Functional Gradients of the Cerebellum: A Fundamental Movement-To-Thought Principle

Abstract

A central principle for understanding the cerebral cortex is that macroscale anatomy reflects a functional hierarchy from primary to transmodal processing. In contrast, the central axis of motor and nonmotor macroscale organization in the cerebellum remains unknown. Here we applied diffusion map embedding to resting-state data from the Human Connectome Project dataset (n=1003), and show for the first time that cerebellar functional regions follow a gradual organization which progresses from primary (motor) to transmodal (DMN, task-unfocused) regions. A secondary axis extends from taskunfocused to task-focused processing. Further, these two principal gradients reveal functional properties of the well-established cerebellar double motor representation, and its relationship with the recently described triple nonmotor representation. These interpretations are further supported by data-driven clustering and cerebello-cerebral functional connectivity analyses. Importantly, these descriptions remain observable at the individual subject level. These findings, from an exceptionally large and high-quality dataset, provide new and fundamental insights into the functional organization of the human cerebellum, unmask new testable hypotheses for future studies, and yield an unprecedented tool for the topographical, macroscale interpretation of cerebellar findings.

Functional Connectivity between the Cerebellum and Somatosensory Areas Implements the Attenuation of Self-Generated Touch

“…5-12). Lobule VI is part of the primary sensorimotor body representation in the cerebellum, whereas lobules VII/VIII constitute the second sensorimotor representation (Grodd et al, 2001;Diedrichsen et al, 2005;Stoodley and Schmahmann, 2009;O'Reilly et al, 2010;Buckner et al, 2011;Bostan et al, 2013;Guell et al, 2018;King et al, 2018). Influential animal studies have provided evidence for a direct anatomical connection between lobules IV, V, VI, and Crus I and motor cortical regions (Kelly and Strick, 2003;Lu et al, 2007;Bostan et al, 2013).…”

“…However, while the anterior part of cerebellar lobule VI, the part adjacent to the primary fissure, is considered to be involved in sensorimotor functions, both the posterior part of lobule VI and lobule Crus I are thought to be involved in cognitive processes (Diedrichsen and Bastian, 2013;Baumann et al, 2015;Sokolov et al, 2017;Guell et al, 2018;Schmahmann, 2019). Why does somatosensory attenuation recruit cerebellar areas that are not traditionally considered related to sensorimotor function?…”

Prenatal neural origins of infant motor development: Associations between fetal brain and infant motor development

“…An example is in the cerebellum where advanced motor outcomes were associated with decreased lateral cerebellar FC and increased midline anterior cerebellar FC. Prior studies in large samples of adults demonstrate that the cerebellum possesses multiple representations of the cerebral cortex (Buckner, Krienen, Castellanos, Diaz, & Yeo, 2011; Guell, Schmahmann, Gabrieli, & Ghosh, 2018). Of note, regions of the cerebellum that Buckner, Guell, and others showed to be mapped to sensorimotor cortical regions encompass the region in which we observed a positive association with future motor ability.…”

A Multi-Domain Task Battery Reveals Functional Boundaries in the Human Cerebellum

“…Task-based studies have been limited by the lack of a comprehensive neuroimaging data set. A few studies have employed data sets involving multiple tasks 7,8 , but the small number of task conditions (<7) and the lack of a common measurement baseline has made it difficult to derive and evaluate a comprehensive task-based functional parcellation. Alternatively, the functional heterogeneity of the cerebellum has been explored using meta-analytic approaches 9 , which has the disadvantage that it requires data sets to be combined across different groups of participants.…”

“…This allowed us to address a fundamental question, namely whether there are distinct functional regions in the cerebellum, or whether the functional specialization is better described in terms of continuous gradients 7 . The approach is predicated on the idea that if a boundary between two regions divides functionally heterogeneous regions, then the activation pattern for voxel pairs that lie within the same region should be more correlated than voxel pairs that span a boundary.…”