebellar lobule VI is crucial for processing social information (Guell, Gabrieli, & Schmahmann, ; Van Overwalle, Baetens, Marien, & Vandekerckhove, ). This is also consistent with previous associations reported between cerebellar atrophy and social cognitive deficits (Clausi et al, ; Van Overwalle et al, ). Therefore the morphological integrity of these regions appears to be of particular importance for efficient social cognitive skills in non‐psychiatric populations.…”

Implicit vs. Explicit Emotion Processing in Autism Spectrum Disorders: An Opinion on the Role of the Cerebellum

“…Furthermore, reduced functional connectivity (FC) between cerebellar posterior lobules, such as the right Crus-II, and cortical regions involved in complex social-emotional reasoning is present in patients with cerebellar degenerative atrophy, whose behavioral profile is characterized by mentalizing impairment and the inability to deduce emotional states (Clausi et al, 2019a).…”

“…These internal models allow us to predict incoming events and to modulate responses implicitly (Leggio and Molinari, 2015). Indeed, in the presence of cerebellar damage, the required rapid and continuous exchange of information between the internal model and the external stimuli might not be operative, thus interfering with the automatic processes (Clausi et al, 2019a).…”

“…Over the years, many scientific studies have recognized the cerebellum as being part of these brain networks (Stoodley and Schmahmann, 2010;Baumann and Mattingley, 2012;Leggio and Olivito, 2018;Clausi et al, 2019a;Van Overwalle et al, 2019a) and have evidenced its role in affective and emotional functioning (Adamaszek et al, 2015;Clausi et al, 2015Clausi et al, , 2019bLupo et al, 2015Lupo et al, , 2018. Accordingly, functional and anatomical connections have been found between the cerebellum and the cortical and subcortical structures involved in both implicit and explicit emotional processing (Critchley et al, 2000;Singer et al, 2004;Schutter et al, 2009;Stoodley and Schmahmann, 2010;Schraa-Tam et al, 2012).…”

“…Instead, regarding the explicit aspects, the cerebellum is involved in the self-perception of negative emotions and in the integration of internal state information with external environmental stimuli to consciously and adaptively elaborate emotions (Timmann et al, 2010;Clausi et al, 2017Clausi et al, , 2019a.…”