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Published in: Experimental Brain Research 1/2007

01-10-2007 | Research Article

Threat sensitivity as assessed by automatic amygdala response to fearful faces predicts speed of visual search for facial expression

Authors: Patricia Ohrmann, Astrid Veronika Rauch, Jochen Bauer, Harald Kugel, Volker Arolt, Walter Heindel, Thomas Suslow

Published in: Experimental Brain Research | Issue 1/2007

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Abstract

It has been argued that the amygdala represents an integral component of a vigilance system that is primarily involved in the perception of ambiguous stimuli of biological relevance. The present investigation was conducted to examine the relationship between automatic amygdala responsivity to fearful faces which may be interpreted as an index of trait-like threat sensitivity and spatial processing characteristics of facial emotions. During 3T fMRI scanning, pictures of human faces bearing fearful, angry, and happy expressions were presented to 20 healthy volunteers using a backward masking procedure based on neutral facial expressions. Subsequently, a computer-based face-in-the-crowd task using schematic face stimuli was administered. The neural response of the (right) amygdala to masked fearful faces correlated consistently with response speed to negative and neutral faces. Neither amygdala activation during the masked presentation of angry faces nor amygdala activation during the presentation of happy faces was correlated with any of the response latencies in the face-in-the-crowd task. Our results suggest that amygdala responsivity to masked facial expression is differentially related to the general visual search speed for facial expression. Neurobiologically defined threat sensitivity seems to represent an important determinant of visual scanning behaviour.
Literature
go back to reference Aguirre G, Zarahn E, D’Esposito M (1998) The inferential impact of global signal covariates in functional neuroimaging analyses. Neuroimage 8:302–306PubMedCrossRef Aguirre G, Zarahn E, D’Esposito M (1998) The inferential impact of global signal covariates in functional neuroimaging analyses. Neuroimage 8:302–306PubMedCrossRef
go back to reference Beringer J (1999) Experimental run time system. Version 3.28. User’s manual. BeriSoft, Frankfurt Beringer J (1999) Experimental run time system. Version 3.28. User’s manual. BeriSoft, Frankfurt
go back to reference Bishop S, Duncan J, Lawrence AD (2004) State anxiety modulation of the amygdala response to unattended threat-related stimuli. J Neurosci 24:10364–10368PubMedCrossRef Bishop S, Duncan J, Lawrence AD (2004) State anxiety modulation of the amygdala response to unattended threat-related stimuli. J Neurosci 24:10364–10368PubMedCrossRef
go back to reference Bradley BP, Mogg K, Falla SJ, Hamilton JR (1998) Attentional bias for threatening facial expressions in anxiety: manipulation of stimulus duration. Cogn Emot 12:737–753CrossRef Bradley BP, Mogg K, Falla SJ, Hamilton JR (1998) Attentional bias for threatening facial expressions in anxiety: manipulation of stimulus duration. Cogn Emot 12:737–753CrossRef
go back to reference Bradley BP, Mogg K, White J, Groom C, deBono J (1999) Attentional bias for emotional faces in generalized anxiety disorder. Br J Clin Psychol 38:267–278PubMedCrossRef Bradley BP, Mogg K, White J, Groom C, deBono J (1999) Attentional bias for emotional faces in generalized anxiety disorder. Br J Clin Psychol 38:267–278PubMedCrossRef
go back to reference Brett M, Anton JL, Valabregue R, Poline JB (2002) Region of interest analysis using an SPM toolbox. Neuroimage 16:497 (abstract) Brett M, Anton JL, Valabregue R, Poline JB (2002) Region of interest analysis using an SPM toolbox. Neuroimage 16:497 (abstract)
go back to reference Critchley H, Daly E, Phillips M, Brammer M, Bullmore E, Williams S, van Amelsvoort T, Robertson D, David A, Murphy D (2000) Explicit and implicit neural mechanisms for processing of social information from facial expressions: a functional magnetic resonance imaging study. Hum Brain Mapp 9:93–105PubMedCrossRef Critchley H, Daly E, Phillips M, Brammer M, Bullmore E, Williams S, van Amelsvoort T, Robertson D, David A, Murphy D (2000) Explicit and implicit neural mechanisms for processing of social information from facial expressions: a functional magnetic resonance imaging study. Hum Brain Mapp 9:93–105PubMedCrossRef
go back to reference Das P, Kemp AH, Liddell BJ, Brown KJ, Olivieri G, Peduto A, Gordon E, Williams LM (2005) Pathways for fear perception: modulation of amygdala activity by thalamo-cortical systems. Neuroimage 26:141–148PubMedCrossRef Das P, Kemp AH, Liddell BJ, Brown KJ, Olivieri G, Peduto A, Gordon E, Williams LM (2005) Pathways for fear perception: modulation of amygdala activity by thalamo-cortical systems. Neuroimage 26:141–148PubMedCrossRef
go back to reference Ekman P, Friesen WV (1976) Pictures of facial affect. Consulting Psychologists, Palo Alto Ekman P, Friesen WV (1976) Pictures of facial affect. Consulting Psychologists, Palo Alto
go back to reference Esteves F, Öhman A (1993) Masking the face: recognition of emotional facial expressions as a function of the parameters of backward masking. Scand J Psychol 34:1–18PubMed Esteves F, Öhman A (1993) Masking the face: recognition of emotional facial expressions as a function of the parameters of backward masking. Scand J Psychol 34:1–18PubMed
go back to reference Etkin A, Klemenhagen KC, Dudman JT, Rogan MT, Hen R, Kandel ER, Hirsch J (2004) Individual differences in trait anxiety predict the response of the basolateral amygdala to unconsciously processed fearful faces. Neuron 44:1043–1055PubMedCrossRef Etkin A, Klemenhagen KC, Dudman JT, Rogan MT, Hen R, Kandel ER, Hirsch J (2004) Individual differences in trait anxiety predict the response of the basolateral amygdala to unconsciously processed fearful faces. Neuron 44:1043–1055PubMedCrossRef
go back to reference Eysenck MW (1992) Anxiety. The cognitive perspective. Lawrence Erlbaum, Hillsdale Eysenck MW (1992) Anxiety. The cognitive perspective. Lawrence Erlbaum, Hillsdale
go back to reference Fox E (2002) Processing emotional facial expressions: the role of anxiety and awareness. Cogn Affect Behav Neurosci 2:53–62CrossRef Fox E (2002) Processing emotional facial expressions: the role of anxiety and awareness. Cogn Affect Behav Neurosci 2:53–62CrossRef
go back to reference Fox E, Lester V, Russo R, Bowles RJ, Pichler A, Dutton K (2000) Facial expressions of emotion: are angry faces detected more efficiently? Cogn Emot 14:61–92PubMedCrossRef Fox E, Lester V, Russo R, Bowles RJ, Pichler A, Dutton K (2000) Facial expressions of emotion: are angry faces detected more efficiently? Cogn Emot 14:61–92PubMedCrossRef
go back to reference Gläscher J, Adolphs R (2003) Processing of the arousal of subliminal and supraliminal emotional stimuli by the human amygdala. J Neurosci 23:10274–10282PubMed Gläscher J, Adolphs R (2003) Processing of the arousal of subliminal and supraliminal emotional stimuli by the human amygdala. J Neurosci 23:10274–10282PubMed
go back to reference Hanley JA, McNeil BJ (1983) A method of comparing the areas under the receiver operating characteristic curve derived from the same cases. Radiology 148:839–843PubMed Hanley JA, McNeil BJ (1983) A method of comparing the areas under the receiver operating characteristic curve derived from the same cases. Radiology 148:839–843PubMed
go back to reference Hutchinson M, Schiffer W, Joseffer S, Liu U, Schlosser RD, Dikshit S, Goldberg E, Brodie JD (1999) Task-specific deactivation patterns in functional magnetic resonance imaging. Magn Reson Imaging 17:1427–1436PubMedCrossRef Hutchinson M, Schiffer W, Joseffer S, Liu U, Schlosser RD, Dikshit S, Goldberg E, Brodie JD (1999) Task-specific deactivation patterns in functional magnetic resonance imaging. Magn Reson Imaging 17:1427–1436PubMedCrossRef
go back to reference Izard CE, Dougherty FE, Bloxom BM, Kotsch WE (1974) The Differential Emotions Scale: a method of measuring the subjective experience of discrete emotions. Vanderbilt University, Nashville Izard CE, Dougherty FE, Bloxom BM, Kotsch WE (1974) The Differential Emotions Scale: a method of measuring the subjective experience of discrete emotions. Vanderbilt University, Nashville
go back to reference Karparova SP, Kersting A, Suslow T (2005) Disengagement of attention from facial emotion in unipolar depression. Psychiatry Clin Neurosci 59:723–729PubMedCrossRef Karparova SP, Kersting A, Suslow T (2005) Disengagement of attention from facial emotion in unipolar depression. Psychiatry Clin Neurosci 59:723–729PubMedCrossRef
go back to reference Killgore WD, Yurgelun-Todd DA (2004) Activation of the amygdala and anterior cingulate during nonconscious processing of sad versus happy faces. Neuroimage 21:1215–1223PubMedCrossRef Killgore WD, Yurgelun-Todd DA (2004) Activation of the amygdala and anterior cingulate during nonconscious processing of sad versus happy faces. Neuroimage 21:1215–1223PubMedCrossRef
go back to reference Lange K, Williams LM, Young AW, Bullmore ET, Brammer MJ, Williams SCR, Gray JA, Phillips ML (2003) Task instructions modulate neural responses to fearful facial expressions. Biol Psychiatry 53:226–232PubMedCrossRef Lange K, Williams LM, Young AW, Bullmore ET, Brammer MJ, Williams SCR, Gray JA, Phillips ML (2003) Task instructions modulate neural responses to fearful facial expressions. Biol Psychiatry 53:226–232PubMedCrossRef
go back to reference Laux L, Glanzmann P, Schaffner P, Spielberger CD (1981) Das State-Trait Angstinventar. Beltz, Weinheim Laux L, Glanzmann P, Schaffner P, Spielberger CD (1981) Das State-Trait Angstinventar. Beltz, Weinheim
go back to reference LeDoux JE (1996) The emotional brain. Simon and Schuster, New York LeDoux JE (1996) The emotional brain. Simon and Schuster, New York
go back to reference Macmillan NA, Creelman CD (1991) Detection theory: a user’s guide. Cambridge University Press, Cambridge Macmillan NA, Creelman CD (1991) Detection theory: a user’s guide. Cambridge University Press, Cambridge
go back to reference McKelvie S (1973) The meaningfulness and meaning of schematic faces. Percept Psychophys 14:343–348 McKelvie S (1973) The meaningfulness and meaning of schematic faces. Percept Psychophys 14:343–348
go back to reference Merten J, Krause R (1993) DAS (Differentielle Affektskala). Saarbrücken: Arbeiten der Fachrichtung Psychologie der Universität des Saarlandes, Nr. 173. Fachbereich Psychologie, Universität Saarbrücken, Saarbrücken Merten J, Krause R (1993) DAS (Differentielle Affektskala). Saarbrücken: Arbeiten der Fachrichtung Psychologie der Universität des Saarlandes, Nr. 173. Fachbereich Psychologie, Universität Saarbrücken, Saarbrücken
go back to reference Morris JS, Frith CD, Perrett DI, Rowland D, Young AW, Calder AJ, Dolan RJ (1996) A differential neural response in the human amygdala to fearful and happy facial expressions. Nature 383:812–815PubMedCrossRef Morris JS, Frith CD, Perrett DI, Rowland D, Young AW, Calder AJ, Dolan RJ (1996) A differential neural response in the human amygdala to fearful and happy facial expressions. Nature 383:812–815PubMedCrossRef
go back to reference Morris JS, Friston KJ, Büchel C, Frith CD, Young AW, Calder AJ, Dolan RJ (1998a) A neuromodulatory role for the human amygdala in processing emotional facial expressions. Brain 121:47–57PubMedCrossRef Morris JS, Friston KJ, Büchel C, Frith CD, Young AW, Calder AJ, Dolan RJ (1998a) A neuromodulatory role for the human amygdala in processing emotional facial expressions. Brain 121:47–57PubMedCrossRef
go back to reference Morris JS, Öhman A, Dolan RJ (1998b) Conscious and unconscious emotional learning in the human amygdala. Nature 393:467–470PubMedCrossRef Morris JS, Öhman A, Dolan RJ (1998b) Conscious and unconscious emotional learning in the human amygdala. Nature 393:467–470PubMedCrossRef
go back to reference Morris JS, Öhman A, Dolan RJ (1999) A subcortical pathway to the right amygdala mediating “unseen” fear. Proc Natl Acad Sci USA 96:1680–1685PubMedCrossRef Morris JS, Öhman A, Dolan RJ (1999) A subcortical pathway to the right amygdala mediating “unseen” fear. Proc Natl Acad Sci USA 96:1680–1685PubMedCrossRef
go back to reference Nomura M, Ohira H, Haneda K, Iidaka T, Sadato N, Okada T, Yonekura Y (2004) Functional association of the amygdala and ventral prefrontal cortex during cognitive evaluation of facial expressions primed by masked angry faces: an event-related fMRI study. Neuroimage 21:352–363PubMedCrossRef Nomura M, Ohira H, Haneda K, Iidaka T, Sadato N, Okada T, Yonekura Y (2004) Functional association of the amygdala and ventral prefrontal cortex during cognitive evaluation of facial expressions primed by masked angry faces: an event-related fMRI study. Neuroimage 21:352–363PubMedCrossRef
go back to reference Öhman A, Lunqvist D, Esteves F (2001) The face in the crowd revisited: a threat advantage with schematic stimuli. J Pers Soc Psychol 80:381–396PubMedCrossRef Öhman A, Lunqvist D, Esteves F (2001) The face in the crowd revisited: a threat advantage with schematic stimuli. J Pers Soc Psychol 80:381–396PubMedCrossRef
go back to reference Purcell DG, Stewart AL, Skov RB (1996) It takes a confounded face to pop out of a crowd. Perception 25:1091–1108PubMedCrossRef Purcell DG, Stewart AL, Skov RB (1996) It takes a confounded face to pop out of a crowd. Perception 25:1091–1108PubMedCrossRef
go back to reference Rauch SL, Whalen PJ, Shin LM, McInerney SC, Macklin ML, Lasko NB, Orr SP, Pitman RK (2000) Exaggerated amygdala response to masked facial stimuli in posttraumatic stress disorder: a functional MRI study. Biol Psychiatry 47:769–776PubMedCrossRef Rauch SL, Whalen PJ, Shin LM, McInerney SC, Macklin ML, Lasko NB, Orr SP, Pitman RK (2000) Exaggerated amygdala response to masked facial stimuli in posttraumatic stress disorder: a functional MRI study. Biol Psychiatry 47:769–776PubMedCrossRef
go back to reference Schienle A, Schäfer A, Stark R, Walter B, Vaitl D (2005) Relationship between disgust sensitivity, trait anxiety and brain activity during disgust induction. Neuropsychobiology 51:86–92PubMedCrossRef Schienle A, Schäfer A, Stark R, Walter B, Vaitl D (2005) Relationship between disgust sensitivity, trait anxiety and brain activity during disgust induction. Neuropsychobiology 51:86–92PubMedCrossRef
go back to reference Spielberger CD, Gorsuch RL, Lushene RE (1970) Manual for the State-Trait Anxiety Inventory. Consulting Psychologists, Palo Alto Spielberger CD, Gorsuch RL, Lushene RE (1970) Manual for the State-Trait Anxiety Inventory. Consulting Psychologists, Palo Alto
go back to reference Suslow T, Junghanns K, Arolt V (2001) Detection of facial expressions of emotions in depression. Percept Mot Skills 92:857–868PubMedCrossRef Suslow T, Junghanns K, Arolt V (2001) Detection of facial expressions of emotions in depression. Percept Mot Skills 92:857–868PubMedCrossRef
go back to reference Suslow T, Roestel C, Ohrmann P, Arolt V (2003) Detection of facial expressions of emotions in schizophrenia. Schizophr Res 64:137–145PubMedCrossRef Suslow T, Roestel C, Ohrmann P, Arolt V (2003) Detection of facial expressions of emotions in schizophrenia. Schizophr Res 64:137–145PubMedCrossRef
go back to reference Suslow T, Dannlowski U, Lalee-Mentzel J, Donges US, Arolt V, Kersting A (2004) Spatial processing of facial emotion in patients with unipolar depression: a longitudinal study. J Affect Disord 83:59–63PubMedCrossRef Suslow T, Dannlowski U, Lalee-Mentzel J, Donges US, Arolt V, Kersting A (2004) Spatial processing of facial emotion in patients with unipolar depression: a longitudinal study. J Affect Disord 83:59–63PubMedCrossRef
go back to reference Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 19:513–531 Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 19:513–531
go back to reference Vuilleumier P, Armony JL, Driver J, Dolan RJ (2003) Distinct spatial frequency sensitivities for processing faces and emotional expressions. Nat Neurosci 6:624–631PubMedCrossRef Vuilleumier P, Armony JL, Driver J, Dolan RJ (2003) Distinct spatial frequency sensitivities for processing faces and emotional expressions. Nat Neurosci 6:624–631PubMedCrossRef
go back to reference Whalen PJ (1998) Fear, vigilance, and ambiguity: initial neuroimaging studies of the human amygdala. Curr Dir Psychol Sci 7:177–188CrossRef Whalen PJ (1998) Fear, vigilance, and ambiguity: initial neuroimaging studies of the human amygdala. Curr Dir Psychol Sci 7:177–188CrossRef
go back to reference Whalen PJ, Rauch SL, Etcoff NL, McInerney SC, Lee MB, Jenike MA (1998) Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. J Neurosci 18:411–418PubMed Whalen PJ, Rauch SL, Etcoff NL, McInerney SC, Lee MB, Jenike MA (1998) Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. J Neurosci 18:411–418PubMed
go back to reference White M (1995) Preattentive analysis of facial expressions of emotion. Cogn Emot 9:439–460 White M (1995) Preattentive analysis of facial expressions of emotion. Cogn Emot 9:439–460
go back to reference Williams JMG, Watts FN, MacLeod C, Mathews A (1997) Cognitive psychology and emotional disorders. Wiley, Chichester Williams JMG, Watts FN, MacLeod C, Mathews A (1997) Cognitive psychology and emotional disorders. Wiley, Chichester
go back to reference Williams MA, Morris AP, McGlone F, Abbott DF, Mattingley JB (2004) Amygdala responses to fearful and happy facial expressions under conditions of binocular suppression. J Neurosci 24:2898–2904PubMedCrossRef Williams MA, Morris AP, McGlone F, Abbott DF, Mattingley JB (2004) Amygdala responses to fearful and happy facial expressions under conditions of binocular suppression. J Neurosci 24:2898–2904PubMedCrossRef
go back to reference Williams LM, Liddell BJ, Kemp AH, Bryant RA, Meares RA, Peduto AS, Gordon E (2006) Amygdala-prefrontal dissociation of subliminal and supraliminal fear. Hum Brain Mapp 27:652–661PubMedCrossRef Williams LM, Liddell BJ, Kemp AH, Bryant RA, Meares RA, Peduto AS, Gordon E (2006) Amygdala-prefrontal dissociation of subliminal and supraliminal fear. Hum Brain Mapp 27:652–661PubMedCrossRef
Metadata
Title
Threat sensitivity as assessed by automatic amygdala response to fearful faces predicts speed of visual search for facial expression
Authors
Patricia Ohrmann
Astrid Veronika Rauch
Jochen Bauer
Harald Kugel
Volker Arolt
Walter Heindel
Thomas Suslow
Publication date
01-10-2007
Publisher
Springer-Verlag
Published in
Experimental Brain Research / Issue 1/2007
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI
https://doi.org/10.1007/s00221-007-1022-0

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