Consensus paper: the role of the cerebellum in perceptual processes

Abstract

Various lines of evidence accumulated over the past 30 years indicate that the cerebellum, long recognized as essential for motor control, also has considerable influence on perceptual processes. In this paper, we bring together experts from psychology and neuroscience, with the aim of providing a succinct but comprehensive overview of key findings related to the involvement of the cerebellum in sensory perception. The contributions cover such topics as anatomical and functional connectivity, evolutionary and comparative perspectives, visual and auditory processing, biological motion perception, nociception, self-motion, timing, predictive processing, and perceptual sequencing. While no single explanation has yet emerged concerning the role of the cerebellum in perceptual processes, this consensus paper summarizes the impressive empirical evidence on this problem and highlights diversities as well as commonalities between existing hypotheses. In addition to work with healthy individuals and patients with cerebellar disorders, it is also apparent that several neurological conditions in which perceptual disturbances occur, including autism and schizophrenia, are associated with cerebellar pathology. A better understanding of the involvement of the cerebellum in perceptual processes will thus likely be important for identifying and treating perceptual deficits that may at present go unnoticed and untreated. This paper provides a useful framework for further debate and empirical investigations into the influence of the cerebellum on sensory perception.

Fig. 1

Composite color-coded summary diagram illustrating the distribution within the basis pontis of rhesus monkey of projections derived from association and paralimbic cortices in the prefrontal (purple), posterior parietal (blue), superior temporal (red), parastriate, and parahippocampal regions (orange), and from motor, premotor and supplementary motor areas (green). a Medial, lateral, and orbital views of the cerebral hemisphere from which the projections are derived. b Plane of section through the pons from which the rostrocaudal levels of the pons I through IX are taken. c Patterns of termination within the nuclei of the basis pontis. Other cerebral areas known to project to the pons are depicted in white. Cortical areas with no pontine projections are shown in yellow (from anterograde and retrograde studies) or gray (from retrograde studies). Dashed lines in the hemisphere diagrams represent sulcal cortices. Dashed lines in the pons diagrams represent pontine nuclei; solid lines depict corticofugal fibers (from [1] and [13])

Fig. 2

a Diagram of the lateral view of a cebus monkey brain (top) to show the location of injections of McIntyre-B strain of herpes simplex virus I in the primary motor cortex arm representation (M1arm), ventral premotor cortex arm representation (PMVarm), and in the prefrontal cortex in areas 9 and 46. The resulting retrogradely labeled neurons (below) in the cerebellar interpositus nucleus (IP) and dentate nucleus (DN) are indicated by solid dots and show the dorsal–ventral dichotomy in dentate projections to motor versus prefrontal cortices. Adapted from [29]. b Representation on flattened views of the cerebellum of the input–output organization of cerebellar loops with motor cortex M1 (left) and area 46 (right) revealed using anterograde and retrograde strains of rabies virus as tract tracer. M1 is interconnected with lobules IV to VI; prefrontal cortical area 46 is linked predominantly with crus II. Adapted from [28]

Fig. 3

MR brain slices showing distinct set of cerebellar regions that were differentially activated for: a visual stimuli and b auditory stimuli, as well as c showing a negative linear relationship between fMRI signal and motion signal strength (red shading represents activity for the visual motion condition; green shading represents activity for the auditory motion condition; yellow shading indicates activation overlap between the visual and auditory conditions). Figure reproduced with permission from [89]

Fig. 4

Loop between the cerebellum and superior temporal sulcus (STS) subserving biological motion perception. a Example of a point-light biological locomotion stimulus with 11 dots placed on the main joints of the walking human body. Outline added for illustrative purpose. From [246] Pion Ltd., London, www.envplan.com. b Dynamic causal modeling shows reciprocal effective communication between the right posterior STS and the left lateral cerebellar lobule crus I during visual processing of biological motion (BM) that modulates the back connection from the cerebellum to the STS. Adapted from [92], Copyright © 2011 Elsevier Inc., with permission of the publisher, Elsevier. c Three-dimensional representation of the structural loop pathway between the right STS and crus I, as revealed by diffusion tensor imaging (DTI). Fibers descending from the STS to the cerebellum pass through the pons and the middle cerebellar peduncle (MCP), while ascending fibers pass through the superior cerebellar peduncle (SCP) and the thalamus. From [37], copyright © The Author 2012. Published by Oxford University Press

Fig. 5

The cerebellum integrates sensory input (green boxes) from multiple systems including: (1) the vestibular, (2) visual, (3) proprioceptive and somatosensory, as well as from (4) motor efference copy signals. Cerebellar output neurons send ascending projections to the thalamus, hippocampus, and superior colliculus, which in turn connect the cerebellum to numerous cortical regions (red boxes) that mediate spatial navigation and voluntary motor control

Fig. 6

Cerebellum and sensory timing. a Adaptive timing of conditioned eye blink response is abolished following infusion of picrotoxin, an agent that disrupts input from cerebellar cortex to deep cerebellar nuclei. Courtesy of Michael Mauk. b Patients with focal cerebellar lesions fail to show attenuated ERP response to self-generated sounds compared with externally produced sounds. Adapted from [156]. c Patients with cerebellar degeneration (SCA6) exhibit selective deficit on time perception tasks that require interval timing (Var, Fix) while spared performance on tasks that require beat-based timing (Reg, Iso, Met). Adapted from [165]. d Cerebellar grey matter volume is correlated with perceptual acuity on time discrimination task, relative to a color discrimination task. Adapted from [173]

Fig. 7

Sequence detection model of prediction. If sensory events appear in a fixed sequence repeatedly in a short time, the sensory sequence is implicitly memorized a which allows cerebellar circuits to compute a prediction for forthcoming perceptual events b. If the prediction holds c, a signal is sent to the cerebral cortex to alert selective brain areas, which become activated prior to the realized event and are thus better suited to process the incoming stimulus. If the prediction fails d, an alert signal is sent, and brain activation is more widespread, accelerating the processing of salient sensory information by the changing events and attuning the behavioral response to the new environment