Functional topography of primary emotion processing in the human cerebellum

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.

[1]  A. Fallon,et al.  A perspective on disgust. , 1987, Psychological review.

[2]  M Dieterich,et al.  Cerebellar activation during optokinetic stimulation and saccades , 2000, Neurology.

[3]  J. Russell A circumplex model of affect. , 1980 .

[4]  R. Snider,et al.  Cerebellar contributions to the papez circuit , 1976, Journal of neuroscience research.

[5]  A. Bastian Moving, sensing and learning with cerebellar damage , 2011, Current Opinion in Neurobiology.

[6]  J. Schmahmann From movement to thought: Anatomic substrates of the cerebellar contribution to cognitive processing , 1996, Human brain mapping.

[7]  H. Johansen-Berg,et al.  Distinct and overlapping functional zones in the cerebellum defined by resting state functional connectivity. , 2010, Cerebral cortex.

[8]  F. Hesse,et al.  Experimental inductions of emotional states and their effectiveness: A review , 1994 .

[9]  J. Panksepp Affective consciousness: Core emotional feelings in animals and humans , 2005, Consciousness and Cognition.

[10]  N. Shimizu [Neurology of eye movements]. , 2000, Rinsho shinkeigaku = Clinical neurology.

[11]  J. Gross,et al.  Emotion elicitation using films , 1995 .

[12]  K. Luan Phan,et al.  Valence, gender, and lateralization of functional brain anatomy in emotion: a meta-analysis of findings from neuroimaging , 2003, NeuroImage.

[13]  Jeremy D. Schmahmann,et al.  The Role of the Cerebellum in Cognition and Emotion: Personal Reflections Since 1982 on the Dysmetria of Thought Hypothesis, and Its Historical Evolution from Theory to Therapy , 2010, Neuropsychology Review.

[14]  G. Rizzolatti,et al.  Both of Us Disgusted in My Insula The Common Neural Basis of Seeing and Feeling Disgust , 2003, Neuron.

[15]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[16]  Marisa O. Hollinshead,et al.  The organization of the human cerebral cortex estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

[17]  J. Schmahmann,et al.  Disorders of the cerebellum: ataxia, dysmetria of thought, and the cerebellar cognitive affective syndrome. , 2004, The Journal of neuropsychiatry and clinical neurosciences.

[18]  B. Anand,et al.  Cerebellar projections to limbic system. , 1959, Journal of neurophysiology.

[19]  P. Ekman Emotion in the human face , 1982 .

[20]  J. Schmahmann,et al.  The neuropsychiatry of the cerebellum — insights from the clinic , 2008, The Cerebellum.

[21]  L. F. Barrett,et al.  Handbook of Emotions , 1993 .

[22]  G. Glover,et al.  Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control , 2007, The Journal of Neuroscience.

[23]  A M Dale,et al.  Optimal experimental design for event‐related fMRI , 1999, Human brain mapping.

[24]  A. Lawrence,et al.  Functional neuroanatomy of emotions: A meta-analysis , 2003, Cognitive, affective & behavioral neuroscience.

[25]  J. Gross The Emerging Field of Emotion Regulation: An Integrative Review , 1998 .

[26]  P. McGuire,et al.  Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. , 2009, Journal of psychiatry & neuroscience : JPN.

[27]  J. Schmahmann The role of the cerebellum in affect and psychosis , 2000, Journal of Neurolinguistics.

[28]  Christopher L. Asplund,et al.  The organization of the human cerebellum estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

[29]  P. Lang International Affective Picture System (IAPS) : Technical Manual and Affective Ratings , 1995 .

[30]  J. Schmahmann The cerebrocerebellar system: anatomic substrates of the cerebellar contribution to cognition and emotion , 2001 .

[31]  H. Barbas Connections underlying the synthesis of cognition, memory, and emotion in primate prefrontal cortices , 2000, Brain Research Bulletin.

[32]  J. Gabrieli,et al.  Rethinking Feelings: An fMRI Study of the Cognitive Regulation of Emotion , 2002, Journal of Cognitive Neuroscience.

[33]  Jeremy D. Schmahmann,et al.  Functional topography in the human cerebellum: A meta-analysis of neuroimaging studies , 2009, NeuroImage.

[34]  K. Phan,et al.  Neural substrates for voluntary suppression of negative affect: A functional magnetic resonance imaging study , 2005, Biological Psychiatry.

[35]  R. Adolphs Neural systems for recognizing emotion , 2002, Current Opinion in Neurobiology.

[36]  John D E Gabrieli,et al.  Sex differences in the neural basis of emotional memories , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Jörn Diedrichsen,et al.  A spatially unbiased atlas template of the human cerebellum , 2006, NeuroImage.

[38]  J. Schmahmann,et al.  Aversion-Related Circuitry in the Cerebellum: Responses to Noxious Heat and Unpleasant Images , 2011, The Journal of Neuroscience.

[39]  Jörn Diedrichsen,et al.  A probabilistic MR atlas of the human cerebellum , 2009, NeuroImage.

[40]  A. Damasio,et al.  Subcortical and cortical brain activity during the feeling of self-generated emotions , 2000, Nature Neuroscience.

[41]  P. Ekman An argument for basic emotions , 1992 .

[42]  R. Davidson,et al.  The functional neuroanatomy of emotion and affective style , 1999, Trends in Cognitive Sciences.

[43]  Turhan Canli,et al.  Individual differences in emotion processing , 2004, Current Opinion in Neurobiology.

[44]  Dennis J. L. G. Schutter,et al.  The cerebellum on the rise in human emotion , 2008, The Cerebellum.

[45]  Jaak Panksepp,et al.  The affective brain and core consciousness: How does neural activity generate emotional feelings? , 2008 .

[46]  M. Washburn,et al.  Bodily Changes in Pain, Hunger, Fear, and Rage. , 1917 .

[47]  Deborah A Yurgelun-Todd,et al.  Activation of the amygdala and anterior cingulate during nonconscious processing of sad versus happy faces , 2004, NeuroImage.

[48]  P. Johnson-Laird,et al.  The language of emotions: An analysis of a semantic field , 2013 .

[49]  Jörn Diedrichsen,et al.  Imaging the deep cerebellar nuclei: A probabilistic atlas and normalization procedure , 2011, NeuroImage.

[50]  Alan C. Evans,et al.  MRI Atlas of the Human Cerebellum , 2000 .

[51]  J. Panksepp Affective Neuroscience: The Foundations of Human and Animal Emotions , 1998 .

[52]  N Ramnani,et al.  A probabilistic MR atlas of the human cerebellum , 2009, NeuroImage.

[53]  Jeff T. Larsen,et al.  Further evidence for mixed emotions. , 2011, Journal of personality and social psychology.

[54]  P. Strick,et al.  Cerebellar Projections to the Prefrontal Cortex of the Primate , 2001, The Journal of Neuroscience.

[55]  R. Plutchik Emotion, a psychoevolutionary synthesis , 1980 .

[56]  Michael D. Greicius,et al.  Distinct Cerebellar Contributions to Intrinsic Connectivity Networks , 2009, NeuroImage.

[57]  G. Holmes THE SYMPTOMS OF ACUTE CEREBELLAR INJURIES DUE TO GUNSHOT INJURIES , 1917 .

[58]  Jody Tanabe,et al.  Brain Activation during Smooth-Pursuit Eye Movements , 2002, NeuroImage.

[59]  M. Skalej,et al.  A new semiautomated, three‐dimensional technique allowing precise quantification of total and regional cerebellar volume using MRI , 1998, Magnetic resonance in medicine.

[60]  M. Bradley,et al.  Emotion and motivation II: sex differences in picture processing. , 2001, Emotion.

[61]  Jaak Panksepp,et al.  Neuroscience and Biobehavioral Reviews the Basic Emotional Circuits of Mammalian Brains: Do Animals Have Affective Lives? , 2022 .

[62]  J. Lynch,et al.  Cortico-cortical networks and cortico-subcortical loops for the higher control of eye movements. , 2006, Progress in brain research.

[63]  H B Danesh,et al.  Anger and fear. , 1977, The American journal of psychiatry.

[64]  H. Flor,et al.  Gender differences in the processing of standardized emotional visual stimuli in humans: a functional magnetic resonance imaging study , 2003, Neuroscience Letters.

[65]  Sam J. Maglio,et al.  Emotional category data on images from the international affective picture system , 2005, Behavior research methods.

[66]  J. Schmahmann An emerging concept. The cerebellar contribution to higher function. , 1991, Archives of neurology.

[67]  K. Luan Phan,et al.  Functional Neuroanatomy of Emotion: A Meta-Analysis of Emotion Activation Studies in PET and fMRI , 2002, NeuroImage.

[68]  M. Fanselow Neural organization of the defensive behavior system responsible for fear , 1994, Psychonomic bulletin & review.

[69]  R. Heath,et al.  Gross Pathology of the Cerebellum in Patients Diagnosed and Treated as Functional Psychiatric Disorders , 1979, The Journal of nervous and mental disease.

[70]  R. Koeppe,et al.  Regulation of human affective responses by anterior cingulate and limbic mu-opioid neurotransmission. , 2003, Archives of general psychiatry.