Elsevier

Cortex

Volume 46, Issue 7, July–August 2010, Pages 845-857
Cortex

Special issue: Review
The human cerebellum contributes to motor, emotional and cognitive associative learning. A review

https://doi.org/10.1016/j.cortex.2009.06.009Get rights and content

Abstract

In this review results of human lesion studies are compared examining associative learning in the motor, emotional and cognitive domain. Motor and emotional learning were assessed using classical eyeblink and fear conditioning. Cerebellar patients were significantly impaired in acquisition of conditioned eyeblink and fear-related autonomic and skeletal responses. An additional finding was disordered timing of conditioned eyeblink responses. Cognitive learning was examined using stimulus-stimulus-response paradigms, with an experimental set-up closely related to classical conditioning paradigms. Cerebellar patients were impaired in the association of two visual stimuli, which could not be related to motor performance deficits.

Human lesion and functional brain imaging studies in healthy subjects are in accordance with a functional compartmentalization of the cerebellum for different forms of associative learning. The medial zone appears to contribute to fear conditioning and the intermediate zone to eyeblink conditioning. The posterolateral hemispheres (that is lateral cerebellum) appear to be of additional importance in fear conditioning in humans. Future studies need to examine the reasonable assumption that the posterolateral cerebellum contributes also to higher cognitive forms of associative learning.

Human cerebellar lesion studies provide evidence that the cerebellum is involved in motor, emotional and cognitive associative learning. Because of its simple and homogeneous micro-circuitry a common computation may underly cerebellar involvement in these different forms of associative learning. The overall task of the cerebellum may be the ability to provide correct predictions about the relationship between sensory stimuli.

Introduction

The cerebellum is known to be involved in motor coordination and learning (Thach et al., 1992, Bastian, 2006). In addition, the cerebellum appears to contribute to certain non-motor functions, including cognition, emotion and behavior (Schmahmann, 2004, Timmann and Daum, 2007, Ito, 2008). Because of its simple and homogeneous micro-circuitry the cerebellum has long been thought to perform a common computation, which serves various functions (Ito, 2006). Functional heterogeneity is explained by the input and output structure of the cerebellum. One example in support of this view is cerebellar involvement in different forms of associative learning. Human and a vast number of animal studies provide good evidence that the cerebellum is involved in classical eyeblink conditioning, a form of associative motor learning (Attwell et al., 2002, Bracha, 2004, Thompson, 2005, Gerwig et al., 2007). Furthermore, in the animal literature there is growing evidence that the cerebellum is involved in associative learning of emotional responses (Sacchetti et al., 2005). Animal data suggest that the intermediate cerebellum is involved in conditioning of specific aversive reactions (for example, eyeblink), and the medial cerebellum in conditioning of unspecific aversive reactions such as fear-related slowing of heart rate (Supple and Leaton, 1990, Bracha et al., 1999) (Fig. 1). Finally, more cognitive forms of associative learning appear to depend on the integrity of the cerebellum (Drepper et al., 1999, Timmann et al., 2002). Given that the posterolateral cerebellum is thought to contribute to cognitive function, the lateral cerebellum may play a role in higher-order associative learning. In the present paper results of human lesion studies will be compared examining associative learning in the motor, emotional and cognitive domain.

Section snippets

Motor associative learning

Cerebellar patients present with disorders in motor coordination (ataxia). Disorders in motor learning likely contribute to impaired motor capacities in daily life. The best investigated form of associative motor learning is classical eyeblink conditioning. A behaviorally neutral conditioned stimulus (CS), such as a tone, is presented and followed by an unconditioned stimulus (US), such as an air-puff that reliably elicits an unconditioned eyeblink response (UR). Repeated paired presentations

Emotional associative learning

The amygdala are the key structure in fear learning (Maren, 2005, Kim and Jung, 2006, for reviews). However, fear learning-related plastic changes take place in a more distributed network including the hippocampus and prefrontal cortex (Sacchetti et al., 2005). A current idea is that the amygdala is essential for fear conditioning to discrete cues, and the hippocampus for fear conditioning to contextual cues. The prefrontal cortex is important in extinction of fear memories. The cerebellum is

Cognitive associative learning

An increasing number of human lesion and functional brain imaging studies appear to support the hypothesis that the cerebellum contributes to a wide range of cognitive functions, including memory, language and visuospatial functions (Timmann and Daum, 2007, Baillieux et al., 2008, Ito, 2008 for recent reviews). However, there are also negative findings (Schoch et al., 2004, Richter et al., 2005, Frank et al., 2007a, Haarmeier and Thier, 2007). Overall, clinical abnormalities appear to be mild

Conclusions

Human cerebellar lesion studies provide strong evidence that the cerebellum is involved in associative learning in the motor, emotional and cognitive domain. Motor and emotional learning were assessed using classical eyeblink and fear conditioning. Classical conditioning is a method to test a type of associative learning, in which subjects learn relationships among stimuli (Dudai, 2002). More specifically, subjects learn that one stimulus (the CS) predicts the other (the US). Cognitive learning

Acknowledgements

The authors like to thank Beate Brol for help in data analysis and preparation of the figures. The study was supported by grants of the Deutsche Forschungsgemeinschaft (Ti 239/7-1; Ti 239/5-2).

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