Enter feelings: somatosensory responses following early stages of visual induction of emotion.

In a MEG experiment, we imaged the early dynamics of the human cerebral cortex during the induction of emotion by visual stimuli. We tested the hypothesis that early cortical responses would correlate with the emotional competence of visual stimuli and subsequent subjective ratings of feeling in a set of specific target regions important for somatosensory, attentional, and motivational functions, just after initial visual and appraisal related cortical responses to picture presentation. Relative to the neutral condition, cortical responses, during the 350-500 ms phase of the MEG evoked response, were stronger for both pleasant and unpleasant stimuli in the orbitofrontal cortex, ventromedial prefrontal cortex, anterior cingulate and somatosensory cortices. These responses, which correlated with subjective ratings of arousal, emerged after an initial spreading of cortical activity from early visual cortex (70-200 ms) to the ventral visual stream, temporopolar and orbitofrontal regions (200-350 ms), higher for emotionally competent stimuli than for neutral in the 200-350 ms window, in a manner compatible with an appraisal function. Heart beats occurring during the first 500 ms post stimulus showed longer intervals for unpleasant than for neutral stimuli relative to the preceding beat. The results support the hypothesis of a sequence of processing regarding the emergence of feelings and suggest that, even in the early phase of feeling induction, actual body responses to the inducing stimuli could be represented in the brain.

[1]  M. Bradley,et al.  Brain potentials in affective picture processing: covariation with autonomic arousal and affective report , 2000, Biological Psychology.

[2]  R. Leahy,et al.  Mapping human brain function with MEG and EEG: methods and validation , 2004, NeuroImage.

[3]  K. Luan Phan,et al.  Functional Neuroimaging Studies of Human Emotions , 2004, CNS Spectrums.

[4]  Joseph E LeDoux Fear and the brain: where have we been, and where are we going? , 1998, Biological Psychiatry.

[5]  M. E. Spencer,et al.  A Study of Dipole Localization Accuracy for MEG and EEG using a Human Skull Phantom , 1998, NeuroImage.

[6]  M. Mesulam,et al.  Insula of the old world monkey. III: Efferent cortical output and comments on function , 1982, The Journal of comparative neurology.

[7]  Georg Northoff,et al.  Self-referential processing in our brain—A meta-analysis of imaging studies on the self , 2006, NeuroImage.

[8]  Elizabeth A. Phelps,et al.  The cognitive neuroscience of emotion , 2002 .

[9]  Neurosciences,et al.  Organization of Visual Areas in Macaque and Human Cerebral Cortex , 2002 .

[10]  T. Shallice,et al.  Human cingulate cortex and autonomic control: converging neuroimaging and clinical evidence. , 2003, Brain : a journal of neurology.

[11]  M. Beauregard,et al.  Neural Correlates of Conscious Self-Regulation of Emotion , 2001, The Journal of Neuroscience.

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

[13]  L. Chalupa,et al.  The visual neurosciences , 2004 .

[14]  Jürgen Dammers,et al.  Time course of regional brain activations during facial emotion recognition in humans , 2003, Neuroscience Letters.

[15]  G. Fricchione Descartes’ Error: Emotion, Reason and the Human Brain , 1995 .

[16]  Derek K. Jones,et al.  Virtual in Vivo Interactive Dissection of White Matter Fasciculi in the Human Brain , 2002, NeuroImage.

[17]  Hugo D. Critchley,et al.  Volitional Control of Autonomic Arousal: A Functional Magnetic Resonance Study , 2002, NeuroImage.

[18]  Gregory McCarthy,et al.  Emotion-attention network interactions during a visual oddball task. , 2004, Brain research. Cognitive brain research.

[19]  C. Don Looking for Spinoza: Joy, Sorrow, and the Feeling Brain , 2004 .

[20]  Ulrich Mayr,et al.  Conflict, consciousness, and control , 2004, Trends in Cognitive Sciences.

[21]  E. Rolls Précis of The brain and emotion. , 2000, The Behavioral and brain sciences.

[22]  G. Rizzolatti,et al.  Premotor cortex and the recognition of motor actions. , 1996, Brain research. Cognitive brain research.

[23]  J. Price,et al.  Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys , 1995, The Journal of comparative neurology.

[24]  G. Fink,et al.  Neural activation during selective attention to subjective emotional responses , 1997, Neuroreport.

[25]  F. Graham,et al.  Constraints on measuring heart rate and period sequentially through real and cardiac time. , 1978, Psychophysiology.

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

[27]  M. Bradley,et al.  Measuring emotion: the Self-Assessment Manikin and the Semantic Differential. , 1994, Journal of behavior therapy and experimental psychiatry.

[28]  Dietrich Lehmann,et al.  Affective judgments of faces modulate early activity (approximately 160 ms) within the fusiform gyri. , 2002, NeuroImage.

[29]  M. Bradley,et al.  Measuring emotion: Behavior, feeling, and physiology , 2000 .

[30]  J. Pernier,et al.  A systematic evaluation of the spherical model accuracy in EEG dipole localization. , 1997, Electroencephalography and clinical neurophysiology.

[31]  J. Decety,et al.  Neuroanatomical Correlates of Visually Evoked Sexual Arousal in Human Males , 1999, Archives of sexual behavior.

[32]  M. Mesulam,et al.  Insula of the old world monkey. II: Afferent cortical input and comments on the claustrum , 1982, The Journal of comparative neurology.

[33]  G. McCarthy,et al.  Dissociable prefrontal brain systems for attention and emotion , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[34]  Anders M. Dale,et al.  Improved Localization of Cortical Activity By Combining EEG and MEG with MRI Cortical Surface Reconstruction , 2002 .

[35]  A. Anderson Affective influences on the attentional dynamics supporting awareness. , 2005, Journal of experimental psychology. General.

[36]  A. Damasio Descartes’ Error. Emotion, Reason and the Human Brain. New York (Grosset/Putnam) 1994. , 1994 .

[37]  Richard M. Leahy,et al.  Electromagnetic brain mapping , 2001, IEEE Signal Process. Mag..

[38]  O. Pollatos,et al.  Neural systems connecting interoceptive awareness and feelings , 2007, Human brain mapping.

[39]  David Rudrauf,et al.  A conjecture regarding the biological mechanism of subjectivity and feeling , 2005 .

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

[41]  R. Maddock,et al.  Time course of the subjective emotional response to aversive pictures: relevance to fMRI studies , 2001, Psychiatry Research: Neuroimaging.

[42]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[43]  H. Critchley,et al.  Cerebral correlates of autonomic cardiovascular arousal: a functional neuroimaging investigation in humans , 2000, The Journal of physiology.

[44]  Matthias M. Müller,et al.  Early modulation of visual perception by emotional arousal: Evidence from steady-state visual evoked brain potentials , 2003, Cognitive, affective & behavioral neuroscience.

[45]  Christopher K. Kovach,et al.  Rapid Interactions between the Ventral Visual Stream and Emotion-Related Structures Rely on a Two-Pathway Architecture , 2008, The Journal of Neuroscience.

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

[47]  M. Bradley,et al.  Emotion and motivation I: defensive and appetitive reactions in picture processing. , 2001, Emotion.

[48]  M. Eimer,et al.  An ERP study on the time course of emotional face processing , 2002, Neuroreport.

[49]  Dietrich Lehmann,et al.  Affective Judgments of Faces Modulate Early Activity (∼160 ms) within the Fusiform Gyri , 2002, NeuroImage.

[50]  E. Rolls,et al.  The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology , 2004, Progress in Neurobiology.

[51]  U. Dimberg,et al.  Facial reactions to happy and angry facial expressions: evidence for right hemisphere dominance. , 2000, Psychophysiology.

[52]  H. Critchley,et al.  Fear Conditioning in Humans The Influence of Awareness and Autonomic Arousal on Functional Neuroanatomy , 2002, Neuron.

[53]  Evian Gordon,et al.  A Direct Brainstem–amygdala–cortical Dalarmt System for Subliminal Signals of Fear , 2004 .

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

[55]  R. Ilmoniemi,et al.  Magnetoencephalography-theory, instrumentation, and applications to noninvasive studies of the working human brain , 1993 .

[56]  Karl J. Friston,et al.  Neuroanatomical correlates of externally and internally generated human emotion. , 1997, The American journal of psychiatry.

[57]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[58]  Andreas A. Ioannides,et al.  Consistent and precise localization of brain activity in human primary visual cortex by MEG and fMRI , 2003, NeuroImage.

[59]  R. H. Myers Classical and modern regression with applications , 1986 .

[60]  A. Craig How do you feel? Interoception: the sense of the physiological condition of the body , 2002, Nature Reviews Neuroscience.

[61]  P. Lang,et al.  Accuracy of psychophysical judgments and physiological response amplitude. , 1973, Journal of experimental psychology.

[62]  E T Rolls,et al.  Representations of pleasant and painful touch in the human orbitofrontal and cingulate cortices. , 2003, Cerebral cortex.

[63]  J. Russell,et al.  Core affect, prototypical emotional episodes, and other things called emotion: dissecting the elephant. , 1999, Journal of personality and social psychology.

[64]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

[65]  A. Damasio The Feeling of What Happens: Body and Emotion in the Making of Consciousness , 1999 .

[66]  Amir Amedi,et al.  Attentional modulation of emotional stimulus processing: An fMRI study using emotional expectancy , 2006, Human brain mapping.

[67]  M. Bradley,et al.  Neuroanatomical correlates of pleasant and unpleasant emotion , 1997, Neuropsychologia.

[68]  Hanna Damasio,et al.  Single-neuron responses to emotional visual stimuli recorded in human ventral prefrontal cortex , 2001, Nature Neuroscience.

[69]  D. V. van Essen,et al.  Computerized Mappings of the Cerebral Cortex: A Multiresolution Flattening Method and a Surface-Based Coordinate System , 1996, Journal of Cognitive Neuroscience.

[70]  Daniel Tranel,et al.  The influence of autonomic arousal and semantic relatedness on memory for emotional words. , 2006, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.