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Cerebellar Damage Affects Contextual Priors for Action Prediction in Patients with Childhood Brain Tumor

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Abstract

Predictive coding accounts of action perception sustain that kinematics information is compared with contextual top-down predictions (i.e., priors) to understand actions in conditions of perceptual ambiguity. It has been previously shown that the cerebellum contributes to motor simulation of observed actions. Here, we tested the hypothesis that a specific contribution of the cerebellum to action perception is to provide contextual priors that guide the sampling of perceptual kinematic information. To this aim, we compared the performance of 42 patients with childhood brain tumor affecting infratentorial (ITT) or supratentorial (STT) areas with that of peers with typical development in an action prediction task. First, participants were exposed to videos depicting a child performing different reaching-to-grasp actions, which were associated with contextual cues in a probabilistic fashion. Then, they were presented with shortened versions of the same videos and asked to infer the action outcome; since kinematics was ambiguous, we expected their responses would be biased toward the previously learned contextual priors. We found that patients with brain tumor were impaired in predicting actions when compared to healthy controls. However, STT patients presented a reliable probabilistic effect, while ITT patients, who had cerebellar damage, did not rely on contextual priors in predicting actions. Furthermore, we found an association between the use of contextual priors and the ability to infer others’ mental states as assessed by a standardized test. These results suggest that the cerebellum provides contextual priors to understand others’ actions and this predictive function might underlie complex social cognition abilities.

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Data Availability

The anonymized datasets generated for this study are available on request to the corresponding author.

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Acknowledgments

We would thank all children and their parents for taking part into the study.

Funding

This study was funded by the Italian Ministry of Health (Ricerca Finalizzata 2013: NET-2013-02356160-4, to RB; Ricerca Finalizzata 2016: GR-2016-02363640 to CU; Ricerca Corrente 2020 to AF).

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Authors and Affiliations

  1. Neuropsychiatry and Neurorehabilitation Unit, Scientific Institute, IRCCS E. Medea, Bosisio Parini, Lecco, Italy

    Niccolò Butti, Claudia Corti & Cosimo Urgesi

  2. Scientific Institute, IRCCS E. Medea, Pasian di Prato, Udine, Italy

    Alessandra Finisguerra

  3. Neuro-oncological and Neuropsychological Rehabilitation Unit, Scientific Institute, IRCCS E. Medea, Bosisio Parini, Lecco, Italy

    Alessandra Bardoni & Geraldina Poggi

  4. IRCCS Mondino Foundation, Pavia, Italy

    Renato Borgatti

  5. Department of Languages and Literatures, Communication, Education and Society, Laboratory of Cognitive Neuroscience, University of Udine, Udine, Italy

    Cosimo Urgesi

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  1. Niccolò Butti
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Contributions

Niccolò Butti, Cosimo Urgesi, and Renato Borgatti conceived the study design. Alessandra Finisguerra contributed to material preparation. Niccolò Butti, Claudia Corti, and Alessandra Finisguerra collected the data. Niccolò Butti, Claudia Corti, and Cosimo Urgesi wrote and revised the first draft. All authors critically read, improved, and approved the final manuscript.

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Correspondence to Niccolò Butti.

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The study was approved by the Ethics Committee of the Scientific Institute IRCCS E. Medea (Prot. N.34/18–CE) and procedures were in accordance with the 1975 Declaration of Helsinki.

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Before starting the experiment, all participants and their parents were informed about aims and methods of the study and asked to sign informed consent.

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Butti, N., Corti, C., Finisguerra, A. et al. Cerebellar Damage Affects Contextual Priors for Action Prediction in Patients with Childhood Brain Tumor. Cerebellum 19, 799–811 (2020). https://doi.org/10.1007/s12311-020-01168-w

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