Changes in effective connectivity during incidental and intentional perception of fearful faces

The present fMRI study examined effective connectivity within an emotional network composed of three brain areas: Amygdala (AMY), Anterior Cingulate Cortex (AAC) and Orbito-Frontal (OFC) in processing fearful faces. Two tasks: an incidental perception (gender identification) and an intentional detection (effortful discrimination) task were performed by 14 and 10 young healthy volunteers, respectively. Participants were scanned while viewing fearful, neutral and ambiguous facial expressions. Effective connectivity was assessed using Structural Equation Modeling (SEM). Results show that the hypothetical network fits the experimental data for both tasks and in both hemispheres. The comparison between Tasks 1 and 2 reveals significant differences in strength and direction of the connectivity patterns for the left and to a less stringent threshold for the right hemisphere. The path coefficients analysis suggests that the fearful information generated in AMY, reaches the OFC through the ACC in incidental perception, while in intentional perception, the route followed is in a reverse direction from OFC to ACC. Our findings confirm a differential brain connectivity between incidental and intentional processing of fearful faces.

[1]  R. J Dolan,et al.  Common and distinct neural responses during direct and incidental processing of multiple facial emotions , 2003, NeuroImage.

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

[3]  E. Rolls,et al.  Face and voice expression identification in patients with emotional and behavioural changes following ventral frontal lobe damage , 1996, Neuropsychologia.

[4]  N. Sadato,et al.  Brain regions involved in verbal or non‐verbal aspects of facial emotion recognition , 2000, Neuroreport.

[5]  P. Bentler,et al.  Tests for stability in linear structural equation systems , 1983 .

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

[7]  Andrew H. Kemp,et al.  Pathways for fear perception: modulation of amygdala activity by thalamo-cortical systems , 2005, NeuroImage.

[8]  J. S. Morris,et al.  The functional anatomy of innate and acquired fear: Perspectives from neuroimaging , 2000 .

[9]  A. Young,et al.  Task instructions modulate neural responses to fearful facial expressions , 2003, Biological Psychiatry.

[10]  E. Rolls.  The orbitofrontal cortex and reward. , 2000, Cerebral cortex.

[11]  P. Bentler,et al.  Significance Tests and Goodness of Fit in the Analysis of Covariance Structures , 1980 .

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

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

[14]  D. Kennedy,et al.  The young adult human brain: an MRI-based morphometric analysis. , 1994, Cerebral cortex.

[15]  R. Kötter,et al.  Functional dissociation between medial and lateral prefrontal cortical spatiotemporal activation in negative and positive emotions: a combined fMRI/MEG study. , 2000, Cerebral cortex.

[16]  E. N. Sokolov,et al.  The dynamics of cortico-amygdala and autonomic activity over the experimental time course of fear perception. , 2004, Brain research. Cognitive brain research.

[17]  C. Büchel,et al.  Modulation of connectivity in visual pathways by attention: cortical interactions evaluated with structural equation modelling and fMRI. , 1997, Cerebral cortex.

[18]  Simon J Graham,et al.  An fMRI study investigating cognitive modulation of brain regions associated with emotional processing of visual stimuli , 2003, Neuropsychologia.

[19]  Mary Katsikitis.  The human face : measurement and meaning , 2002 .

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

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

[22]  S. Rauch,et al.  Differential prefrontal cortex and amygdala habituation to repeatedly presented emotional stimuli , 2001, Neuroreport.

[23]  Joseph E LeDoux.  Emotion Circuits in the Brain , 2000 .

[24]  A. Meyer-Lindenberg,et al.  Interindividual differences in functional interactions among prefrontal, parietal and parahippocampal regions during working memory. , 2003, Cerebral cortex.

[25]  Robert C. MacCallum,et al.  SPECIFICATION SEARCHES IN COVARIANCE STRUCTURE MODELING , 1986 .

[26]  M. Browne,et al.  Alternative Ways of Assessing Model Fit , 1992 .

[27]  Jens Frahm,et al.  COMMENTS AND CONTROVERSIES Functional MRI of the Human Amygdala , 2001 .

[28]  S. Mineka,et al.  Fears, phobias, and preparedness: toward an evolved module of fear and fear learning. , 2001, Psychological review.

[29]  Karl J. Friston,et al.  Psychophysiological and Modulatory Interactions in Neuroimaging , 1997, NeuroImage.

[30]  Tom Johnstone,et al.  Stability of amygdala BOLD response to fearful faces over multiple scan sessions , 2005, NeuroImage.

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

[32]  E. Bullmore,et al.  How Good Is Good Enough in Path Analysis of fMRI Data? , 2000, NeuroImage.

[33]  Kenneth A. Bollen,et al.  Structural Equations with Latent Variables , 1989 .

[34]  J. Fox,et al.  Effect Analysis in Structural Equation Models , 1980 .

[35]  J. Fox,et al.  Effect Analysis in Structural-Equation Models II , 1985 .

[36]  R. J. Dolan,et al.  Human Amygdala Responses to Fearful Eyes , 2002, NeuroImage.

[37]  D. Perrett,et al.  A differential neural response in the human amygdala to fearful and happy facial expressions , 1996, Nature.

[38]  Jacob Cohen,et al.  A power primer. , 1992, Psychological bulletin.

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

[40]  Karl J. Friston,et al.  A neuromodulatory role for the human amygdala in processing emotional facial expressions. , 1998, Brain : a journal of neurology.

[41]  Richard J. Davidson,et al.  Amygdalar interhemispheric functional connectivity differs between the non-depressed and depressed human brain , 2004, NeuroImage.

[42]  D. Zald.  The human amygdala and the emotional evaluation of sensory stimuli , 2003, Brain Research Reviews.

[43]  Duane T. Wegener,et al.  The problem of equivalent models in applications of covariance structure analysis. , 1993, Psychological bulletin.

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

[45]  Nick Medford,et al.  Time courses of left and right amygdalar responses to fearful facial expressions , 2001 .

[46]  M S Mega,et al.  The limbic system: an anatomic, phylogenetic, and clinical perspective. , 1997, The Journal of neuropsychiatry and clinical neurosciences.

[47]  K. Bollen.  A New Incremental Fit Index for General Structural Equation Models , 1989 .

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

[49]  P. Bentler,et al.  Cutoff criteria for fit indexes in covariance structure analysis : Conventional criteria versus new alternatives , 1999 .

[50]  T. Iidaka,et al.  Frontal lobe networks for effective processing of ambiguously expressed emotions in humans , 2003, Neuroscience Letters.

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

[52]  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.

[53]  N. Sadato,et al.  Neural Interaction of the Amygdala with the Prefrontal and Temporal Cortices in the Processing of Facial Expressions as Revealed by fMRI , 2001, Journal of Cognitive Neuroscience.

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

[55]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[56]  G. Pagnoni,et al.  Explicit and Incidental Facial Expression Processing: An fMRI Study , 2001, NeuroImage.

[57]  H. Barbas,et al.  Pathways for emotion: interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey , 2002, Neuroscience.