Functional Recruitment of the Cerebellum Supports the Emergence of Theory of Mind in Early Childhood

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Abstract Submission 

Aikaterina Manoli^1,2,3,4, Charlotte Grosse Wiesmann², Sofie Valk^2,3,5

¹International Max Planck Research School on Cognitive Neuroimaging, Leipzig, Germany, ²Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany, ³Institute of Neuroscience and Medicine, Brain & Behavior (INM-7), Research Centre Jülich, Jülich, Germany, ⁴Faculty of Medicine, Leipzig University, Leipzig, Germany, ⁵Institute of Systems Neuroscience, Medical Faculty, Heinrich Heine University Düsseldorf, Düsseldorf, Germany

Aikaterina Manoli  
International Max Planck Research School on Cognitive Neuroimaging|Max Planck Institute for Human Cognitive and Brain Sciences|Institute of Neuroscience and Medicine, Brain & Behavior (INM-7), Research Centre Jülich|Faculty of Medicine, Leipzig University
Leipzig, Germany|Leipzig, Germany|Jülich, Germany|Leipzig, Germany

Charlotte Grosse Wiesmann  
Max Planck Institute for Human Cognitive and Brain Sciences
Leipzig, Germany

Sofie Valk  
Max Planck Institute for Human Cognitive and Brain Sciences|Institute of Neuroscience and Medicine, Brain & Behavior (INM-7), Research Centre Jülich|Institute of Systems Neuroscience, Medical Faculty, Heinrich Heine University Düsseldorf
Leipzig, Germany|Jülich, Germany|Düsseldorf, Germany

Although traditionally associated with motor processing, accumulating evidence suggests that the cerebellum is heavily implicated in social cognition, including Theory of Mind (ToM), i.e., the ability to infer the mental states of others (Frith & Frith, 2006). However, the role of the cerebellum in ToM development remains elusive, despite clinical evidence linking early-life cerebellar injury to dramatic and long-lasting social cognitive deficits (Olson et al., 2023). Here, we investigated the contribution of the cerebellum to the emergence of ToM in young children in the context of local functional activations and functional connectivity to the cerebral cortex. We expected to observe differences in the functional involvement of the cerebellum between children who have and have not yet developed ToM abilities, as well as between childhood and adulthood.

We leveraged open functional MRI and behavioral data of typically developing children (N=41; age range: 3-12 years) and adults (N=78) who watched an in-scanner ToM movie (Kliemann et al., 2022; Richardson et al., 2018). Children's ToM abilities were measured with an out-of-scanner task requiring them to point out others' false beliefs. Prior to analyses, the cerebellum was isolated and normalized to the Spatially Unbiased Infratentorial Template (SUIT; Diedrichsen, 2006). Functional images were masked with the cerebellar isolation mask, only retaining signals originating from the cerebellum. We used contrast analyses to identify cerebellar functional clusters in response to ToM movie events in children with ToM abilities (N=22), children without ToM abilities (N=19), and adults, while controlling for general executive functions (i.e., response inhibition and intelligence). Cerebellar activation clusters were used in seed-to-voxel correlation analyses to compare cerebro-cerebellar connectivity between the three groups. Lastly, we used dynamic causal modelling (DCM) to examine the directionality of cerebro-cerebellar connections during ToM processing. We specified full bilinear deterministic DCMs between seeds in the cerebellum and the cerebral ToM network (Schurz et al., 2014), based on ToM movie activation clusters. This way, we allowed for all possible forward and backward connections to be estimated. We then constructed a group-level parametric empirical Bayes (PEB) model which allowed us to examine individual differences in connectivity (e.g., ToM abilities) by including them as covariates in our models (Friston et al., 2015).

Children with ToM abilities demonstrated activation clusters in the posterior cerebellum (Crura I-II), which were consistent with activations in adults, but absent in children without ToM abilities (Fig. 1A). Seed-to-voxel correlations revealed a functional reorganization of the cerebellum as a function of ToM abilities, shifting from non-ToM network connections with the right Crus I towards connections between the ToM network and the right Crus II as children developed ToM abilities (Fig. 1B). Lastly, DCM analyses identified forward connections from the posterior cerebellum to the ToM network in children with ToM abilities, whereas adults primarily demonstrated inverse connections from the ToM network to the posterior cerebellum (Fig. 2).

We showed functional involvement of the posterior cerebellum in early-life ToM emergence, with growing connections to the cerebral ToM network as a function of ToM abilities. Interestingly, we found inverse cerebro-cerebellar connectivity patterns in children with ToM abilities and adults, with greater dependence on connections from cerebellar Crura I-II to the cerebral ToM network early in life. This could suggest a crucial role of the posterior cerebellum in the initial construction of ToM schemas. Future research should investigate how the development of the posterior cerebellum might contribute to social cognitive deficits in neurodevelopmental disorders, such as autism.

Social Cognition ¹

Early life, Adolescence, Aging ²

Activation (eg. BOLD task-fMRI)

Connectivity (eg. functional, effective, structural)

Cerebellum

Cognition

Cortex

Development

FUNCTIONAL MRI

Modeling

Open Data

Social Interactions

Other - Functional Connectivity