Levels of appraisal: A medial prefrontal role in high-level appraisal of emotional material

Appraisal refers to the evaluation of the meaning of emotional stimuli and is considered causal in the generation of an emotional response. Cognitive neuroscience has paid little attention to a theoretical distinction between low-level appraisal, considered to be automatic and preattentive, and high-level appraisal that requires attentional and working memory resources. To disentangle low-level from high-level appraisal, we varied cognitive load in a concurrent, unrelated working memory task, while anxiety was induced through anticipation of impending pain. Confirming theoretical predictions, we show that anxiety-related activity in dorsal medial prefrontal/rostral anterior cingulate cortex (dorsal MPFC/ACC) is attenuated under high, relative to low, cognitive load. Lateral prefrontal regions previously implicated in reappraisal and cognitive emotion regulation show a similar interaction between anxiety and cognitive load. Critically, there were no changes in physiological and subjective measures of low-level appraisal outcome and emotional response generation as a function of load, allowing us to conclude that MPFC/ACC and lateral PFC activity during anticipatory anxiety reflects high-level appraisal. Our data provide neurobiological evidence for a distinction between low-level and high-level appraisal mechanisms.

[1]  David Sander,et al.  A systems approach to appraisal mechanisms in emotion , 2005, Neural Networks.

[2]  Richard S. Lazarus,et al.  Anticipatory stress and coping reactions under various conditions of uncertainty. , 1972, Journal of personality and social psychology.

[3]  M. Erdelyi,et al.  Cognitive masking: The disruptive effect of an emotional stimulus upon the perception of contiguous neutral items* , 1973 .

[4]  R. Lazarus,et al.  Autonomic discrimination without awareness: A study of subception. , 1951, Psychological review.

[5]  Peter Dayan,et al.  Temporal difference models describe higher-order learning in humans , 2004, Nature.

[6]  R. Zajonc,et al.  Affective discrimination of stimuli that cannot be recognized. , 1980, Science.

[7]  K. Scherer Appraisal considered as a process of multilevel sequential checking. , 2001 .

[8]  Sterling C. Johnson,et al.  Neural correlates of self-reflection. , 2002, Brain : a journal of neurology.

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

[10]  M. Preul The Human Brain: Surface, Blood Supply, and Three-Dimensional Sectional Anatomy , 2001 .

[11]  M. Raichle,et al.  Emotion-induced changes in human medial prefrontal cortex: I. During cognitive task performance. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[12]  大平 典明 State Trait Anxiety Inventory(From Y)の日本語版作成の試み , 1987 .

[13]  P Vuilleumier,et al.  Neural response to emotional faces with and without awareness: event-related fMRI in a parietal patient with visual extinction and spatial neglect , 2002, Neuropsychologia.

[14]  M. Kozak,et al.  Emotional processing of fear: exposure to corrective information. , 1986, Psychological bulletin.

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

[16]  R. Lazarus Psychological stress and the coping process , 1970 .

[17]  M. Raichle,et al.  Emotion-induced changes in human medial prefrontal cortex: II. During anticipatory anxiety. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[18]  Matthew L. Ho,et al.  Brain metabolic changes associated with symptom factor improvement in major depressive disorder , 2001, Biological Psychiatry.

[19]  Ravi S. Menon,et al.  Dissociating pain from its anticipation in the human brain. , 1999, Science.

[20]  N. Moray Attention in Dichotic Listening: Affective Cues and the Influence of Instructions , 1959 .

[21]  G. Pagnoni,et al.  Does Anticipation of Pain Affect Cortical Nociceptive Systems? , 2002, The Journal of Neuroscience.

[22]  K. R. Ridderinkhof,et al.  The Role of the Medial Frontal Cortex in Cognitive Control , 2004, Science.

[23]  Juan Lupiáñez,et al.  Automatic and controlled processing in stroop negative priming : The role of attentional set , 1999 .

[24]  D. Tucker,et al.  Electrophysiological Responses to Errors and Feedback in the Process of Action Regulation , 2003, Psychological science.

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

[26]  Martial Van der Linden,et al.  Neural correlates of “hot” and “cold” emotional processing: a multilevel approach to the functional anatomy of emotion , 2003, NeuroImage.

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

[28]  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.

[29]  A. Beck,et al.  An information processing model of anxiety: automatic and strategic processes. , 1997, Behaviour research and therapy.

[30]  R Turner,et al.  Optimisation of the 3D MDEFT sequence for anatomical brain imaging: technical implications at 1.5 and 3 T , 2004, NeuroImage.

[31]  P. Matthews,et al.  Exacerbation of Pain by Anxiety Is Associated with Activity in a Hippocampal Network , 2001, The Journal of Neuroscience.

[32]  Raymond J. Dolan,et al.  Anxiety Reduction through Detachment: Subjective, Physiological, and Neural Effects , 2005, Journal of Cognitive Neuroscience.

[33]  N. Frijda The place of appraisal in emotion , 1993 .

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

[35]  C. N. Macrae,et al.  Finding the Self? An Event-Related fMRI Study , 2002, Journal of Cognitive Neuroscience.

[36]  O. John,et al.  Individual differences in two emotion regulation processes: implications for affect, relationships, and well-being. , 2003, Journal of personality and social psychology.

[37]  Joseph P. Forgas,et al.  Emotion and Social Judgments , 2020 .

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

[39]  J. Teasdale,et al.  Emotional processing, three modes of mind and the prevention of relapse in depression. , 1999, Behaviour research and therapy.

[40]  Raymond J. Dolan,et al.  Neural Correlates of Self-distraction from Anxiety and a Process Model of Cognitive Emotion Regulation , 2006, Journal of Cognitive Neuroscience.

[41]  S. Epstein,et al.  Heart rate and skin conductance during experimentally induced anxiety: effects of anticipated intensity of noxious stimulation and experience. , 1970, Journal of experimental psychology.

[42]  J. Gore,et al.  Activation of the left amygdala to a cognitive representation of fear , 2001, Nature Neuroscience.

[43]  Raja Parasuraman,et al.  Varieties of attention , 1984 .

[44]  S. Salloway,et al.  Alteration of intention and self-initiated action associated with bilateral anterior cingulotomy. , 1999, The Journal of neuropsychiatry and clinical neurosciences.

[45]  D. Broadbent,et al.  The Cognitive Failures Questionnaire (CFQ) and its correlates. , 1982, The British journal of clinical psychology.

[46]  Michael D. Robinson Running from William James' bear: A review of preattentive mechanisms and their contributions to emotional experience. , 1998 .

[47]  P. Lang The Cognitive Psychophysiology of Emotion , 2019, Anxiety and the Anxiety Disorders.

[48]  Classical Conditioning and Reinforcement Learning 9.1 Introduction , .

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

[50]  S. Christianson Emotional stress and eyewitness memory: a critical review. , 1992, Psychological bulletin.

[51]  Geraint Rees,et al.  Neural correlates of consciousness in humans , 2002, Nature Reviews Neuroscience.

[52]  Edward E. Smith,et al.  Placebo-Induced Changes in fMRI in the Anticipation and Experience of Pain , 2004, Science.

[53]  Charles S. Carver,et al.  Influence of Subliminal Visual Images on the Experience of Anxiety , 1987 .

[54]  Jennifer C. Britton,et al.  Neural correlates of individual ratings of emotional salience: a trial-related fMRI study , 2004, NeuroImage.

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

[56]  S Epstein,et al.  Heart rate and skin conductance during experimentally induced anxiety: the effect of uncertainty about receiving a noxious stimulus. , 1970, Journal of personality and social psychology.

[57]  D. S. Holmes,et al.  Effect of avoidant thinking and reappraisal for coping with threat involving temporal uncertainty. , 1974, Journal of personality and social psychology.

[58]  M. Leboyer,et al.  Conscious and subliminal conflicts in normal subjects and patients with schizophrenia: The role of the anterior cingulate , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[59]  H. Critchley The human cortex responds to an interoceptive challenge. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

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

[61]  Arne Öhman,et al.  The role of the amygdala in human fear: Automatic detection of threat , 2005, Psychoneuroendocrinology.

[62]  A. Nobre The attentive homunculus: Now you see it, now you don't , 2001, Neuroscience & Biobehavioral Reviews.

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

[64]  Leslie G. Ungerleider,et al.  Neuroimaging Studies of Attention: From Modulation of Sensory Processing to Top-Down Control , 2003, The Journal of Neuroscience.

[65]  Craig A. Smith,et al.  Toward delivering on the promise of appraisal theory. , 2001 .

[66]  Irwin G. Sarason,et al.  Emotion, Personality, and Selective Attention , 1981 .

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

[68]  R. Dolan,et al.  A Functional Anatomy of Anticipatory Anxiety , 1999, NeuroImage.

[69]  R J Howard,et al.  Persecutory delusions and the determination of self-relevance: an fMRI investigation , 2004, Psychological Medicine.

[70]  Robert D. Hare,et al.  Denial of threat and emotional response to impending painful stimulation. , 1966 .

[71]  S. Kapur,et al.  Direct Activation of the Ventral Striatum in Anticipation of Aversive Stimuli , 2003, Neuron.

[72]  K. Scherer,et al.  Appraisal processes in emotion: Theory, methods, research. , 2001 .

[73]  Marc D. Lewis Bridging emotion theory and neurobiology through dynamic systems modeling , 2005, Behavioral and Brain Sciences.

[74]  J. Maser,et al.  Anxiety and the Anxiety Disorders , 2019 .

[75]  R Turner,et al.  Optimized EPI for fMRI studies of the orbitofrontal cortex , 2003, NeuroImage.

[76]  P. Ekman,et al.  Approaches To Emotion , 1985 .

[77]  K. Scherer,et al.  The Relationship of Emotion to Cognition: A Functional Approach to a Semantic Controversy , 1987 .

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

[79]  F. Craik,et al.  In search of the emotional self: an fMRI study using positive and negative emotional words. , 2003, The American journal of psychiatry.

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

[81]  Gerald L. Clore,et al.  Moods and Their Vicissitudes: Thoughts and Feelings as Information , 1991 .

[82]  Tomás Paus,et al.  Anatomical Variability of the Anterior Cingulate Gyrus and Basic Dimensions of Human Personality , 2002, NeuroImage.

[83]  B. Mensour,et al.  Neural basis of emotional self-regulation in childhood , 2004, Neuroscience.

[84]  Joseph E LeDoux The emotional brain , 1996 .

[85]  Arne Öhman,et al.  Fear and anxiety as emotional phenomena: Clinical phenomenology, evolutionary perspectives, and information-processing mechanisms. , 1993 .