Skip to main content Accessibility help
×
Home

Neural response during attentional control and emotion processing predicts improvement after cognitive behavioral therapy in generalized social anxiety disorder

  • H. Klumpp (a1), D. A. Fitzgerald (a1) (a2), M. Angstadt (a3), D. Post (a1) and K. L. Phan (a1) (a2)...

Abstract

Background

Individuals with generalized social anxiety disorder (gSAD) exhibit attentional bias to salient stimuli, which is reduced in patients whose symptoms improve after treatment, indicating that mechanisms of bias mediate treatment success. Therefore, pre-treatment activity in regions implicated in attentional control over socio-emotional signals (e.g. anterior cingulate cortex, dorsolateral prefrontal cortex) may predict response to cognitive behavioral therapy (CBT), evidence-based psychotherapy for gSAD.

Method

During functional magnetic resonance imaging, 21 participants with gSAD viewed images comprising a trio of geometric shapes (circles, rectangles or triangles) alongside a trio of faces (angry, fearful or happy) within the same field of view. Attentional control was evaluated with the instruction to ‘match shapes’, directing attention away from faces, which was contrasted with ‘match faces’, whereby attention was directed to emotional faces.

Results

Whole-brain voxel-wise analyses showed that symptom improvement was predicted by enhanced pre-treatment activity in the presence of emotional face distractors in the dorsal anterior cingulate cortex and dorsal medial prefrontal cortex. Additionally, CBT success was foretold by less activity in the amygdala and/or increased activity in the medial orbitofrontal gyrus during emotion processing.

Conclusions

CBT response was predicted by pre-treatment activity in prefrontal regions and the amygdala. The direction of activity suggests that individuals with intact attentional control in the presence of emotional distractors, regulatory capacity over emotional faces and/or less reactivity to such faces are more likely to benefit from CBT. Findings indicate that baseline neural activity in the context of attentional control and emotion processing may serve as a step towards delineating mechanisms by which CBT exerts its effects.

Copyright

Corresponding author

* Address for correspondence: H. Klumpp, Ph.D., Department of Psychiatry, University of Illinois at Chicago, 1747 W. Roosevelt Road, Chicago, IL 606 08 USA. (Email: hklumpp@psych.uic.edu)

References

Hide All
Abend, R, Bar-Haim, Y (2013). Threat-related attention bias in the early stages of cognitive–behavior therapy action for panic disorder. Biological Psychiatry 73, 10411042.
Adolphs, R, Tranel, D, Damasio, H, Damasio, A (1995). Fear and the human amygdala. Journal of Neuroscience 15, 58795891.
Alexander, GE, DeLong, MR, Strick, PL (1986). Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annual Review of Neuroscience 9, 357381.
Ball, TM, Stein, MB, Ramsawh, HJ, Campbell-Sills, L, Paulus, MP (2013). Single-subject anxiety treatment outcome prediction using functional neuroimaging. Neuropsychopharmacology. Published online 25 November 2013 . doi:10.1038/npp.2013.328.
Banich, MT, Mackiewicz, KL, Depue, BE, Whitmer, A, Miller, GA, Heller, W (2009). Cognitive control mechanisms, emotion & memory: a neural perspective with implications for psychopathology. Neuroscience and Biobehavioral Reviews 33, 613630.
Beck, AT, Steer, RA, Ball, R, Ranieri, WF (1996). Comparison of Beck Depression Inventories-IA and -II in psychiatric outpatients. Journal of Personality Assessment 67, 588597.
Blair, KS, Geraci, M, Smith, BW, Hollon, N, Devido, J, Otero, M, Blair, JR, Pine, DS (2012). Reduced dorsal anterior cingulate cortical activity during emotional regulation and top-down attentional control in generalized social phobia, generalized anxiety disorder, and comorbid generalized social phobia/generalized anxiety disorder. Biological Psychiatry 72, 476482.
Bögels, SM, Mansell, W (2004). Attention processes in the maintenance and treatment of social phobia: hypervigilance, avoidance and self-focused attention. Clinical Psychology Review 24, 827856.
Botvinick, MM, Braver, TS, Barch, DM, Carter, CS, Cohen, JD (2001). Conflict monitoring and cognitive control. Psychological Review 108, 624652.
Bryant, RA, Felmingham, K, Kemp, A, Das, P, Hughes, G, Peduto, A, Williams, L (2008). Amygdala and ventral anterior cingulate activation predicts treatment response to cognitive behaviour therapy for post-traumatic stress disorder. Psychological Medicine 38, 555561.
Bush, G, Luu, P, Posner, MI (2000). Cognitive and emotional influences in anterior cingulate cortex. Trends in Cognitive Sciences 4, 215222.
Busner, J, Targum, SD (2007). The Clinical Global Impressions Scale. Psychiatry 4, 2837.
Carter, CS, Braver, TS, Barch, DM, Botvinick, MM, Noll, D, Cohen, JD (1998). Anterior cingulate cortex, error detection, and the online monitoring of performance. Science 280, 747749.
Craig, ADB (2009). How do you feel – now? The anterior insula and human awareness. Nature Reviews. Neuroscience 10, 5970.
Cremers, HR, Demenescu, LR, Aleman, A, Renken, R, van Tol, M-J, van der Wee, NJA, Veltman, DJ, Roelofs, K (2010). Neuroticism modulates amygdala–prefrontal connectivity in response to negative emotional facial expressions. NeuroImage 49, 963970.
Critchley, HD (2009). Psychophysiology of neural, cognitive and affective integration: fMRI and autonomic indicants. International Journal of Psychophysiology 73, 8894.
Davidson, JRT, Foa, EB, Huppert, JD, Keefe, FJ, Franklin, ME, Compton, JS, Zhao, N, Connor, KM, Lynch, TR, Gadde, KM (2004). Fluoxetine, comprehensive cognitive behavioral therapy, and placebo in generalized social phobia. Archives of General Psychiatry 61, 10051013.
Davidson, RJ (2000). Affective style, psychopathology, and resilience: brain mechanisms and plasticity. American Psychologist 55, 11961214.
Davis, M, Whalen, PJ (2001). The amygdala: vigilance and emotion. Molecular Psychiatry 6, 1334.
Derryberry, D, Reed, MA (2002). Anxiety-related attentional biases and their regulation by attentional control. Journal of Abnormal Psychology 111, 225236.
Doehrmann, O, Ghosh, SS, Polli, FE, Reynolds, GO, Horn, F, Keshavan, A, Triantafyllou, C, Saygin, ZM, Whitfield-Gabrieli, S, Hofmann, SG, Pollack, M, Gabrieli, JD (2013). Predicting treatment response in social anxiety disorder from functional magnetic resonance imaging. JAMA Psychiatry 70, 8797.
Etkin, A, Egner, T, Kalisch, R (2011). Emotional processing in anterior cingulate and medial prefrontal cortex. Trends in Cognitive Sciences 15, 8593.
Etkin, A, Egner, T, Peraza, DM, Kandel, ER, Hirsch, J (2006). Resolving emotional conflict: a role for the rostral anterior cingulate cortex in modulating activity in the amygdala. Neuron 51, 871882.
Etkin, A, 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.
Eysenck, M (1992). Anxiety: The Cognitive Perspective. Lawrence Erlbaum Associates Ltd: Hove, UK.
First, MB, Spitzer, RL, Gibbon, M, Williams, JBW (1996). Structured Clinical Interview for DSM-IV Axis I Disorders, Clinician Version (SCID-CV). American Psychiatric Association: Washington, DC.
Foa, EB, Kozak, MJ (1986). Emotional processing of fear: exposure to corrective information. Psychological Bulletin 99, 2035.
Fox, E, Russo, R, Dutton, K (2002). Attentional bias for threat: evidence for delayed disengagement from emotional faces. Cognition and Emotion 16, 355379.
Freitas-Ferrari, MC, Hallak, JEC, Trzesniak, C, Filho, AS, Machado-de-Sousa, JP, Chagas, MHN, Nardi, AE, Crippa, JAS (2010). Neuroimaging in social anxiety disorder: a systematic review of the literature. Progress in Neuro-Psychopharmacology and Biological Psychiatry 34, 565580.
Gur, RC, Schroeder, L, Turner, T, McGrath, C, Chan, RM, Turetsky, BI, Alsop, D, Maldjian, J, Gur, RE (2002). Brain activation during facial emotion processing. NeuroImage 16, 651662.
Haxby, JV, Hoffman, EA, Gobbini, MI (2002). Human neural systems for face recognition and social communication. Biological Psychiatry 51, 5967.
Heimberg, RG, Horner, KJ, Juster, HR, Safren, SA, Brown, EJ, Schneier, FR, Liebowitz, MR (1999). Psychometric properties of the Liebowitz Social Anxiety Scale. Psychological Medicine 29, 199212.
Heimberg, RG, Liebowitz, MR, Hope, DA, Schneier, FR, Holt, CS, Welkowitz, LA, Juster, HR, Campeas, R, Bruch, MA, Cloitre, M, Fallon, B, Klein, DF (1998). Cognitive behavioral group therapy vs phenelzine therapy for social phobia: 12-week outcome. Archives of General Psychiatry 55, 11331141.
Hofmann, SG, Ellard, KK, Siegle, GJ (2012). Neurobiological correlates of cognitions in fear and anxiety: a cognitive–neurobiological information-processing model. Cognition and Emotion 26, 282299.
Hope, DA, Heimberg, RG, Turk, CL (2006). Managing Social Anxiety: A Cognitive–Behavioral Therapy Approach. Oxford University Press: New York.
Jones, CL, Ward, J, Critchley, HD (2010). The neuropsychological impact of insular cortex lesions. Journal of Neurology, Neurosurgery, and Psychiatry 81, 611618.
Kanske, P, Kotz, SA (2011). Emotion speeds up conflict resolution: a new role for the ventral anterior cingulate cortex? Cerebral Cortex 21, 911919.
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.
Klumpp, H, Angstadt, M, Phan, KL (2012 a). Insula reactivity and connectivity to anterior cingulate cortex when processing threat in generalized social anxiety disorder. Biological Psychology 89, 273276.
Klumpp, H, Angstadt, M, Phan, KL (2012 b). Shifting the focus of attention modulates amygdala and anterior cingulate cortex reactivity to emotional faces. Neuroscience Letters 514, 210213.
Klumpp, H, Fitzgerald, DA, Phan, KL (2013 b). Neural predictors and mechanisms of cognitive behavioral therapy on threat processing in social anxiety disorder. Progress in Neuro-Psychopharmacology and Biological Psychiatry 45, 8391.
Klumpp, H, Post, D, Angstadt, M, Fitzgerald, DA, Phan, KL (2013 a). Anterior cingulate cortex and insula response during indirect and direct processing of emotional faces in generalized social anxiety disorder. Biology of Mood and Anxiety Disorders 3, 7.
Lancaster, JL, Woldorff, MG, Parsons, LM, Liotti, M, Freitas, CS, Rainey, L, Kochunov, PV, Nickerson, D, Mikiten, SA, Fox, PT (2000). Automated Talairach Atlas labels for functional brain mapping. Human Brain Mapping 10, 120131.
Lasa, L, Ayuso-Mateos, J, Vázquez-Barquero, J, Dı́ez-Manrique, F, Dowrick, C (2000). The use of the Beck Depression Inventory to screen for depression in the general population: a preliminary analysis. Journal of Affective Disorders 57, 261265.
Lieberman, MD, Cunningham, WA (2009). Type I and type II error concerns in fMRI research: re-balancing the scale. Social Cognitive and Affective Neuroscience 4, 423428.
Liebowitz, MR (1987). Social phobia. Modern Problems of Pharmacopsychiatry 22, 141173.
Liu, X, Banich, MT, Jacobson, BL, Tanabe, JL (2006). Functional dissociation of attentional selection within PFC: response and non-response related aspects of attentional selection as ascertained by fMRI. Cerebral Cortex 16, 827834.
Lundh, LG, Öst, LG (2001). Attentional bias, self-consciousness and perfectionism in social phobia before and after cognitive–behaviour therapy. Scandinavian Journal of Behaviour Therapy 30, 416.
MacDonald, AW, Cohen, JD, Stenger, VA, Carter, CS (2000). Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. Science 288, 18351838.
Marks, I (1978). Behavioral psychotherapy of adult neurosis. In Handbook of Psychotherapy and Behavior Change: An Empirical Analysis, 2nd edn (ed. Garfield, S. L. and Bergin, A. E.), p. 493547. Wiley: New York.
Mathews, A (1990). Why worry? The cognitive function of anxiety. Behaviour Research and Therapy 28, 455468.
Mathews, A, MacLeod, C (2005). Cognitive vulnerability to emotional disorders. Annual Review of Clinical Psychology 1, 167195.
Mattia, JI, Heimberg, RG, Hope, DA (1993). The revised Stroop color-naming task in social phobics. Behaviour Research and Therapy 31, 305313.
McNally, RJ (1995). Automaticity and the anxiety disorders. Behaviour Research and Therapy 33, 747754.
McTeague, LM, Shumen, JR, Wieser, MJ, Lang, PJ, Keil, A (2011). Social vision: sustained perceptual enhancement of affective facial cues in social anxiety. NeuroImage 54, 16151624.
Mennin, DS, Heimberg, RG, Turk, CL, Fresco, DM (2002). Applying an emotion regulation framework to integrative approaches to generalized anxiety disorder. Clinical Psychology: Science and Practice 9, 8590.
Milad, MR, Wright, CI, Orr, SP, Pitman, RK, Quirk, GJ, Rauch, SL (2007). Recall of fear extinction in humans activates the ventromedial prefrontal cortex and hippocampus in concert. Biological Psychiatry 62, 446454.
Mogg, K, Bradley, B, Miles, F, Dixon, R (2004). Time course of attentional bias for threat scenes: testing the vigilance–avoidance hypothesis. Cognition and Emotion 18, 689700.
Mogg, K, McNamara, J, Powys, M, Rawlinson, H, Seiffer, A, Bradley, BP (2000). Selective attention to threat: a test of two cognitive models of anxiety. Cognition and Emotion 14, 375399.
Moriya, J, Tanno, Y (2008). Relationships between negative emotionality and attentional control in effortful control. Personality and Individual Differences 44, 13481355.
Norton, PJ, Hayes-Skelton, SA, Klenck, SC (2011). What happens in session does not stay in session: changes within exposures predict subsequent improvement and dropout. Journal of Anxiety Disorders 25, 654660.
Ochsner, KN, Silvers, JA, Buhle, JT (2012). Functional imaging studies of emotion regulation: a synthetic review and evolving model of the cognitive control of emotion. Annals of the New York Academy of Sciences 1251, E1E24.
Öhman, A, Soares, J (1994). ‘Unconscious anxiety’: phobic responses to masked stimuli. Journal of Abnormal Psychology 103, 231240.
Olson, IR, Plotzker, A, Ezzyat, Y (2007). The enigmatic temporal pole: a review of findings on social and emotional processing. Brain 130, 17181731.
Öngür, D, Price, JL (2000). The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cerebral Cortex 10, 206219.
Ormel, J, Bastiaansen, A, Riese, H, Bos, EH, Servaas, M, Ellenbogen, M, Rosmalen, JGM, Aleman, A (2013). The biological and psychological basis of neuroticism: current status and future directions. Neuroscience and Biobehavioral Reviews 37, 5972.
Phan, KL, Wager, T, Taylor, SF, Liberzon, I (2002). Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. NeuroImage 16, 331348.
Pishyar, R, Harris, LM, Menzies, RG (2008). Responsiveness of measures of attentional bias to clinical change in social phobia. Cognition and Emotion 22, 12091227.
Price, JL (1999). Prefrontal cortical networks related to visceral function and mood. Annals of the New York Academy of Sciences 877, 383396.
Price, JL, Drevets, WC (2009). Neurocircuitry of mood disorders. Neuropsychopharmacology 35, 192216.
Quirk, GJ, Garcia, R, González-Lima, F (2006). Prefrontal mechanisms in extinction of conditioned fear. Biological Psychiatry 60, 337343.
Rektor, I (2000). Parallel information processing in motor systems: intracerebral recordings of readiness potential and CNV in human subjects. Neural Plasticity 7, 6572.
Robinson, OJ, Charney, DR, Overstreet, C, Vytal, K, Grillon, C (2012). The adaptive threat bias in anxiety: amygdala–dorsomedial prefrontal cortex coupling and aversive amplification. NeuroImage 60, 523529.
Sabatinelli, D, Fortune, EE, Li, Q, Siddiqui, A, Krafft, C, Oliver, WT, Beck, S, Jeffries, J (2011). Emotional perception: meta-analyses of face and natural scene processing. NeuroImage 54, 25242533.
Schmidt, S, Mohr, A, Miltner, WHR, Straube, T (2010). Task-dependent neural correlates of the processing of verbal threat-related stimuli in social phobia. Biological Psychology 84, 304312.
Shin, LM, Davis, FC, Vanelzakker, MB, Dahlgren, MK, Dubois, SJ (2013). Neuroimaging predictors of treatment response in anxiety disorders. Biology of Mood and Anxiety Disorders 3, 15.
Siegle, GJ, Carter, CS, Thase, ME (2006). Use of fMRI to predict recovery from unipolar depression with cognitive behavior therapy. American Journal of Psychiatry 163, 735738.
Simon, SR, Meunier, M, Piettre, L, Berardi, AM, Segebarth, CM, Boussaoud, D (2002). Spatial attention and memory versus motor preparation: premotor cortex involvement as revealed by fMRI. Journal of Neurophysiology 88, 20472057.
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 15, 273289.
Wager, TD, Phan, KL, Liberzon, I, Taylor, SF (2003). Valence, gender, and lateralization of functional brain anatomy in emotion: a meta-analysis of findings from neuroimaging. NeuroImage 19, 513531.
Whalen, PJ, Bush, G, Shin, LM, Rauch, SL (2006). The emotional counting Stroop: a task for assessing emotional interference during brain imaging. Nature Protocols 1, 293296.
Williams, JMG, Watts, FN, MacLeod, CM, Mathews, A (1997). Cognitive Psychology and Emotional Disorders, 2nd edn. Wiley: New York.
Yiend, J, Mathews, A (2001). Anxiety and attention to threatening pictures. Quarterly Journal of Experimental Psychology. A: Human Experimental Psychology 54, 665681.

Keywords

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed