Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-03T00:21:25.431Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  21 March 2014

H. Klumpp ,
D. A. Fitzgerald ,
M. Angstadt ,
D. Post  and
K. L. Phan
H. Klumpp*
Affiliation:
Mood and Anxiety Disorders Research Program, Department of Psychiatry, University of Illinois at Chicago, Chicago, IL, USA
D. A. Fitzgerald
Affiliation:
Mood and Anxiety Disorders Research Program, Department of Psychiatry, University of Illinois at Chicago, Chicago, IL, USA Mental Health Service, Jesse Brown VA Medical Center, Chicago, IL, USA
M. Angstadt
Affiliation:
Department of Psychiatry, University of Michigan, Ann Arbor, MI, USA
D. Post
Affiliation:
Mood and Anxiety Disorders Research Program, Department of Psychiatry, University of Illinois at Chicago, Chicago, IL, USA
K. L. Phan
Affiliation:
Mood and Anxiety Disorders Research Program, Department of Psychiatry, University of Illinois at Chicago, Chicago, IL, USA Mental Health Service, Jesse Brown VA Medical Center, Chicago, IL, USA
*
* Address for correspondence: H. Klumpp, Ph.D., Department of Psychiatry, University of Illinois at Chicago, 1747 W. Roosevelt Road, Chicago, IL 606 08USA. (Email: [email protected])
Get access Rights & Permissions [Opens in a new window]

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.

Keywords

Attentional controlbrain imagingneural predictorspsychotherapysocial anxiety
Type
Original Articles
Information
Psychological Medicine , Volume 44 , Issue 14 , October 2014 , pp. 3109 - 3121
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

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, 1041–1042.Google Scholar
Adolphs, R, Tranel, D, Damasio, H, Damasio, A (1995). Fear and the human amygdala. Journal of Neuroscience 15, 5879–5891.Google Scholar
Alexander, GE, DeLong, MR, Strick, PL (1986). Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annual Review of Neuroscience 9, 357–381.CrossRefGoogle ScholarPubMed
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.Google Scholar
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, 613–630.Google Scholar
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, 588–597.Google Scholar
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, 476–482.Google Scholar
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, 827–856.Google Scholar
Botvinick, MM, Braver, TS, Barch, DM, Carter, CS, Cohen, JD (2001). Conflict monitoring and cognitive control. Psychological Review 108, 624–652.CrossRefGoogle ScholarPubMed
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, 555–561.CrossRefGoogle ScholarPubMed
Bush, G, Luu, P, Posner, MI (2000). Cognitive and emotional influences in anterior cingulate cortex. Trends in Cognitive Sciences 4, 215–222.Google Scholar
Busner, J, Targum, SD (2007). The Clinical Global Impressions Scale. Psychiatry 4, 28–37.Google Scholar
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, 747–749.Google Scholar
Craig, ADB (2009). How do you feel – now? The anterior insula and human awareness. Nature Reviews. Neuroscience 10, 59–70.Google Scholar
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, 963–970.Google Scholar
Critchley, HD (2009). Psychophysiology of neural, cognitive and affective integration: fMRI and autonomic indicants. International Journal of Psychophysiology 73, 88–94.Google Scholar
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, 1005–1013.Google Scholar
Davidson, RJ (2000). Affective style, psychopathology, and resilience: brain mechanisms and plasticity. American Psychologist 55, 1196–1214.CrossRefGoogle ScholarPubMed
Davis, M, Whalen, PJ (2001). The amygdala: vigilance and emotion. Molecular Psychiatry 6, 13–34.Google Scholar
Derryberry, D, Reed, MA (2002). Anxiety-related attentional biases and their regulation by attentional control. Journal of Abnormal Psychology 111, 225–236.CrossRefGoogle ScholarPubMed
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, 87–97.Google Scholar
Etkin, A, Egner, T, Kalisch, R (2011). Emotional processing in anterior cingulate and medial prefrontal cortex. Trends in Cognitive Sciences 15, 85–93.Google Scholar
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, 871–882.CrossRefGoogle ScholarPubMed
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, 1476–1488.Google Scholar
Eysenck, M (1992). Anxiety: The Cognitive Perspective. Lawrence Erlbaum Associates Ltd: Hove, UK.Google Scholar
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.Google Scholar
Foa, EB, Kozak, MJ (1986). Emotional processing of fear: exposure to corrective information. Psychological Bulletin 99, 20–35.CrossRefGoogle ScholarPubMed
Fox, E, Russo, R, Dutton, K (2002). Attentional bias for threat: evidence for delayed disengagement from emotional faces. Cognition and Emotion 16, 355–379.CrossRefGoogle ScholarPubMed
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, 565–580.Google Scholar
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, 651–662.Google Scholar
Haxby, JV, Hoffman, EA, Gobbini, MI (2002). Human neural systems for face recognition and social communication. Biological Psychiatry 51, 59–67.CrossRefGoogle ScholarPubMed
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, 199–212.Google Scholar
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, 1133–1141.Google Scholar
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, 282–299.Google Scholar
Hope, DA, Heimberg, RG, Turk, CL (2006). Managing Social Anxiety: A Cognitive–Behavioral Therapy Approach. Oxford University Press: New York.Google Scholar
Jones, CL, Ward, J, Critchley, HD (2010). The neuropsychological impact of insular cortex lesions. Journal of Neurology, Neurosurgery, and Psychiatry 81, 611–618.Google Scholar
Kanske, P, Kotz, SA (2011). Emotion speeds up conflict resolution: a new role for the ventral anterior cingulate cortex? Cerebral Cortex 21, 911–919.Google Scholar
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, 593–602.Google Scholar
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, 273–276.Google Scholar
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, 210–213.CrossRefGoogle ScholarPubMed
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, 83–91.Google Scholar
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.Google Scholar
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, 120–131.Google Scholar
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, 261–265.Google Scholar
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, 423–428.CrossRefGoogle ScholarPubMed
Liebowitz, MR (1987). Social phobia. Modern Problems of Pharmacopsychiatry 22, 141–173.Google Scholar
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, 827–834.Google Scholar
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, 4–16.Google Scholar
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, 1835–1838.Google Scholar
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. 493–547. Wiley: New York.Google Scholar
Mathews, A (1990). Why worry? The cognitive function of anxiety. Behaviour Research and Therapy 28, 455–468.Google Scholar
Mathews, A, MacLeod, C (2005). Cognitive vulnerability to emotional disorders. Annual Review of Clinical Psychology 1, 167–195.Google Scholar
Mattia, JI, Heimberg, RG, Hope, DA (1993). The revised Stroop color-naming task in social phobics. Behaviour Research and Therapy 31, 305–313.CrossRefGoogle ScholarPubMed
McNally, RJ (1995). Automaticity and the anxiety disorders. Behaviour Research and Therapy 33, 747–754.CrossRefGoogle ScholarPubMed
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, 1615–1624.Google Scholar
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, 85–90.Google Scholar
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, 446–454.Google Scholar
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, 689–700.Google Scholar
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, 375–399.CrossRefGoogle Scholar
Moriya, J, Tanno, Y (2008). Relationships between negative emotionality and attentional control in effortful control. Personality and Individual Differences 44, 1348–1355.Google Scholar
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, 654–660.Google Scholar
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, E1–E24.Google Scholar
Öhman, A, Soares, J (1994). ‘Unconscious anxiety’: phobic responses to masked stimuli. Journal of Abnormal Psychology 103, 231–240.Google Scholar
Olson, IR, Plotzker, A, Ezzyat, Y (2007). The enigmatic temporal pole: a review of findings on social and emotional processing. Brain 130, 1718–1731.Google Scholar
Öngür, D, Price, JL (2000). The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cerebral Cortex 10, 206–219.Google Scholar
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, 59–72.Google Scholar
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, 331–348.Google Scholar
Pishyar, R, Harris, LM, Menzies, RG (2008). Responsiveness of measures of attentional bias to clinical change in social phobia. Cognition and Emotion 22, 1209–1227.Google Scholar
Price, JL (1999). Prefrontal cortical networks related to visceral function and mood. Annals of the New York Academy of Sciences 877, 383–396.Google Scholar
Price, JL, Drevets, WC (2009). Neurocircuitry of mood disorders. Neuropsychopharmacology 35, 192–216.Google Scholar
Quirk, GJ, Garcia, R, González-Lima, F (2006). Prefrontal mechanisms in extinction of conditioned fear. Biological Psychiatry 60, 337–343.CrossRefGoogle ScholarPubMed
Rektor, I (2000). Parallel information processing in motor systems: intracerebral recordings of readiness potential and CNV in human subjects. Neural Plasticity 7, 65–72.Google Scholar
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, 523–529.Google Scholar
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, 2524–2533.Google Scholar
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, 304–312.Google Scholar
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.CrossRefGoogle ScholarPubMed
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, 735–738.Google Scholar
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, 2047–2057.Google Scholar
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, 273–289.Google Scholar
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, 513–531.Google Scholar
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, 293–296.Google Scholar
Williams, JMG, Watts, FN, MacLeod, CM, Mathews, A (1997). Cognitive Psychology and Emotional Disorders, 2nd edn. Wiley: New York.Google Scholar
Yiend, J, Mathews, A (2001). Anxiety and attention to threatening pictures. Quarterly Journal of Experimental Psychology. A: Human Experimental Psychology 54, 665–681.Google Scholar