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Electrophysiological evidence of attentional biases in social anxiety disorder

Published online by Cambridge University Press:  15 December 2008

E. M. Mueller
Affiliation:
Department of Psychology, Boston University, Boston, MA, USA Department of Psychology, Harvard University, Cambridge, MA, USA
S. G. Hofmann
Affiliation:
Department of Psychology, Boston University, Boston, MA, USA
D. L. Santesso
Affiliation:
Department of Psychology, Harvard University, Cambridge, MA, USA
A. E. Meuret
Affiliation:
Department of Psychology, Southern Methodist University, Dallas, TX, USA
S. Bitran
Affiliation:
Department of Psychology, Boston University, Boston, MA, USA
D. A. Pizzagalli*
Affiliation:
Department of Psychology, Harvard University, Cambridge, MA, USA
*
*Address for correspondence: D. A. Pizzagalli, Ph.D., Department of Psychology, Harvard University, 1220 William James Hall, 33 Kirkland Street, Cambridge, MA 02138, USA. (Email: [email protected])

Abstract

Background

Previous studies investigating attentional biases in social anxiety disorder (SAD) have yielded mixed results. Recent event-related potential (ERP) studies using the dot-probe paradigm in non-anxious participants have shown that the P1 component is sensitive to visuospatial attention towards emotional faces. We used a dot-probe task in conjunction with high-density ERPs and source localization to investigate attentional biases in SAD.

Method

Twelve SAD and 15 control participants performed a modified dot-probe task using angry–neutral and happy–neutral face pairs. The P1 component elicited by face pairs was analyzed to test the hypothesis that SAD participants would display early hypervigilance to threat-related cues. The P1 component to probes replacing angry, happy or neutral faces was used to evaluate whether SAD participants show either sustained hypervigilance or decreased visual processing of threat-related cues at later processing stages.

Results

Compared to controls, SAD participants showed relatively (a) potentiated P1 amplitudes and fusiform gyrus (FG) activation to angry–neutral versus happy–neutral face pairs; (b) decreased P1 amplitudes to probes replacing emotional (angry and happy) versus neutral faces; and (c) higher sensitivity (d′) to probes following angry–neutral versus happy–neutral face pairs. SAD participants also showed significantly shorter reaction times (RTs) to probes replacing angry versus happy faces, but no group differences emerged for RT.

Conclusions

The results provide electrophysiological support for early hypervigilance to angry faces in SAD with involvement of the FG, and reduced visual processing of emotionally salient locations at later stages of information processing, which might be a manifestation of attentional avoidance.

Type
Original Articles
Copyright
Copyright © 2008 Cambridge University Press

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References

Adolphs, R (2002). Recognizing emotion from facial expressions: psychological and neurological mechanisms. Behavioral and Cognitive Neuroscience Reviews 1, 2161.CrossRefGoogle ScholarPubMed
Amaral, DG, Price, JL, Pitkanen, A, Carmichael, ST (1992). Anatomical organization of the primate amygdaloid complex. In The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction (ed. Aggleton, J. P.), pp. 166. Wiley: New York.Google Scholar
Amir, N, Foa, EB, Coles, ME (1998). Automatic activation and strategic avoidance of threat-relevant information in social phobia. Journal of Abnormal Psychology 107, 285290.Google Scholar
Bar-Haim, Y, Lamy, D, Pergamin, L, Bakermans-Kranenburg, MJ, van Ijzendoorn, MH (2007). Threat-related attentional bias in anxious and nonanxious individuals: a meta-analytic study. Psychological Bulletin 133, 124.CrossRefGoogle ScholarPubMed
Beck, AT, Steer, RA, Brown, GK (1996). Beck Depression Inventory: Manual, 2nd edn. The Psychological Corporation: San Antonio, TX.Google Scholar
Bentin, S, Allison, T, Puce, A, Perez, E, McCarthy, G (1996). Electrophysiological studies of face perception in human. Journal of Cognitive Neuroscience 8, 551565.Google Scholar
Buchel, C, Dolan, RJ (2000). Classical fear conditioning in functional neuroimaging. Current Opinion in Neurobiology 10, 219223.Google Scholar
Chapman, LJ, Chapman, JP (1987). The measurement of handedness. Brain and Cognition 6, 175183.CrossRefGoogle ScholarPubMed
Chen, YP, Ehlers, A, Clark, DM, Mansell, W (2002). Patients with generalized social phobia direct their attention away from faces. Behaviour Research and Therapy 40, 677687.CrossRefGoogle ScholarPubMed
Clark, DM, Wells, A (1995). A cognitive model of social phobia. In Social Phobia: Diagnosis, Assessment, and Treatment (ed. Heimberg, R., Liebowitz, M., Hope, D. A. and Schneier, F. R.), pp. 6993. Guilford Press: New York.Google Scholar
Clark, VP, Hillyard, SA (1996). Spatial selective attention affects early extrastriate but not striate components of the visual evoked potential. Journal of Cognitive Neuroscience 8, 387402.CrossRefGoogle Scholar
Cooney, RE, Atlas, LY, Joormann, J, Eugène, F, Gotlib, IH (2006). Amygdala activation in the processing of neutral faces in social anxiety disorder: is neutral really neutral? Psychiatry Research: Neuroimaging 148, 5559.CrossRefGoogle ScholarPubMed
Di Russo, F, Martínez, A, Hillyard, SA (2003). Source analysis of event-related cortical activity during visuo-spatial attention. Cerebral Cortex 13, 486499.CrossRefGoogle ScholarPubMed
DiNardo, PA, Brown, TA, Barlow, DH (1994). Anxiety Disorders Interview Schedule for DSM-IV. Oxford University Press: Oxford.Google Scholar
Eimer, M, Holmes, A (2007). Event-related brain potential correlates of emotional face processing. Neuropsychologia 45, 1531.CrossRefGoogle ScholarPubMed
Ekman, P, Friesen, WV (1976). Pictures of Facial Affect. Consulting Psychologists Press: Palo Alto, CA.Google Scholar
Etkin, AE, Wager, TD (2007). Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. American Journal of Psychiatry 164, 14761488.CrossRefGoogle ScholarPubMed
Eysenck, MW (1992). Anxiety: The Cognitive Perspective. Psychology Press: Hove.Google Scholar
Fox, E, Russo, R, Dutton, K (2002). Attentional bias for threat: evidence for delayed disengagement from emotional faces. Cognition and Emotion 16, 355379.Google Scholar
Fu, S, Caggiano, DM, Greenwood, PM, Parasuraman, R (2005 a). Event-related potentials reveal dissociable mechanisms for orienting and focusing visuospatial attention. Brain Research: Cognitive Brain Research 23, 341353.Google ScholarPubMed
Fu, S, Greenwood, PM, Parasuraman, R (2005 b). Brain mechanisms of involuntary visuospatial attention: an event-related potential study. Human Brain Mapping 25, 378390.Google Scholar
Garner, M, Mogg, K, Bradley, BP (2006). Orienting and maintenance of gaze to facial expressions in social anxiety. Journal of Abnormal Psychology 115, 760770.CrossRefGoogle ScholarPubMed
Green, D, Swets, J (1966). Signal Detection Theory and Psychophysics. Wiley: New York.Google Scholar
Halgren, E, Baudena, P, Heit, G, Clarke, JM, Marinkovic, K, Clarke, M (1994). Spatio-temporal stages in face and word processing. I. Depth-recorded potentials in the human occipital, temporal and parietal lobes. Journal of Physiology 88, 150.Google ScholarPubMed
Hämäläinen, MS (1995). Discrete and distributed source estimates. In Source Localization: Continuing Discussion of the Inverse Problem. ISBET Newsletter No. 6 (ed. Skrandies, W.), pp. 912.Google Scholar
Handy, TC, Green, V, Klein, RM, Mangun, GR (2001). Combined expectancies: event-related potentials reveal the early benefits of spatial attention that are obscured by reaction time measures. Journal of Experimental Psychology: Human Perception and Performance 27, 303317.Google ScholarPubMed
Heinrichs, N, Hofmann, SG (2001). Information processing in social phobia: a critical review. Clinical Psychology Review 21, 751770.CrossRefGoogle ScholarPubMed
Heuer, K, Rinck, M, Becker, ES (2007). Avoidance of emotional facial expressions in social anxiety: the Approach-Avoidance Task. Behaviour Research and Therapy 45, 29903001.Google Scholar
Hillyard, SA, Anllo-Vento, L (1998). Event-related brain potentials in the study of visual selective attention. Proceedings of the National Academy of Sciences of the United States of America 95, 781787.Google Scholar
Hopfinger, JB, West, VM (2006). Interactions between endogenous and exogenous attention on cortical visual processing. NeuroImage 31, 774789.Google Scholar
Hofmann, SG (2007). Cognitive factors that maintain social anxiety disorder: a comprehensive model and its treatment implications. Cognitive Behaviour Therapy 36, 195209.CrossRefGoogle ScholarPubMed
Horley, K, Williams, LM, Gonsalvez, C, Gordon, E (2003). Social phobics do not see eye to eye: a visual scanpath study of emotional expression processing. Journal of Anxiety Disorders 17, 3344.Google Scholar
Horley, K, Williams, LM, Gonsalvez, C, Gordon, E (2004). Face to face: visual scanpath evidence for abnormal processing of facial expressions in social phobia. Psychiatry Research 127, 4353.Google Scholar
Klucharev, V, Sams, M (2004). Interaction of gaze direction and facial expressions processing: ERP study. Neuroreport 15, 621625.Google Scholar
Kolassa, IT, Miltner, WHR (2006). Psychophysiological correlates of face processing in social phobia. Brain Research 1118, 130141.Google Scholar
Lehmann, D, Skrandies, W (1984). Spatial analysis of evoked potentials in man – a review. Progress in Neurobiology 23, 227250.CrossRefGoogle ScholarPubMed
Li, W, Zinbarg, RE, Boehm, SG, Paller, KA (2008). Neural and behavioral evidence for affective priming from unconsciously perceived emotional facial expressions and the influence of trait anxiety. Journal of Cognitive Neuroscience 20, 95107.CrossRefGoogle ScholarPubMed
Luu, P, Ferree, T (2000). Determination of the Geodesic Sensor Net's Average Electrode Positions and their 10–10 International Equivalents. Technical Note 1–15. Electrical Geodesics, Inc.: Eugene, OR.Google Scholar
MacLeod, C, Mathews, A, Tata, P (1986). Attentional bias in emotional disorders. Journal of Abnormal Psychology 95, 1520.Google Scholar
MacLeod, C, Rutherford, E, Campbell, L, Ebsworthy, G, Holker, L (2002). Selective attention and emotional vulnerability: assessing the causal basis of their association through the experimental manipulation of attentional bias. Journal of Abnormal Psychology 111, 107123.CrossRefGoogle ScholarPubMed
Mangun, GR, Hopfinger, JB, Heinze, HJ (1998). Integrating electrophysiology and neuroimaging in the study of human cognition. Behavior Research Methods, Instruments and Computers 30, 118130.Google Scholar
Mansell, W, Clark, DM, Ehlers, A, Chen, YP (1999). Social anxiety and attention away from emotional faces. Cognition and Emotion 13, 673690.Google Scholar
Martin, M, Williams, RM, Clark, DM (1991). Does anxiety lead to selective processing of threat-related information? Behaviour Research and Therapy 29, 147160.Google Scholar
Mathews, A, MacLeod, C (2002). Induced processing biases have causal effects on anxiety. Cognition and Emotion 16, 331354.Google Scholar
Mattick, RP, Clarke, JC (1998). Development and validation of measures of social phobia scrutiny fear and social interaction anxiety. Behaviour Research and Therapy 36, 455470.CrossRefGoogle ScholarPubMed
Mogg, K, Bradley, BP (2002). Selective orienting of attention to masked threat faces in social anxiety. Behaviour Research and Therapy 40, 14031414.Google Scholar
Mogg, K, Mathews, A, Weinman, J (1987). Memory bias in clinical anxiety. Journal of Abnormal Psychology 96, 9498.CrossRefGoogle ScholarPubMed
Mogg, K, Philippot, P, Bradley, BP (2004). Selective attention to angry faces in clinical social phobia. Journal of Abnormal Psychology 113, 160165.Google Scholar
Mulert, C, Jager, L, Schmitt, R, Bussfeld, P, Pogarell, O, Moller, HJ, Juckel, G, Hegerl, U (2004). Integration of fMRI and simultaneous EEG: towards a comprehensive understanding of localization and time-course of brain activity in target detection. NeuroImage 22, 8394.Google ScholarPubMed
Musa, C, Lepine, JP, Clark, DM, Mansell, W, Ehlers, A (2003). Selective attention in social phobia and the moderating effect of a concurrent depressive disorder. Behaviour Research and Therapy 41, 10431054.CrossRefGoogle ScholarPubMed
Pascual-Marqui, RD (1995). Reply to comments by Hämäläinen, Ilmoniemi and Nunez. In Source Localization: Continuing Discussion of the Inverse Problem. ISBET Newsletter No. 6 (ed. Skrandies, W.), pp. 1628.Google Scholar
Pascual-Marqui, RD, Lehmann, D, Koenig, T, Kochi, K, Merlo, MCG, Hell, D, Koukkou, M (1999). Low resolution brain electromagnetic tomography (LORETA) functional imaging in acute, neuroleptic-naive, first-episode, productive schizophrenia. Psychiatry Research: Neuroimaging 90, 169179.Google Scholar
Pascual-Marqui, RD, Michel, CM, Lehmann, D (1994). Low resolution electromagnetic tomography: a new method for localizing electrical activity in the brain. International Journal of Psychophysiology 18, 4965.Google ScholarPubMed
Pineles, SL, Mineka, S (2005). Attentional biases to internal and external sources of potential threat in social anxiety. Journal of Abnormal Psychology 114, 314318.CrossRefGoogle ScholarPubMed
Pizzagalli, DA, Greischar, LL, Davidson, RJ (2003). Spatio-temporal dynamics of brain mechanisms in aversive classical conditioning: high-density event-related potential and brain electrical tomography analyses. Neuropsychologia 41, 184194.CrossRefGoogle ScholarPubMed
Pizzagalli, DA, Lehmann, D, Hendrick, AM, Regard, M, Pascual-Marqui, RD, Davidson, RJ (2002). Affective judgments of faces modulate early activity (160 ms) within the fusiform gyri. NeuroImage 16, 663677.CrossRefGoogle ScholarPubMed
Pizzagalli, DA, Oakes, TR, Fox, AS, Chung, MK, Larson, CL, Abercrombie, HC, Schaefer, SM, Benca, RM, Davidson, RJ (2004). Functional but not structural subgenual prefrontal cortex abnormalities in melancholia. Molecular Psychiatry 9, 393405.Google Scholar
Pourtois, G, Dan, ES, Grandjean, D, Sander, D, Vuilleumier, P (2005). Enhanced extrastriate visual response to bandpass spatial frequency filtered fearful faces: time course and topographic evoked-potentials mapping. Human Brain Mapping 26, 6579.Google Scholar
Pourtois, G, Grandjean, D, Sander, D, Vuilleumier, P (2004). Electrophysiological correlates of rapid spatial orienting towards fearful faces. Cerebral Cortex 14, 619633.Google Scholar
Rapee, RM, Heimberg, RG (1997). A cognitive-behavioral model of anxiety in social phobia. Behaviour Research and Therapy 35, 741756.Google Scholar
Rossignol, M, Anselme, C, Vermeulen, N, Philippot, P, Campanella, S (2007). Categorical perception of anger and disgust facial expression is affected by non-clinical social anxiety: an ERP study. Brain Research 1132, 166176.Google Scholar
Santesso, DL, Meuret, AE, Hofmann, SG, Mueller, EM, Ratner, K, Roesch, E, Pizzagalli, DA (2008). Electrophysiological correlates of spatial orienting towards angry faces: a source localization study. Neuropsychologia 46, 13381348.Google Scholar
Spielberger, CD, Gorsuch, RL (1983). Manual for the State-Trait Anxiety Inventory (Form Y): Self-evaluation Questionnaire. Consulting Psychologists Press: Palo Alto, CA.Google Scholar
Sposari, JA, Rapee, RM (2007). Attentional bias toward facial stimuli under conditions of social threat in socially phobic and nonclinical participants. Cognitive Therapy and Research 31, 2337.Google Scholar
Stolarova, M, Keil, A, Moratti, S (2006). Modulation of the C1 visual event-related component by conditioned stimuli: evidence for sensory plasticity in early affective perception. Cerebral Cortex 16, 876887.Google Scholar
Straube, T, Kolassa, IT, Glauer, M, Mentzel, HJ, Miltner, WHR (2004). Effect of task conditions on brain responses to threatening faces in social phobics: an event-related functional magnetic resonance imaging study. Biological Psychiatry 56, 921930.Google Scholar
Streit, M, Dammers, J, Simsek-Kraues, S, Brinkmeyer, J, Wolwer, W, Ioannides, A (2003). Time course of regional brain activations during facial emotion recognition in humans. Neuroscience Letters 342, 101104.Google Scholar
Vassilopoulos, SP (2005). Social anxiety and the vigilance-avoidance pattern of attentional processing. Behavioural and Cognitive Psychotherapy 33, 1324.Google Scholar
Vitacco, D, Brandeis, D, Pascual-Marqui, RD, Martin, E (2002). Correspondence of event-related potential tomography and functional magnetic resonance imaging during language processing. Human Brain Mapping 17, 412.CrossRefGoogle ScholarPubMed
Vuilleumier, P, Pourtois, G (2007). Distributed and interactive brain mechanisms during emotion face perception: evidence from functional neuroimaging. Neuropsychologia 45, 174194.CrossRefGoogle ScholarPubMed
Williams, JMG, Watts, FN, MacLeod, C, Mathews, A (1988). Cognitive Psychology and the Emotional Disorders. Wiley: Chichester.Google Scholar
Zumsteg, D, Friedman, A, Wennberg, RA, Wieser, HG (2005). Source localization of mesial temporal interictal epileptiform discharges: correlation with intracranial foramen ovale electrode recordings. Clinical Neurophysiology 116, 28102818.CrossRefGoogle ScholarPubMed