Separating subjective emotion from the perception of emotion-inducing stimuli: An fMRI study

fMRI was used to dissociate neural responses temporally associated with the subjective experience of emotion from those associated with the perception of emotion-inducing stimuli in order to better define the emotion-related functions of the amygdala, lateral orbital frontal cortex (OFC), and hippocampus. Subjects viewed aversive pictures followed by an extended post-stimulus period of sustained subjective emotion. Brain regions showing activation paralleling the period of sustained subjective emotion were distinguished from those showing activation limited to the period of aversive picture presentation. Behavioral results showed that subjective ratings of emotion remained elevated for 20 s after offset of the aversive pictures. fMRI results showed that viewing aversive pictures activated the amygdala, lateral OFC, and hippocampus. Subjective emotion (present both during and after aversive pictures) was temporally associated with activation in the right lateral OFC and left hippocampus but not the amygdala. Ratings of subjective emotion were correlated with activation in the right lateral OFC and left hippocampus. The results support direct amygdala involvement in emotion perception but suggest that amygdala activation is not temporally associated with subjective emotion that occurs after the offset of emotion-related stimuli. The results are consistent with a general role for the lateral OFC in monitoring or reflecting on internal experience and show that hippocampal activation is sustained during a period of subjective emotion, possibly related to enhanced memory encoding for the aversive pictures.

[1]  Brandall Y. Suyenobu,et al.  The neural correlates of placebo effects: a disruption account , 2004, NeuroImage.

[2]  Alan C. Evans,et al.  Changes in brain activity related to eating chocolate: from pleasure to aversion. , 2001, Brain : a journal of neurology.

[3]  S. Thompson-Schill,et al.  Modulation of Amygdalar Activity by the Conscious Regulation of Negative Emotion , 2002, Journal of Cognitive Neuroscience.

[4]  D. Lehmann,et al.  Rapid emotional face processing in the human right and left brain hemispheres: an ERP study. , 1999, Neuroreport.

[5]  K. Luan Phan,et al.  Subjective rating of emotionally salient stimuli modulates neural activity , 2003, NeuroImage.

[6]  Denis Paré,et al.  Role of the basolateral amygdala in memory consolidation , 2003, Progress in Neurobiology.

[7]  A. Young,et al.  Recognition of facial emotion in nine individuals with bilateral amygdala damage , 1999, Neuropsychologia.

[8]  J. Desmond,et al.  Making memories: brain activity that predicts how well visual experience will be remembered. , 1998, Science.

[9]  J. Price Prefrontal Cortical Networks Related to Visceral Function and Mood , 1999, Annals of the New York Academy of Sciences.

[10]  M. Mesulam,et al.  Dissociation of Neural Representation of Intensity and Affective Valuation in Human Gustation , 2003, Neuron.

[11]  Kenichi Ohki,et al.  Neural Correlates for Feeling-of-Knowing An fMRI Parametric Analysis , 2002, Neuron.

[12]  G. Glover,et al.  Dissociated neural representations of intensity and valence in human olfaction , 2003, Nature Neuroscience.

[13]  Scott T. Grafton,et al.  Amygdala activity related to enhanced memory for pleasant and aversive stimuli , 1999, Nature Neuroscience.

[14]  Edward E. Smith,et al.  Neuroimaging studies of working memory: , 2003, Cognitive, affective & behavioral neuroscience.

[15]  R. Poldrack,et al.  Recovering Meaning Left Prefrontal Cortex Guides Controlled Semantic Retrieval , 2001, Neuron.

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

[17]  Jonathan W. Schooler,et al.  Re-representing consciousness: dissociations between experience and meta-consciousness , 2002, Trends in Cognitive Sciences.

[18]  G. Dawson A summation technique for the detection of small evoked potentials. , 1954, Electroencephalography and clinical neurophysiology.

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

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

[21]  Adam K. Anderson,et al.  Expression Without Recognition: Contributions of the Human Amygdala to Emotional Communication , 2000, Psychological science.

[22]  Asaid Khateb,et al.  Decoupling of autonomic and cognitive emotional reactions after cerebellar stroke , 2003, Annals of neurology.

[23]  R. Dolan,et al.  Encoding of emotional memories depends on amygdala and hippocampus and their interactions , 2004, Nature Neuroscience.

[24]  Stephan Hamann,et al.  Cognitive and neural mechanisms of emotional memory , 2001, Trends in Cognitive Sciences.

[25]  Michael B. Miller,et al.  Separable Routes to Human Memory Formation: Dissociating Task and Material Contributions in the Prefrontal Cortex , 2004, Journal of Cognitive Neuroscience.

[26]  John D E Gabrieli,et al.  Amygdala Response to Happy Faces as a Function of Extraversion , 2002, Science.

[27]  Randy L. Buckner,et al.  Mixed blocked/event-related designs separate transient and sustained activity in fMRI , 2003, NeuroImage.

[28]  R. T. Hurlburt,et al.  Telling what we know: describing inner experience , 2001, Trends in Cognitive Sciences.

[29]  L. Nadel,et al.  Cognitive neuroscience of emotion , 2000 .

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

[31]  O Josephs,et al.  Dissociable Human Perirhinal, Hippocampal, and Parahippocampal Roles during Verbal Encoding , 2002, The Journal of Neuroscience.

[32]  Ralph Adolphs,et al.  Recognition of facial emotion in nine individuals with bilateral amygdala damage , 1999, Neuropsychologia.

[33]  R. Lane,et al.  Neural Correlates of Levels of Emotional Awareness: Evidence of an Interaction between Emotion and Attention in the Anterior Cingulate Cortex , 1998, Journal of Cognitive Neuroscience.

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

[35]  J. Mazziotta,et al.  Modulating emotional responses: effects of a neocortical network on the limbic system , 2000, Neuroreport.

[36]  C. Stark,et al.  Making Memories without Trying: Medial Temporal Lobe Activity Associated with Incidental Memory Formation during Recognition , 2003, The Journal of Neuroscience.

[37]  Guillén Fernández,et al.  Human declarative memory formation: Segregating rhinal and hippocampal contributions , 2002, Hippocampus.

[38]  M. Buonocore,et al.  Posterior cingulate cortex activation by emotional words: fMRI evidence from a valence decision task , 2003, Human brain mapping.

[39]  B. Mensour,et al.  Neural circuitry underlying voluntary suppression of sadness , 2003, Biological Psychiatry.

[40]  M. Bradley,et al.  Picture media and emotion: effects of a sustained affective context. , 1996, Psychophysiology.

[41]  Karl J. Friston,et al.  Generalisability, Random Effects & Population Inference , 1998, NeuroImage.

[42]  J. W. Rudy,et al.  The Role of the Dorsal Hippocampus in the Acquisition and Retrieval of Context Memory Representations , 2004, The Journal of Neuroscience.

[43]  M. Buonocore,et al.  Ghost artifact reduction for echo planar imaging using image phase correction , 1997, Magnetic resonance in medicine.

[44]  Ralph Adolphs Preferences for visual stimuli following amygdala damage , 2000 .

[45]  James L. McGaugh,et al.  Mechanisms of emotional arousal and lasting declarative memory , 1998, Trends in Neurosciences.

[46]  J. D. McGaugh Memory--a century of consolidation. , 2000, Science.

[47]  L. Parsons,et al.  Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. , 1999, The American journal of psychiatry.

[48]  E. Gordon,et al.  Arousal Dissociates Amygdala and Hippocampal Fear Responses: Evidence from Simultaneous fMRI and Skin Conductance Recording , 2001, NeuroImage.

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

[50]  Karl J. Friston,et al.  Combining Spatial Extent and Peak Intensity to Test for Activations in Functional Imaging , 1997, NeuroImage.

[51]  D. Amaral,et al.  Topographic organization of projections from the amygdala to the visual cortex in the macaque monkey , 2003, Neuroscience.

[52]  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.

[53]  Frank Schneider,et al.  Same or different? Neural correlates of happy and sad mood in healthy males , 2005, NeuroImage.

[54]  Mary-Frances O'Connor,et al.  Functional neuroanatomy of grief: an FMRI study. , 2003, The American journal of psychiatry.

[55]  S. Rauch,et al.  Neurobiology of emotion perception I: the neural basis of normal emotion perception , 2003, Biological Psychiatry.

[56]  David G. Amaral,et al.  The primate amygdala and the neurobiology of social behavior: implications for understanding social anxiety , 2002, Biological Psychiatry.

[57]  T A Ketter,et al.  Anterior paralimbic mediation of procaine-induced emotional and psychosensory experiences. , 1996, Archives of general psychiatry.

[58]  Jason P. Mitchell,et al.  Multiple routes to memory: Distinct medial temporal lobe processes build item and source memories , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[59]  Richard D. Lane,et al.  Neural correlates of conscious emotional experience. , 2000 .

[60]  Kevin N. Ochsner,et al.  For better or for worse: neural systems supporting the cognitive down- and up-regulation of negative emotion , 2004, NeuroImage.

[61]  R. Dolan,et al.  The interaction between mood and cognitive function studied with PET , 1997, Psychological Medicine.

[62]  Daniel Tranel,et al.  Intact recognition of emotional prosody following amygdala damage , 1999, Neuropsychologia.

[63]  E. Rolls,et al.  Changes in emotion after circumscribed surgical lesions of the orbitofrontal and cingulate cortices. , 2003, Brain : a journal of neurology.

[64]  R. Lane,et al.  Neuroanatomical correlates of happiness, sadness, and disgust. , 1997, The American journal of psychiatry.

[65]  A. Anderson,et al.  Lesions of the human amygdala impair enhanced perception of emotionally salient events , 2001, Nature.

[66]  J. D. McGaugh,et al.  Involvement of the amygdala in memory storage: interaction with other brain systems. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[67]  Eric E. Nelson,et al.  Orbitofrontal cortex tracks positive mood in mothers viewing pictures of their newborn infants , 2004, NeuroImage.

[68]  Vinod Goel,et al.  The Hippocampal System Mediates Logical Reasoning about Familiar Spatial Environments , 2004, Journal of Cognitive Neuroscience.

[69]  Marcia K. Johnson,et al.  Prefrontal activity associated with working memory and episodic long-term memory , 2003, Neuropsychologia.

[70]  E. Rolls,et al.  Activation of the human orbitofrontal cortex to a liquid food stimulus is correlated with its subjective pleasantness. , 2003, Cerebral cortex.

[71]  A. Anderson,et al.  Is the Human Amygdala Critical for the Subjective Experience of Emotion? Evidence of Intact Dispositional Affect in Patients with Amygdala Lesions , 2002, Journal of Cognitive Neuroscience.

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

[73]  S. Taylor,et al.  Limbic Activation and Psychophysiologic Responses to Aversive Visual Stimuli: Interaction with Cognitive Task , 2000, Neuropsychopharmacology.

[74]  G. Schwartz,et al.  Facial muscle activity during induced mood states: differential growth and carry-over of elated versus depressed patterns. , 1987, Psychophysiology.

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

[76]  R. Henson,et al.  Neural activity associated with episodic memory for emotional context , 2001, Neuropsychologia.

[77]  U. Habel,et al.  Subjective Ratings of Pain Correlate with Subcortical-Limbic Blood Flow: An fMRI Study , 2001, Neuropsychobiology.

[78]  Daniel L Schacter,et al.  Encoding activity in anterior medial temporal lobe supports subsequent associative recognition , 2004, NeuroImage.

[79]  D. Schacter,et al.  On the Tip of the Tongue An Event-Related fMRI Study of Semantic Retrieval Failure and Cognitive Conflict , 2001, Neuron.

[80]  Larry Cahill,et al.  Amygdala modulation of parahippocampal and frontal regions during emotionally influenced memory storage , 2003, NeuroImage.

[81]  R. Cabeza,et al.  Interaction between the Amygdala and the Medial Temporal Lobe Memory System Predicts Better Memory for Emotional Events , 2004, Neuron.

[82]  J. D Steele,et al.  Segregation of cognitive and emotional function in the prefrontal cortex: a stereotactic meta-analysis , 2004, NeuroImage.

[83]  Bibiana Scelfo,et al.  The Cerebellum: Synaptic Changes and Fear Conditioning , 2005, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[84]  Stephen Maren Neurobiology of Pavlovian fear conditioning. , 2001, Annual review of neuroscience.