Representation of attitudinal knowledge: role of prefrontal cortex, amygdala and parahippocampal gyrus

It has been proposed that behavior is influenced by representations of different types of knowledge: action representations, event knowledge, attitudes and stereotypes. Attitudes (representations of a concept or object and its emotional evaluation) allow us to respond quickly to a given stimulus. In this study, we explored the representation and inhibition of attitudes. We show that right dorsolateral prefrontal cortex mediates negative attitudes whereas left ventrolateral prefrontal cortex mediates positive attitudes. Parahippocampal regions and amygdala mediate evaluative processing. Furthermore, anxiety modulates right dorsolateral prefrontal activation during negative attitude processing. Inhibition of negative attitudes activates left orbitofrontal cortex: a region that when damaged is associated with socially inappropriate behavior in patients. Inhibition of positive attitudes activates a brain system involving right inferior frontal gyrus and bilateral anterior cingulate. Thus, we show that there are dissociable networks for the representation and inhibition of attitudes.

[1]  M. Jeannerod,et al.  Awareness of action in schizophrenia , 2003, Neuroreport.

[2]  J. N. Wood.  Social cognition and the prefrontal cortex. , 2003, Behavioral and cognitive neuroscience reviews.

[3]  Marcia K. Johnson,et al.  Do alcoholic Korsakoff's syndrome patients acquire affective reactions? , 1985, Journal of experimental psychology. Learning, memory, and cognition.

[4]  J. Grafman,et al.  Ventromedial Prefrontal Cortex Lesions in Humans Eliminate Implicit Gender Stereotyping , 2001, The Journal of Neuroscience.

[5]  C. Degueldre,et al.  The Functional Anatomy of Inhibition Processes Investigated with the Hayling Task , 2001, NeuroImage.

[6]  J. Cohen,et al.  Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. , 2000, Science.

[7]  T. Robbins,et al.  The prefrontal cortex: Executive and cognitive functions. , 1998 .

[8]  D. Schacter,et al.  Do Amnesics Exhibit Cognitive Dissonance Reduction? The Role of Explicit Memory and Attention in Attitude Change , 2001, Psychological science.

[9]  J. Cummings,et al.  Frontal-subcortical circuits: the anatomic basis of executive, social and motivated behaviors , 1997, Journal of psychopharmacology.

[10]  D Y von Cramon,et al.  Segregating semantic and syntactic aspects of processing in the human brain: an fMRI investigation of different word types. , 2000, Cerebral cortex.

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

[12]  J. Lieberman,et al.  Implications for the neural basis of social cognition for the study of schizophrenia. , 2003, The American journal of psychiatry.

[13]  R. Fazio,et al.  Attitude accessibility, attitude-behavior consistency, and the strength of the object-evaluation association , 1982 .

[14]  Keith J. Holyoak,et al.  Structure and Functions of the Human Prefrontal Cortex , 1996 .

[15]  H Fischer,et al.  Differential response in the human amygdala to racial outgroup vs ingroup face stimuli , 2000, Neuroreport.

[16]  Y. He.  Attitudes as determinants of behavior. , 1965 .

[17]  R. Fazio.  On the power and functionality of attitudes: The role of attitude accessibility. , 1989 .

[18]  Max Coltheart,et al.  The MRC Psycholinguistic Database , 1981 .

[19]  D. Gaffan,et al.  Lesions of the primate rhinal cortex cause deficits in flavour–visual associative memory , 1998, Behavioural Brain Research.

[20]  R. Fazio,et al.  Variability in the likelihood of automatic attitude activation: data reanalysis and commentary on Bargh, Chaiken, Govender, and Pratto (1992) , 1993, Journal of personality and social psychology.

[21]  M. Farah,et al.  Role of left inferior prefrontal cortex in retrieval of semantic knowledge: a reevaluation. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[22]  J. O'Doherty,et al.  Automatic and intentional brain responses during evaluation of trustworthiness of faces , 2002, Nature Neuroscience.

[23]  I. Ajzen.  Nature and operation of attitudes. , 2001, Annual review of psychology.

[24]  Alex Martin,et al.  Semantic memory and the brain: structure and processes , 2001, Current Opinion in Neurobiology.

[25]  J. Cummings,et al.  Anatomic and Behavioral Aspects of Frontal‐Subcortical Circuits a , 1995, Annals of the New York Academy of Sciences.

[26]  Kenneth H. Rubin,et al.  Temperamental contributions to social behavior: the moderating roles of frontal EEG asymmetry and gender. , 2001, Journal of the American Academy of Child and Adolescent Psychiatry.

[27]  T. Robbins,et al.  Dissociable contributions of the orbitofrontal and lateral prefrontal cortex of the marmoset to performance on a detour reaching task , 2001, The European journal of neuroscience.

[28]  E. Crone,et al.  Dissociation of response conflict, attentional selection, and expectancy with functional magnetic resonance imaging. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[29]  D. Perani,et al.  The Effects of Semantic Category and Knowledge Type on Lexical-Semantic Access: A PET Study , 1998, NeuroImage.

[30]  J. Desmond,et al.  Functional Specialization for Semantic and Phonological Processing in the Left Inferior Prefrontal Cortex , 1999, NeuroImage.

[31]  M. Mega,et al.  The Neuropsychiatric Inventory , 1994, Neurology.

[32]  J. Grafman,et al.  Category-Specific Representations of Social and Nonsocial Knowledge in the Human Prefrontal Cortex , 2003, Journal of Cognitive Neuroscience.

[33]  E. Stein,et al.  Right hemispheric dominance of inhibitory control: an event-related functional MRI study. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[34]  M. Jeannerod.  The mechanism of self-recognition in humans , 2003, Behavioural Brain Research.

[35]  Wendy A Suzuki,et al.  The anatomy, physiology and functions of the perirhinal cortex , 1996, Current Opinion in Neurobiology.

[36]  Terry M. Peters,et al.  3D statistical neuroanatomical models from 305 MRI volumes , 1993, 1993 IEEE Conference Record Nuclear Science Symposium and Medical Imaging Conference.

[37]  M. J. Rosenberg.  Attitude Organization and Change: An Analysis of Consistency among Attitude Components , 1980 .

[38]  Y. Miyashita,et al.  No‐go dominant brain activity in human inferior prefrontal cortex revealed by functional magnetic resonance imaging , 1998, The European journal of neuroscience.

[39]  Richard S. J. Frackowiak,et al.  The anatomy of phonological and semantic processing in normal subjects. , 1992, Brain : a journal of neurology.

[40]  R. Davidson.  Toward a Biology of Personality and Emotion , 2001, Annals of the New York Academy of Sciences.

[41]  N. Fox,et al.  Behavioral and psychophysiological correlates of self-presentation in temperamentally shy children. , 1999, Developmental psychobiology.

[42]  S. Breckler.  Empirical validation of affect, behavior, and cognition as distinct components of attitude. , 1984, Journal of personality and social psychology.

[43]  J. Cummings,et al.  Frontal-subcortical circuits and human behavior. , 1993, Journal of psychosomatic research.

[44]  Frank R. Kardes,et al.  On the automatic activation of attitudes. , 1986 .

[45]  Peter Olausson,et al.  Impairments of Reversal Learning and Response Perseveration after Repeated, Intermittent Cocaine Administrations to Monkeys , 2002, Neuropsychopharmacology.

[46]  A. Damasio.  The somatic marker hypothesis and the possible functions of the prefrontal cortex. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[47]  Francesco Fera,et al.  The Amygdala Response to Emotional Stimuli: A Comparison of Faces and Scenes , 2002, NeuroImage.

[48]  Anthony G. Greenwald,et al.  Attitude structure and function , 1990 .

[49]  A. Damasio.  On Some Functions of the Human Prefrontal Cortex a , 1995, Annals of the New York Academy of Sciences.

[50]  David C. Alsop,et al.  Brain Activation during Facial Emotion Processing , 2002, NeuroImage.

[51]  G. Micheletti.  The Prefrontal Cortex. Anatomy, Physiology and Neuropsychology of the Frontal Lobe, Fuster J.M.. Raven Press, New York (1989) , 1989 .

[52]  R. Dolan,et al.  The functional anatomy of humor: segregating cognitive and affective components , 2001, Nature Neuroscience.

[53]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited , 1995, NeuroImage.

[54]  J. Fuster.  The Prefrontal Cortex , 1997 .

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

[56]  Newell,et al.  A neural basis for general intelligence , 2000, American journal of ophthalmology.

[57]  H. Weingartner,et al.  The effects of lateralized frontal lesions on mood regulation. , 1986, Brain : a journal of neurology.

[58]  P. Skudlarski,et al.  An event-related functional MRI study of the stroop color word interference task. , 2000, Cerebral cortex.

[59]  Hugh Garavan,et al.  Right hemispheric dominance of inhibitory control: an event-related fMRI study. , 1999 .

[60]  N. Fox,et al.  Frontal brain asymmetry predicts infants' response to maternal separation. , 1989, Journal of abnormal psychology.

[61]  C. Frith,et al.  Reading the mind in cartoons and stories: an fMRI study of ‘theory of mind’ in verbal and nonverbal tasks , 2000, Neuropsychologia.

[62]  S. Chaiken,et al.  The generality of the automatic attitude activation effect. , 1992, Journal of personality and social psychology.

[63]  Y. Miyashita,et al.  Common inhibitory mechanism in human inferior prefrontal cortex revealed by event-related functional MRI. , 1999, Brain : a journal of neurology.

[64]  M Jeannerod,et al.  The prefrontal cortex and conscious monitoring of action An experimental study , 2003, Neuropsychologia.

[65]  J. Grafman,et al.  Human prefrontal cortex: processing and representational perspectives , 2003, Nature Reviews Neuroscience.

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

[67]  M Erb,et al.  Differential activation in parahippocampal and prefrontal cortex during word and face encoding tasks , 2001, Neuroreport.

[68]  M. J. Rosenberg.  Cognitive, Affective and Behavioral Components of Attitudes , 1960 .

[69]  Cheuk Y. Tang,et al.  Differential amygdala activation during emotional decision and recognition memory tasks using unpleasant words: an fMRI study , 2001, Neuropsychologia.

[70]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[71]  P. Roland,et al.  Interference between two concurrent tasks is associated with activation of overlapping fields in the cortex. , 1997, Brain research. Cognitive brain research.

[72]  F. Happé,et al.  Acquired mind-blindness following frontal lobe surgery? A single case study of impaired ‘theory of mind’ in a patient treated with stereotactic anterior capsulotomy , 2001, Neuropsychologia.

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

[74]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[75]  David M. Sanbonmatsu,et al.  On the automatic activation of attitudes. , 1986, Journal of personality and social psychology.

[76]  S. Pappatà,et al.  Cortical Networks Implicated in Semantic and Episodic Memory: Common or Unique? , 1998, Cortex.

[77]  Florin Dolcos,et al.  Similarities and Differences in the Neural Correlates of Episodic Memory Retrieval and Working Memory , 2002, NeuroImage.

[78]  Michael Davis,et al.  The amygdala , 2000, Current Biology.

[79]  Richard S. J. Frackowiak,et al.  Functional anatomy of a common semantic system for words and pictures , 1996, Nature.

[80]  S. Chaiken,et al.  The Automatic Evaluation Effect: Unconditional Automatic Attitude Activation with a Pronunciation Task , 1996 .

[81]  N. Fox,et al.  The psychobiology of affective development , 1985 .

[82]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.

[83]  福田 博一.  State-Trait Anxiety Inventoryによるペインクリニック外来患者の不安の評価 , 1994 .

[84]  N. Fox,et al.  Individual differences in response to stress and cerebral asymmetry. , 1992 .

[85]  Joseph E LeDoux,et al.  Perirhinal Cortex and Thalamic Stimulation Induces LTP in Different Areas of the Amygdala , 2000 .

[86]  D. Weinberger,et al.  Neocortical modulation of the amygdala response to fearful stimuli , 2003, Biological Psychiatry.

[87]  Matthew D. Lieberman,et al.  The emergence of social cognitive neuroscience. , 2001, The American psychologist.

[88]  M. J. Rosenberg,et al.  Attitude organization and change. An analysis of consistency among attitude components. , 1961 .

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

[90]  Michael Wilson.  MRC Psycholinguistic Database , 2001 .

[91]  J. Spatt.  Déjà vu: possible parahippocampal mechanisms. , 2002, The Journal of neuropsychiatry and clinical neurosciences.

[92]  E. Higgins,et al.  Handbook of motivation and cognition : foundations of social behavior , 1991 .

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

[94]  M. Kinsbourne.  Asymmetrical function of the brain , 1978 .

[95]  Norman W. Park,et al.  Automatic activation of positive but not negative attitudes after traumatic brain injury , 2001, Neuropsychologia.

[96]  William A. Cunningham,et al.  Performance on Indirect Measures of Race Evaluation Predicts Amygdala Activation , 2000, Journal of Cognitive Neuroscience.

[97]  R. Spinks.  The Prefrontal Cortex: Anatomy, Physiology, and Neuropsychology of the Frontal Lobe, 3rd ed. , 2000 .

[98]  R. Fazio.  How do attitudes guide behavior , 1986 .

[99]  Jemett L. Desmond,et al.  Semantic encoding and retrieval in the left inferior prefrontal cortex: a functional MRI study of task difficulty and process specificity , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.