Functional topography of primary emotion processing in the human cerebellum
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.).
References (67)
Neural systems for recognizing emotion
Curr. Opin. Neurobiol.
(2002)Connections underlying the synthesis of cognition, memory, and emotion in primate prefrontal cortices
Brain Res. Bull.
(2000)Moving, sensing and learning with cerebellar damage
Curr. Opin. Neurobiol.
(2011)- et al.
The functional neuroanatomy of emotion and affective style
Trends Cogn. Sci.
(1999) A spatially unbiased atlas template of the human cerebellum
NeuroImage
(2006)- et al.
A probabilistic atlas of the human cerebellum
NeuroImage
(2009) - et al.
Imaging the deep cerebellar nuclei: a probabilistic atlas and normalization procedure
NeuroImage
(2011) - et al.
Individual differences in emotion processing
Curr. Opin. Neurobiol.
(2004) - et al.
Activation of the amygdala and anterior cingulate during nonconscious processing of sad versus happy faces
NeuroImage
(2004) - et al.
Cortico-cortical networks and cortico-subcortical loops for the higher control of eye movements
Prog. Brain Res.
(2006)
Affective consciousness: core emotional feelings in animals and humans
Conscious. Cogn.
The basic emotional circuits of mammalian brains: do animals have affective lives?
Neurosci. Biobehav. Rev.
Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and FMRI
NeuroImage
Neural substrates for voluntary suppression of negative affect: a functional magnetic resonance imaging study
Biol. Psychiatry
Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies
NeuroImage
Brain activation during smooth-pursuit eye movements
NeuroImage
Valence, gender, and lateralization of functional brain anatomy in emotion: a meta-analysis of findings from neuroimaging
NeuroImage
Both of us disgusted in my insula: the common neural basis of seeing and feeling disgust
Neuron
Cerebellar projections to limbic system
J. Neurophysiol.
Emotion and motivation II: sex differences in picture processing
Emotion
The organization of the human cerebellum estimated by intrinsic functional connectivity
J. Neurophysiol.
Sex differences in the neural basis of emotional memories
Proc. Natl. Acad. Sci. U. S. A.
Bodily Changes in Pain, Hunger, Fear and Rage
Optimal experimental design for event-related fMRI
Hum. Brain Mapp.
Subcortical and cortical brain activity during the feeling of self-generated emotions
Nature
Anger and fear
Am. J. Psychiatry
Cerebellar activation during optokinetic stimulation and saccades
Neurology
Emotion in the Human Face
An argument for basic emotions
Cogn. Emot.
Neural organization of the defensive behavior system responsible for fear
Psychon. Bull. Rev.
Statistical parametric maps in functional imaging: a general linear approach
Hum. Brain Mapp.
Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies
J. Psychiatry Neurosci.
Experimental inductions of emotional states and their effectiveness: a review
Br. J. Psychol.
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