Subjective rating of emotionally salient stimuli modulates neural activity

Studies using emotionally salient stimuli have demonstrated neural activation in limbic and paralimbic brain regions. In some studies, subjects passively perceive evocative stimuli, while in other studies, they perform specific cognitive tasks. Evidence is emerging that even a simple cognitive task performed on emotionally salient stimuli can affect neural activation in emotion-associated brain regions. We tested the hypothesis that rating the subjective experience of an aversive visual stimulus would decrease limbic/paralimbic activation and increase activity in medial frontal regions. Ten healthy subjects underwent (15)O PET scans while they viewed pictures of aversive (AV) and nonaversive (NA) content, taken from the International Affective Picture System. Subjects appraised pictures on a scale of pleasantness/unpleasantness during one set of scans (RTNG), and they passively viewed pictures during another set (PSVW). After each scan, emotional responses were assessed. RTNG was associated with significantly less intensity of sadness and significantly less activation (AV - NA) of the right insula/amygdala and left insula, relative to PSVW. RTNG also activated the dorsal medial prefrontal cortex and the anterior cingulate sulcus, which were not differentially activated during PSVW. For both RTNG and PSVW, subjects activated the left fusiform gyrus. The results support the proposition that task instructions about how subjects should process evocative stimuli can affect neural activity.

[1]  S. Kosslyn,et al.  Neural effects of visualizing and perceiving aversive stimuli: a PET investigation. , 1996, Neuroreport.

[2]  M. Lowe,et al.  Human amygdala activation detected with echo-planar functional magnetic resonance imaging. , 1996, Neuroreport.

[3]  S. G. Cox,et al.  Functional MRI study of the cognitive generation of affect. , 1999, The American journal of psychiatry.

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

[5]  J. Pennebaker Putting stress into words: health, linguistic, and therapeutic implications. , 1993, Behaviour research and therapy.

[6]  H. Critchley,et al.  Explicit and implicit neural mechanisms for processing of social information from facial expressions: A functional magnetic resonance imaging study , 2000, Human brain mapping.

[7]  Alan C. Evans,et al.  A Three-Dimensional Statistical Analysis for CBF Activation Studies in Human Brain , 1992, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

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

[9]  M. Raichle,et al.  The Emotional Modulation of Cognitive Processing: An fMRI Study , 2000, Journal of Cognitive Neuroscience.

[10]  Michael Davis,et al.  Normal conditioned inhibition and extinction of freezing and fear-potentiated startle following electrolytic lesions of medial prefrontal cortex in rats , 1997 .

[11]  Michael Davis,et al.  Cortical Afferents to the Extended Amygdala , 1999, Annals of the New York Academy of Sciences.

[12]  G. Shulman,et al.  Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function , 2001, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[15]  S. Paradiso,et al.  Cerebral blood flow changes associated with attribution of emotional valence to pleasant, unpleasant, and neutral visual stimuli in a PET study of normal subjects. , 1999, The American journal of psychiatry.

[16]  J. Voogd,et al.  The human central nervous system , 1978 .

[17]  L. Berkowitz,et al.  Feelings, direction of attention, and expressed evaluations of others , 1990 .

[18]  R. Lazarus,et al.  The principle of short-circuiting of threat: further evidence. , 1965, Journal of personality.

[19]  Richard S. J. Frackowiak,et al.  Two Modulatory Effects of Attention That Mediate Object Categorization in Human Cortex , 1997, Science.

[20]  Joseph E. LeDoux,et al.  Emotion and the amygdala. , 1992 .

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

[22]  A. Damasio,et al.  Individuals with sociopathic behavior caused by frontal damage fail to respond autonomically to social stimuli , 1990, Behavioural Brain Research.

[23]  L. Brothers,et al.  Response of neurons in the macaque amygdala to complex social stimuli , 1990, Behavioural Brain Research.

[24]  S. Taylor,et al.  The effect of graded aversive stimuli on limbic and visual activation , 2000, Neuropsychologia.

[25]  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.

[26]  I. Marks Behavioral psychotherapy for anxiety disorders. , 1985, The Psychiatric clinics of North America.

[27]  G. Fink,et al.  Cerebral Representation of One’s Own Past: Neural Networks Involved in Autobiographical Memory , 1996, The Journal of Neuroscience.

[28]  S. Rauch,et al.  Response and Habituation of the Human Amygdala during Visual Processing of Facial Expression , 1996, Neuron.

[29]  P. Fox,et al.  Differential limbic–cortical correlates of sadness and anxiety in healthy subjects: implications for affective disorders , 2000, Biological Psychiatry.

[30]  J R Augustine,et al.  The insular lobe in primates including humans. , 1985, Neurological research.

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

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

[33]  Joseph E. LeDoux,et al.  Extinction of emotional learning: Contribution of medial prefrontal cortex , 1993, Neuroscience Letters.

[34]  Joseph E LeDoux,et al.  Differential contribution of dorsal and ventral medial prefrontal cortex to the acquisition and extinction of conditioned fear in rats. , 1995, Behavioral neuroscience.

[35]  S. Taylor,et al.  The Effect of Emotional Content on Visual Recognition Memory: A PET Activation Study , 1998, NeuroImage.

[36]  A. C. Dandoy,et al.  The use of cognitive appraisal to reduce stress reactions: A replication. , 1990 .

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

[38]  D. Amaral,et al.  Amygdalo‐cortical projections in the monkey (Macaca fascicularis) , 1984, The Journal of comparative neurology.

[39]  M. Mesulam Principles of Behavioral and Cognitive Neurology , 2000 .

[40]  R. Koeppe,et al.  Anatomic standardization: linear scaling and nonlinear warping of functional brain images. , 1994, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[41]  J. Gross Emotion Regulation: Past, Present, Future , 1999 .

[42]  M. Bradley,et al.  Emotional arousal and activation of the visual cortex: an fMRI analysis. , 1998, Psychophysiology.

[43]  Simon R. Cherry,et al.  Improved signal-to-noise in activation studies by exploiting the kinetics of oxygen-15 labeled water , 1993 .

[44]  J. Schwerdtner,et al.  fMRI an der Forensischen Klinik am Bezirksklinikum Regensburg - Neuroanatomische Grundlagen der Emotionsverarbeitung , 2004 .

[45]  S. Rauch,et al.  Masked Presentations of Emotional Facial Expressions Modulate Amygdala Activity without Explicit Knowledge , 1998, The Journal of Neuroscience.

[46]  J. Schmahmann,et al.  The cerebellar cognitive affective syndrome. , 1998, Brain : a journal of neurology.

[47]  Karl J. Friston,et al.  Neural responses to salient visual stimuli , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[48]  J. R. Augustine Circuitry and functional aspects of the insular lobe in primates including humans , 1996, Brain Research Reviews.

[49]  R. Davidson,et al.  Dysfunction in the neural circuitry of emotion regulation--a possible prelude to violence. , 2000, Science.

[50]  D. Stuss,et al.  The Frontal Lobes , 1986 .

[51]  J. Desmond,et al.  Hemispheric asymmetry for emotional stimuli detected with fMRI , 1998, Neuroreport.

[52]  D. Weinberger,et al.  Persistent elevations in dopamine and its metabolites in the nucleus accumbens after mild subchronic stress in rats with ibotenic acid lesions of the medial prefrontal cortex , 1990, Brain Research.

[53]  E. Stern,et al.  Linguistic threat activates the human amygdala. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

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

[55]  B. Vogt,et al.  Contributions of anterior cingulate cortex to behaviour. , 1995, Brain : a journal of neurology.

[56]  M. Mesulam,et al.  Insula of the old world monkey. Architectonics in the insulo‐orbito‐temporal component of the paralimbic brain , 1982, The Journal of comparative neurology.

[57]  D. Watson,et al.  Development and validation of brief measures of positive and negative affect: the PANAS scales. , 1988, Journal of personality and social psychology.

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

[59]  John P. Aggleton,et al.  The amygdala: Neurobiological aspects of emotion, memory, and mental dysfunction. , 1992 .

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