Elsevier

NeuroImage

Volume 61, Issue 4, 16 July 2012, Pages 805-811
NeuroImage

Functional topography of primary emotion processing in the human cerebellum

https://doi.org/10.1016/j.neuroimage.2012.03.044Get rights and content

Abstract

The cerebellum has an important role in the control and coordination of movement. It is now clear, however, that the cerebellum is also involved in neural processes underlying a wide variety of perceptual and cognitive functions, including the regulation of emotional responses. Contemporary neurobiological models of emotion assert that a small set of discrete emotions are mediated through distinct cortical and subcortical areas. Given the connectional specificity of neural pathways that link the cerebellum with these areas, we hypothesized that distinct sub-regions of the cerebellum might subserve the processing of different primary emotions. We used functional magnetic resonance imaging (fMRI) to identify neural activity patterns within the cerebellum in 30 healthy human volunteers as they categorized images that elicited each of the five primary emotions: happiness, anger, disgust, fear and sadness. In support of our hypothesis, all five emotions evoked spatially distinct patterns of activity in the posterior lobe of the cerebellum. We also detected overlaps between cerebellar activations for particular emotion categories, implying the existence of shared neural networks. By providing a detailed map of the functional topography of emotion processing in the cerebellum, our study provides important clues to the diverse effects of cerebellar pathology on human affective function.

Introduction

In humans the cerebellum has long been recognized as being crucial for sensorimotor control (Holmes, 1917, Schmahmann, 2004). In recent years, however, a wealth of evidence from clinical, experimental and neuroimaging studies has led to the hypothesis that the cerebellum is also critically involved in perceptual, cognitive and, perhaps most intriguingly, emotional processes (Bastian, 2011, Schmahmann, 2010, Stoodley and Schmahmann, 2009). In a longitudinal follow-up study of 20 patients with cerebellar lesions, Schmahmann and Sherman (1998) observed prominent behavioral and affective changes, ranging from apathy to pathological crying and laughing, symptoms that they identified as a “cerebellar cognitive–affective syndrome”. Further support for a cerebellar role in emotional processes comes from anatomical studies in animals which have shown that the cerebellum has connections with other brain areas known to be involved in affective regulation, mood and higher cognition, including the hypothalamus, septum, amygdala, insula, basal ganglia, as well as the neocortex and brainstem nuclei (Anand et al., 1959, Middleton and Strick, 2001, Schmahmann, 2001, Schutter and van Honk, 2005, Snider and Maiti, 1976).

Surprisingly, despite the large literature on brain imaging of human emotions, potential contributions of the cerebellum have been largely ignored, or reported only as incidental to activity within the cerebrum (Fusar-Poli et al., 2009). One recent exception is a study by Moulton et al. (2011), which investigated aversion-related responses in the cerebellum to noxious heat and unpleasant images, and identified overlapping areas in the posterior cerebellum. By contrast, the authors found a distinct region of activation in response to pleasant images within right cerebellar hemispheric lobules VI and Crus II. These findings suggest a degree of neural specialization within the cerebellum for aversive (painful) stimuli as opposed to neutral or non-aversive stimuli.

Cognitive models predominantly consider emotions as being represented by just a small number of dimensions, and commonly conceptualize the affective space as a circle or circumplex (Russel, 1980). In contrast, neurobiological models of emotion have argued for the existence of a small set of discrete emotions that are instantiated by dedicated neural systems (e.g. Ekman, 1992, Panksepp, 2005, Panksepp, 2008, Panksepp, 2011). This latter view is supported by a number of human neuroimaging studies, which have shown that different primary emotions activate, at least partially, distinct networks of cortical and subcortical structures (Murphey et al., 2003, Phan et al., 2002). Thus, for example, the amygdala is critically involved in mediating the so-called “threat-related” emotions of fear and anger (Adolphs, 2002, Davidson and Irwin, 1999), whereas the insula is involved in reactions of disgust (Wicker et al., 2003). Given the connectional specificity of the neural pathways that link the cerebellum with various cortical and subcortical structures involved in emotional processing (e.g. Anand et al., 1959), it is possible that such anatomical segregation and specialization for different emotional categories also exists within the cerebellum.

Here we employed functional magnetic resonance imaging (fMRI) to determine whether the human cerebellum is functionally segregated into distinct regions for processing the five primary emotions of anger, fear, disgust, sadness and happiness (Ekman, 1992, Johnson-Laird and Oatley, 1989).

Section snippets

Participants

Thirty healthy participants gave informed consent to the behavioral and brain imaging procedures, as approved by The University of Queensland Human Research Ethics Committee. The participants' ages ranged from 18 to 30 years (mean age = 22.2, SD = 2.9 years). Fifteen of the participants were female; all were right-handed.

Elicitation of emotions

Emotions were evoked by presenting participants with images from the International Affective Picture System (IAPS; Lang et al., 1999), a standardized set of color photographs that

Behavioral data

Fig. 2 shows the average relative frequencies of emotions elicited by the set of IAPS images. With the exception of anger, all emotions were well represented. We found that five of the female participants and two of the male participants rarely reported the experience of anger (< 10 trials each), which explains the relatively low average frequency for this emotion (6.57%). This outcome is consistent with previous studies in which difficulties were noted in eliciting anger under artificial

Discussion

In recent years, clinical and neuroimaging studies have provided compelling evidence for a cerebellar role in the processing of emotion (Stoodley and Schmahmann, 2009). In the present study we tested the hypothesis that different primary emotions are associated with distinct patterns of cerebellar activity. While earlier work had already revealed different cortical and subcortical networks for distinct emotions (Murphey et al., 2003, Phan et al., 2002), it was not clear whether the same

Conclusions

We have provided the first evidence in healthy humans that distinct subregions of the cerebellum are responsive during the experience of happiness, anger, disgust, fear and sadness. Our findings also reveal overlaps between the activation patterns for selected emotions, indicating the existence of shared neural networks. For instance, we detected partial overlap in activations associated with fear and anger (paravermal lobules VI and Crus I), anger and disgust (vermal lobule IX), and happiness

Acknowledgments

This work was supported by an Australian Research Council Discovery Early Career Researcher Award (DE120100535; O.B.), a University of Queensland Early Career Researcher Grant (O.B.), and an Australian Research Council ‘Thinking Systems’ Grant (TS0669699; J.B.M.).

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