In search of specificity: functional MRI in the study of emotional experience.

The growing availability of functional magnetic resonance imaging (fMRI) with its property of high spatial resolution has energized the search for specific neural substrates of basic emotions and their feeling components. In the present article, we address the question as to whether recent fMRI studies on primary affective experiences have truly helped to pinpoint emotion-specific areas in the human brain or whether these studies are afflicted with methodological problems which make such inferences difficult. As one approach for improvement, we suggest the combination of fMRI with methods characterized by high temporal resolution, such as electroencephalography (EEG). Simultaneous recoding allows the correlation of temporally specific EEG components (e.g., the late positive potential) with regional blood-oxygen-level-dependent (BOLD) signals during affective experiences. Combined information on the source as well as the exact temporal pattern of a neural affective response will help to improve our understanding of emotion-specific brain activation.

[1]  A. Jedynak,et al.  Rapid extraction of emotional expression: evidence from evoked potential fields during brief presentation of face stimuli , 2003, Neuropsychologia.

[2]  C. F. Beckmann,et al.  Tensorial extensions of independent component analysis for multisubject FMRI analysis , 2005, NeuroImage.

[3]  J. Cacioppo,et al.  Handbook Of Psychophysiology , 2019 .

[4]  Bertram Walter,et al.  Relationship between Disgust Sensitivity, Trait Anxiety and Brain Activity during Disgust Induction , 2005, Neuropsychobiology.

[5]  S. Rauch,et al.  Brain habituation during repeated exposure to fearful and neutral faces: A functional MRI study , 2003, Brain Research Bulletin.

[6]  J. Gross,et al.  The Neural Bases of Emotion Regulation: Reappraisal and Suppression of Negative Emotion , 2008, Biological Psychiatry.

[7]  Kenneth Hugdahl,et al.  Assessing the spatiotemporal evolution of neuronal activation with single-trial event-related potentials and functional MRI. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[8]  Functional MRI: an overview , 2007, Acta Neuropsychiatrica.

[9]  M. Reuter,et al.  Personality and emotion: test of Gray's personality theory by means of an fMRI study. , 2004, Behavioral neuroscience.

[10]  I. Christie,et al.  Autonomic specificity of discrete emotion and dimensions of affective space: a multivariate approach. , 2004, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[11]  Karl J. Friston CHAPTER 41 – Dynamic Causal Models for fMRI , 2007 .

[12]  Axel Schäfer,et al.  Event-Related Brain Potentials of Spider Phobics to Disorder- Relevant, Generally Disgust- and Fear-Inducing Pictures , 2008 .

[13]  Axel Schäfer,et al.  Stimulus type and design influence hemodynamic responses towards visual disgust and fear elicitors. , 2005, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[14]  R. Oostenveld,et al.  Frontal theta EEG activity correlates negatively with the default mode network in resting state. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[15]  W. Goodman,et al.  Disgust and the insula: fMRI responses to pictures of mutilation and contamination , 2004, Neuroreport.

[16]  A. Engel,et al.  Single-trial EEG–fMRI reveals the dynamics of cognitive function , 2006, Trends in Cognitive Sciences.

[17]  Richard J. Davidson,et al.  Functional MRI in the Study of Emotion , 2000 .

[18]  T. Dalgleish,et al.  Handbook of cognition and emotion , 1999 .

[19]  A. Ax The Physiological Differentiation between Fear and Anger in Humans , 1953, Psychosomatic medicine.

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

[21]  S. Debener,et al.  Properties of the ballistocardiogram artefact as revealed by EEG recordings at 1.5, 3 and 7 T static magnetic field strength. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[22]  Karl J. Friston,et al.  Statistical parametric mapping , 2013 .

[23]  A. Young,et al.  Neural responses to facial and vocal expressions of fear and disgust , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[24]  Giorgio Bonmassar,et al.  EEG/(f)MRI measurements at 7 Tesla using a new EEG cap (“InkCap”) , 2006, NeuroImage.

[25]  Jeff T. Larsen,et al.  May I have your attention, please: Electrocortical responses to positive and negative stimuli , 2003, Neuropsychologia.

[26]  V. Calhoun,et al.  Joint independent component analysis for simultaneous EEG-fMRI: principle and simulation. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[27]  R. Stark,et al.  Hemodynamic responses to fear and disgust-inducing pictures: an fMRI study. , 2003, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[28]  Jill Keane,et al.  Disgust sensitivity predicts the insula and pallidal response to pictures of disgusting foods , 2007, The European journal of neuroscience.

[29]  E. Gordon,et al.  BOLD, sweat and fears: fMRI and skin conductance distinguish facial fear signals , 2005, Neuroreport.

[30]  R D Pascual-Marqui,et al.  Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. , 2002, Methods and findings in experimental and clinical pharmacology.

[31]  M. Roth,et al.  Single‐trial analysis of oddball event‐related potentials in simultaneous EEG‐fMRI , 2007, Human brain mapping.

[32]  S. C. Gandevia,et al.  Somatotopic organization of the processing of muscle and cutaneous pain in the left and right insula cortex: A single-trial fMRI study , 2007, Pain.

[33]  R. Schmidt,et al.  Physiologie des Menschen , 1993, Springer-Lehrbuch.

[34]  K. Phan,et al.  Neural correlates of internally-generated disgust via autobiographical recall: a functional magnetic resonance imaging investigation , 2004, Neuroscience Letters.

[35]  R. Stark,et al.  The insula is not specifically involved in disgust processing: an fMRI study , 2002, Neuroreport.

[36]  Lisa Feldman Barrett,et al.  The Structure of Emotion , 2006 .

[37]  Karl J. Friston,et al.  The functional anatomy of the MMN: A DCM study of the roving paradigm , 2008, NeuroImage.

[38]  G. Stemmler,et al.  The autonomic differentiation of emotions revisited: convergent and discriminant validation. , 1989, Psychophysiology.

[39]  N. Kalin,et al.  Emotion, plasticity, context, and regulation: perspectives from affective neuroscience. , 2000, Psychological bulletin.

[40]  S. Debener,et al.  Simultaneous recording of EEG and BOLD responses: a historical perspective. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[41]  Richard J. Davidson,et al.  Fear Is Fast in Phobic Individuals: Amygdala Activation in Response to Fear-Relevant Stimuli , 2006, Biological Psychiatry.

[42]  Andrew W. Young,et al.  Differential effects of object-based attention on evoked potentials to fearful and disgusted faces , 2008, Neuropsychologia.

[43]  David N. Kennedy,et al.  fMRI of sensitization to angry faces , 2005, NeuroImage.

[44]  Bertram Walter,et al.  Hemodynamic brain correlates of disgust and fear ratings , 2007, NeuroImage.

[45]  Dieter Vaitl,et al.  Relationship between regional hemodynamic activity and simultaneously recorded EEG‐theta associated with mental arithmetic‐induced workload , 2007, Human brain mapping.

[46]  F. Boiten,et al.  Autonomic response patterns during voluntary facial action. , 1996, Psychophysiology.

[47]  Vera Ferrari,et al.  Repetitive picture processing: Autonomic and cortical correlates , 2006, Brain Research.

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

[49]  S. Rauch,et al.  Differential prefrontal cortex and amygdala habituation to repeatedly presented emotional stimuli , 2001, Neuroreport.

[50]  Martin A. Lindquist,et al.  Handbook of Psychophysiology: Elements of Functional Neuroimaging , 2007 .

[51]  Axel Schäfer,et al.  Individual differences in disgust imagery: a functional magnetic resonance imaging study , 2008, Neuroreport.

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

[53]  E. Bullmore,et al.  A differential neural response in obsessive–compulsive disorder patients with washing compared with checking symptoms to disgust , 2000, Psychological Medicine.

[54]  Karl J. Friston,et al.  Dynamic causal modeling for EEG and MEG , 2009, Human brain mapping.

[55]  Axel Schäfer,et al.  Diminished medial prefrontal cortex activity in blood-injection-injury phobia , 2007, Biological Psychology.

[56]  Vincent Giampietro,et al.  Individual differences in disgust sensitivity modulate neural responses to aversive/disgusting stimuli , 2008, The European journal of neuroscience.

[57]  M. Bradley,et al.  Brain activation by disgust-inducing pictures in obsessive-compulsive disorder , 2003, Biological Psychiatry.

[58]  R. Stark,et al.  Evaluative Conditioning: A Possible Explanation for the Acquisition of Disgust Responses? , 2001 .

[59]  Axel Schäfer,et al.  Hemodynamic Effects of Negative Emotional Pictures – A Test-Retest Analysis , 2004, Neuropsychobiology.

[60]  M. Bradley,et al.  Emotional perception: correlation of functional MRI and event-related potentials. , 2006, Cerebral cortex.

[61]  Margot J. Taylor,et al.  Early processing of the six basic facial emotional expressions. , 2003, Brain research. Cognitive brain research.

[62]  C. Adsett,et al.  Changes in Coronary Blood Flow and Other Hemodynamic Indicators Induced by Stressful Interviews , 1962, Psychosomatic medicine.

[63]  M Esslen,et al.  Brain areas and time course of emotional processing , 2004, NeuroImage.

[64]  Jonas K. Olofsson,et al.  Affective picture processing: An integrative review of ERP findings , 2008, Biological Psychology.

[65]  Axel Schäfer,et al.  Erotic and disgust-inducing pictures—Differences in the hemodynamic responses of the brain , 2005, Biological Psychology.

[66]  P. Ekman,et al.  Autonomic nervous system activity distinguishes among emotions. , 1983, Science.

[67]  Axel Schäfer,et al.  fMRI responses to pictures of mutilation and contamination , 2006, Neuroscience Letters.

[68]  John Polich,et al.  Affective visual event-related potentials: Arousal, repetition, and time-on-task , 2007, Biological Psychology.

[69]  Axel Schäfer,et al.  Disgust Processing in Phobia of Blood-Injection-Injury: An fMRI Study , 2003 .

[70]  R. Stark,et al.  Influences of disgust sensitivity on hemodynamic responses towards a disgust-inducing film clip. , 2005, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[71]  D. Perrett,et al.  A specific neural substrate for perceiving facial expressions of disgust , 1997, Nature.

[72]  U. Eysel,et al.  Neural structures associated with recognition of facial expressions of basic emotions , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[73]  Karl J. Friston,et al.  Brain Systems Mediating Aversive Conditioning: an Event-Related fMRI Study , 1998, Neuron.