Pr Pierre Aurélien BEURIAT 

Objective: We investigated whether the cerebellum plays a critical or supportive role in in executive and emotion processes in adults. Many investigators now espouse the hypothesis that participants with cerebellar lesions experience executive functions and emotions (EE) disorders. But we hypothesized that these disorders would be milder if the damage is relatively limited to the cerebellum compared to damage involving the cerebellum plus additional cortical areas. Methods: We studied veterans with penetrating Traumatic Brain Injury (pTBI) participating in the Vietnam Head Injury Study (VHIS). We selected veterans with a cerebellar lesion (n = 24), a prefrontal cortex lesion (n = 20), along with healthy controls (HC) (n = 55). Tests of executive functions and emotions were analyzed as well as caregiver burden. We performed between-group null hypothesis significance testing, Bayesian hypothesis tests and correlational analyses. Results: Performance of participants with cerebellar lesions which extended to the cerebral cortex was similar to the HC on the Executive Function tests but they were significantly impaired on the Working Memory Index. No differences were found on the emotional processing tasks with one exception-the Facial Expression of Emotion-Test (FEEST). We then examined a sub-group of participants with large cerebellar lesions (>15%) but minimal lesions in the cerebral cortex (<15%). This sub-group of participants performed similarly to the HC on the Working Memory Index and on the FEEST. Conclusions: We suggest that the cerebellar cortex may not be critical for executive functions or processing emotional stimuli in adults as suggested. Instead, we find that the cerebellum has a supportive role characterized by its computing of the motor requirements when EE processing is required.

The cerebellum’s anatomical and functional organization and network interactions between the cerebellum and the cerebral cortex and subcortical structures are dynamic across the lifespan. Executive, emotional and social (EES) functions have likewise evolved during human development from contributing to primitive behaviors during infancy and childhood to being able to modulate complex actions in adults. In this review, we address how the importance of the cerebellum in the processing of EES functions might change across development. This evolution is driven by the macroscopic and microscopic modifications of the cerebellum that are occurring during development including its increasing connectivity with distant supra-tentorial cortical and sub-cortical regions. As a result of anatomical and functional changes, neuroimaging and clinical data indicate that the importance of the role of the cerebellum in human EES-related networks shifts from being crucial in newborns and young children to being only supportive later in life. In early life, given the immaturity of cortically mediated EES functions, EES functions and motor control and perception are more closely interrelated. At that time, the cerebellum due to its important role in motor control and sequencing makes EES functions more reliant on these computational properties that compute spatial distance, motor intent, and assist in the execution of sequences of behavior related to their developing EES expression. As the cortical brain matures, EES functions and decisions become less dependent upon these aspects of motor behavior and more dependent upon high-order cognitive and social conceptual processes. At that time, the cerebellum assumes a supportive role in these EES-related behaviors by computing their motor and sequential features. We suspect that this evolving role of the cerebellum has complicated the interpretation of its contribution to EES computational demands.

Early studies on long-term functional recovery after motor and premotor lesions showed better outcomes in younger monkeys than in older monkeys. This finding led to the widespread belief that brain injuries cause less impairment in children than adults. However, this view has limitations and a large body of evidence now indicates that cerebral damages can be more harmful when inflicted at young age, during critical periods of neural development. To date, this issue has been mainly investigated in the context of focal and diffuse cortical lesions. Much less is known about the potential influence of early cerebellar damages. Several studies exist in survivor of posterior fossa tumours. However, in these studies, critical confounders were not always considered and contradictory conclusions were provided. We studied the impact or early cerebellar damage on long-term functional recovery in three groups of 15 posterior fossa survivors, comparable with respect to their tumour characteristics (type, size and location) but operated at different ages: young (≤7 years), middle (>7 and ≤13 years) and older (>13 years). Daily (health-related quality of life scale, performance status scale), motor (International Cooperative Ataxia Rating Scale, Pegboard Purdue Test) and cognitive (full-scale intelligence quotient) functioning were assessed. A general linear model controlling for age at surgery, radiotherapy, preservation of deep cerebellar nuclei, tumour volume and delay between surgery and assessment was used to investigate significant variations in outcome measures. Early age at surgery, lesion of deep cerebellar nuclei and postoperative radiotherapy had a significant, independent negative influence on long-term recovery. Tumour volume and delay between surgery and assessment had no statistically detectable impact. The negative influence of early age at surgery was significant in all domains: daily functioning (health-related quality of life scale, performance status scale), motor functioning (International Cooperative Ataxia Rating Scale, Pegboard Purdue Test) and cognitive functioning (full-scale intelligence quotient). These results support the existence of an early critical period of development during which the cerebellar ‘learning machine’ is of critical importance. Although the extent to which the early deficits here observed can be reversed needs now to be established, our data plead for the implementation of prompt and intense rehabilitation interventions in children operated before 7 years of age.