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Face processing in adolescents with positive and negative threat bias

  • C. M. Sylvester (a1), S. E. Petersen (a2) (a3), J. L. Luby (a1) and D. M. Barch (a1) (a3) (a4)

Abstract

Background

Individuals with anxiety disorders exhibit a ‘vigilance-avoidance’ pattern of attention to threatening stimuli when threatening and neutral stimuli are presented simultaneously, a phenomenon referred to as ‘threat bias’. Modifying threat bias through cognitive retraining during adolescence reduces symptoms of anxiety, and so elucidating neural mechanisms of threat bias during adolescence is of high importance. We explored neural mechanisms by testing whether threat bias in adolescents is associated with generalized or threat-specific differences in the neural processing of faces.

Method

Subjects were categorized into those with (n = 25) and without (n = 27) threat avoidance based on a dot-probe task at average age 12.9 years. Threat avoidance in this cohort has previously been shown to index threat bias. Brain response to individually presented angry and neutral faces was assessed in a separate session using functional magnetic resonance imaging.

Results

Adolescents with threat avoidance exhibited lower activity for both angry and neutral faces relative to controls in several regions in the occipital, parietal, and temporal lobes involved in early visual and facial processing. Results generalized to happy, sad, and fearful faces. Adolescents with a prior history of depression and/or an anxiety disorder had lower activity for all faces in these same regions. A subset of results replicated in an independent dataset.

Conclusions

Threat bias is associated with generalized, rather than threat-specific, differences in the neural processing of faces in adolescents. Findings may aid in the development of novel treatments for anxiety disorders that use attention training to modify threat bias.

Copyright

Corresponding author

*Address for correspondence: C. M. Sylvester, M.D., Ph.D., Department of Psychiatry, Washington University School of Medicine, 4444 Forest Park Avenue, Campus Box 8511, St Louis, MO, 63108, USA. (Email: sylvestc@psychiatry.wustl.edu)

References

Hide All
Angold, A, Costello, EJ (2000). The Child and Adolescent Psychiatric Assessment (CAPA). Journal of the American Academy of Child and Adolescent Psychiatry 39, 3948.
Bar-Haim, Y (2010). Research review: attention bias modification (ABM): a novel treatment for anxiety disorders. Journal of Child Psychology and Psychiatry 51, 859870.
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.
Barch, DM, Gaffrey, MS, Botteron, KN, Belden, AC, Luby, JL (2012). Functional brain activation to emotionally valenced faces in school-aged children with a history of preschool-onset major depression. Biological Psychiatry 72, 10351042.
Barlow, DH (2002). Anxiety and Its Disorders. Guilford Press: New York.
Bird, HR, Gould, MS, Staghezza, B (1992). Aggregating data from multiple informants in child psychiatry epidemiological research. Journal of the American Academy of Child and Adolescent Psychiatry 31, 7885.
Britton, JC, Bar-Haim, Y, Carver, FW, Holroyd, T, Norcross, MA, Detloff, A, Leibenluft, E, Ernst, M, Pine, DS (2012). Isolating neural components of threat bias in pediatric anxiety. Journal of Child Psychology and Psychiatry 53, 678686.
Buckner, RL, Head, D, Parker, J, Fotenos, AF, Marcus, D, Morris, JC, Snyder, AZ (2004). A unified approach for morphometric and functional data analysis in young, old, and demented adults using automated atlas-based head size normalization: reliability and validation against manual measurement of total intracranial volume. Neuroimage 23, 724738.
Cisler, JM, Koster, EH (2010). Mechanisms of attentional biases towards threat in anxiety disorders: an integrative review. Clinical Psychology Review 30, 203216.
Corbetta, M, Shulman, GL (2002). Control of goal-directed and stimulus-driven attention in the brain. Nature Reviews Neuroscience 3, 201215.
Desimone, R (1998). Visual attention mediated by biased competition in extrastriate visual cortex. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 353, 12451255.
Desimone, R, Duncan, J (1995). Neural mechanisms of selective visual attention. Annual Review of Neuroscience 18, 193222.
Egger, HL, Ascher, B, Angold, A (2003). The Preschool Age Psychiatric Assessment: Version 1.4. Duke University Medical Center: Durham, NC.
Eldar, S, Apter, A, Lotan, D, Edgar, KP, Naim, R, Fox, NA, Pine, DS, Bar-Haim, Y (2012). Attention bias modification treatment for pediatric anxiety disorders: a randomized controlled trial. American Journal of Psychiatry 169, 213220.
Eldar, S, Ricon, T, Bar-Haim, Y (2008). Plasticity in attention: implications for stress response in children. Behaviour Research and Therapy 46, 450461.
Fani, N, Jovanovic, T, Ely, TD, Bradley, B, Gutman, D, Tone, EB, Ressler, KJ (2012). Neural correlates of attention bias to threat in post-traumatic stress disorder. Biological Psychology 90, 134142.
Gotlib, IH, Sivers, H, Gabrieli, JD, Whitfield-Gabrieli, S, Goldin, P, Minor, KL, Canli, T (2005). Subgenual anterior cingulate activation to valenced emotional stimuli in major depression. Neuroreport 16, 17311734.
Hsieh, PJ, Colas, JT, Kanwisher, NG (2012). Pre-stimulus pattern of activity in the fusiform face area predicts face percepts during binocular rivalry. Neuropsychologia 50, 522529.
Joormann, J, Talbot, L, Gotlib, IH (2007). Biased processing of emotional information in girls at risk for depression. Journal of Abnormal Psychology 116, 135143.
Kanwisher, N, Yovel, G (2006). The fusiform face area: a cortical region specialized for the perception of faces. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 361, 21092128.
Kastner, S, Ungerleider, LG (2001). The neural basis of biased competition in human visual cortex. Neuropsychologia 39, 12631276.
Kessler, RC, Berglund, P, Demler, O, Jin, R, Merikangas, KR, Walters, EE (2005). Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Archives of General Psychiatry 62, 593602.
Klein, R (2000). Inhibition of return. Trends in Cognitive Sciences 4, 138147.
Koster, EH, Baert, S, Bockstaele, M, De Raedt, R (2010). Attentional retraining procedures: manipulating early or late components of attentional bias? Emotion (Washington, DC) 10, 230236.
Koster, EH, Crombez, G, Verschuere, B, Van Damme, S, Wiersema, JR (2006). Components of attentional bias to threat in high trait anxiety: facilitated engagement, impaired disengagement, and attentional avoidance. Behaviour Research and Therapy 44, 17571771.
Koster, EH, Verschuere, B, Crombez, G, Van Damme, S (2005). Time-course of attention for threatening pictures in high and low trait anxiety. Behaviour Research and Therapy 43, 10871098.
Luby, JL, Belden, AC, Pautsch, J, Si, X, Spitznagel, E (2009 a). The clinical significance of preschool depression: impairment in functioning and clinical markers of the disorder. Journal of Affective Disorders 112, 111119.
Luby, JL, Si, X, Belden, AC, Tandon, M, Spitznagel, E (2009 b). Preschool depression: homotypic continuity and course over 24 months. Archives of General Psychiatry 66, 897905.
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.
Merikangas, KR, He, J-P, Burstein, M, Swanson, SA, Avenevoli, S, Cui, L, Benjet, C, Georgiades, K, Swendsen, J (2010). Lifetime prevalence of mental disorders in U.S. adolescents: results from the National Comorbidity Survey Replication – Adolescent Supplement (NCS-A). Journal of the American Academy of Child and Adolescent Psychiatry 49, 980989.
Mogg, K, Bradley, BP, de Bono, J, Painter, M (1997). Time course of attentional bias for threat information in non-clinical anxiety. Behaviour Research and Therapy 35, 297303.
Mogg, K, Bradley, BP, Miles, F, Dixon, R (2004). Time course of attentional bias for threat scenes: testing the vigilance-avoidance hypothesis. Cognition & Emotion 18, 689700.
Ojemann, JG, Akbudak, E, Snyder, AZ, McKinstry, RC, Raichle, ME, Conturo, TE (1997). Anatomic localization and quantitative analysis of gradient refocused echo-planar fMRI susceptibility artifacts. Neuroimage 6, 156167.
Price, RB, Kuckertz, JM, Siegle, GJ, Ladouceur, CD, Silk, JS, Ryan, ND, Dahl, RE, Amir, N (2015). Empirical recommendations for improving the stability of the dot-probe task in clinical research. Psychological Assessment 27, 365376.
Price, RB, Rosen, D, Siegle, GJ, Ladouceur, CD, Tang, K, Allen, KB, Ryan, ND, Dahl, RE, Forbes, EE, Silk, JS (2016). From anxious youth to depressed adolescents: prospective prediction of 2-year depression symptoms via attentional bias measures. Journal of Abnormal Psychology 125, 267278.
Price, RB, Siegle, GJ, Silk, JS, Ladouceur, CD, McFarland, A, Dahl, RE, Ryan, ND (2014). Looking under the hood of the dot-probe task: an fMRI study in anxious youth. Depression and Anxiety 31, 178187.
Shechner, T, Britton, JC, Pérez-Edgar, K, Bar-Haim, Y, Ernst, M, Fox, NA, Leibenluft, E, Pine, DS (2012). Attention biases, anxiety, and development: toward or away from threats or rewards? Depression and Anxiety 29, 282294.
Shechner, T, Rimon-Chakir, A, Britton, JC, Lotan, D, Apter, A, Bliese, PD, Pine, DS, Bar-Haim, Y (2014). Attention bias modification treatment augmenting effects on cognitive behavioral therapy in children with anxiety: randomized controlled trial. Journal of the American Academy of Child and Adolescent Psychiatry 53, 6171.
Siegel, JS, Power, JD, Dubis, JW, Vogel, AC, Church, JA, Schlaggar, BL, Petersen, SE (2014). Statistical improvements in functional magnetic resonance imaging analyses produced by censoring high-motion data points. Human Brain Mapping 35, 19811996.
Sylvester, CM, Barch, DM, Corbetta, M, Power, JD, Schlaggar, BL, Luby, JL (2013). Resting state functional connectivity of the ventral attention network in children with a history of depression or anxiety. Journal of the American Academy of Child and Adolescent Psychiatry 52, 13261336.
Sylvester, CM, Hudziak, JJ, Gaffrey, MS, Barch, DM, Luby, JL (2016). Stimulus-driven attention, threat bias, and sad bias in youth with a history of an anxiety disorder or depression. Journal of Abnormal Child Psychology 44, 219231.
Sylvester, CM, Shulman, GL, Jack, AI, Corbetta, M (2007). Asymmetry of anticipatory activity in visual cortex predicts the locus of attention and perception. Journal of Neuroscience 27, 1442414433.
Talairach, J, Tournoux, P (1988). Co-planar Stereotaxic Atlas of the Human Brain. Thieme Medical: New York.
Teachman, BA, Joormann, J, Steinman, SA, Gotlib, IH (2012). Automaticity in anxiety disorders and major depressive disorder. Clinical Psychology Review 32, 575603.
Tottenham, N, Tanaka, JW, Leon, AC, McCarry, T, Nurse, M, Hare, TA, Marcus, DJ, Westerlund, A, Casey, BJ, Nelson, C (2009). The NimStim set of facial expressions: judgments from untrained research participants. Psychiatry Research 168, 242249.
Waechter, S, Nelson, AL, Wright, C, Hyatt, A, Oakman, J (2014). Measuring attentional bias to threat: reliability of dot probe and eye movement indices. Cognitive Therapy and Research 38, 313333.
Williams, JMG, Watts, FN, MacLeod, C, Mathews, A (1997). Cognitive Psychology and Emotional Disorders. Wiley: Chichester.

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