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Differential patterns of activity and functional connectivity in emotion processing neural circuitry to angry and happy faces in adolescents with and without suicide attempt

Published online by Cambridge University Press:  09 January 2013

L. A. Pan ,
S. Hassel ,
A. M. Segreti ,
S. A. Nau ,
D. A. Brent  and
M. L. Phillips
L. A. Pan*
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
S. Hassel
Affiliation:
Department of Psychiatry and Hotchkiss Brain Institute, University of Calgary, School of Medicine, Calgary, AB, Canada
A. M. Segreti
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
S. A. Nau
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
D. A. Brent
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
M. L. Phillips
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA Department of Psychological Medicine, School of Medicine, Cardiff University, Cardiff, UK
*
*Address for correspondence: L. A. Pan, M.D., Assistant Professor of Psychiatry, Child and Adolescent Psychiatry, Loeffler Building, 121 Meyran Avenue, Room 304, Pittsburgh, PA 15213, USA. (Email: [email protected])
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Abstract

Background

Neural substrates of emotion dysregulation in adolescent suicide attempters remain unexamined.

Method

We used functional magnetic resonance imaging to measure neural activity to neutral, mild or intense (i.e. 0%, 50% or 100% intensity) emotion face morphs in two separate emotion-processing runs (angry and happy) in three adolescent groups: (1) history of suicide attempt and depression (ATT, n = 14); (2) history of depression alone (NAT, n = 15); and (3) healthy controls (HC, n = 15). Post-hoc analyses were conducted on interactions from 3 group × 3 condition (intensities) whole-brain analyses (p < 0.05, corrected) for each emotion run.

Results

To 50% intensity angry faces, ATT showed significantly greater activity than NAT in anterior cingulate gyral–dorsolateral prefrontal cortical attentional control circuitry, primary sensory and temporal cortices; and significantly greater activity than HC in the primary sensory cortex, while NAT had significantly lower activity than HC in the anterior cingulate gyrus and ventromedial prefrontal cortex. To neutral faces during the angry emotion-processing run, ATT had significantly lower activity than NAT in the fusiform gyrus. ATT also showed significantly lower activity than HC to 100% intensity happy faces in the primary sensory cortex, and to neutral faces in the happy run in the anterior cingulate and left medial frontal gyri (all p < 0.006,corrected). Psychophysiological interaction analyses revealed significantly reduced anterior cingulate gyral–insula functional connectivity to 50% intensity angry faces in ATT v. NAT or HC.

Conclusions

Elevated activity in attention control circuitry, and reduced anterior cingulate gyral–insula functional connectivity, to 50% intensity angry faces in ATT than other groups suggest that ATT may show inefficient recruitment of attentional control neural circuitry when regulating attention to mild intensity angry faces, which may represent a potential biological marker for suicide risk.

Keywords

Adolescentsanterior cingulatedepressionemotion processinginsulasuicide
Type
Original Articles
Information
Psychological Medicine , Volume 43 , Issue 10 , October 2013 , pp. 2129 - 2142
Copyright
Copyright © Cambridge University Press 2013 

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References

Anand, A, Li, Y, Wang, Y, Wu, J, Gao, S, Bukhari, L, Mathews, VP, Kalnin, A, Lowe, MJ (2005). Activity and connectivity of brain mood regulating circuit in depression: a functional magnetic resonance study. Biological Psychiatry 57, 1079–1088.CrossRefGoogle ScholarPubMed
Banich, MT (2009). Executive function: the search for an integrated account. Current Directions in Psychological Science 18, 89–94.CrossRefGoogle Scholar
Beck, AT, Schuyler, D, Herman, I (1974). Development of suicidal intent scales. In The Prediction of Suicide (ed. Beck, A. T., Resnick, H. L. P. and Lettieri, D. J.), pp. 45–56. Charles Press: Bowie, MD.Google Scholar
Beck, AT, Ward, CH, Mendelson, M, Mock, J, Erbaugh, J (1961). An inventory for measuring depression. Archives of General Psychiatry 4, 561–571.CrossRefGoogle ScholarPubMed
Birmaher, B, Khetarpal, S, Brent, D, Cully, M, Balach, L, Kaufman, J, Neer, SM (1997). The Screen for Child Anxiety Related Emotional Disorders (SCARED): scale construction and psychometric characteristics. Journal of the American Academy of Child and Adolescent Psychiatry 36, 545–553.CrossRefGoogle ScholarPubMed
Brent, DA, Baugher, M, Bridge, J, Chen, T, Chiappetta, L (1999). Age- and sex-related risk factors for adolescent suicide. Journal of the American Academy of Child and Adolescent Psychiatry 38, 1497–1505.CrossRefGoogle ScholarPubMed
Calder, AJ, Young, AW, Rowland, D, Perrett, DI (1997). Computer-enhanced emotion in facial expressions. Proceedings in Biological Science 264, 919–925.CrossRefGoogle ScholarPubMed
Craig, AD (2011). Significance of the insula for the evolution of human awareness of feelings from the body. Annals of the New York Academy of Sciences 1225, 72–82.CrossRefGoogle ScholarPubMed
Cullen, KR, Gee, DG, Klimes-Dougan, B, Gabbay, V, Hulvershorn, L, Mueller, BA, Camchong, J, Bell, CJ, Houri, A, Kumra, S, Lim, KO, Castellanos, FX, Milham, MP (2009). A preliminary study of functional connectivity in co-morbid adolescent depression. Neuroscience Letters 460, 227–231.CrossRefGoogle Scholar
Dickstein, DP, Finger, EC, Skup, M, Pine, DS, Blair, JR, Leibenluft, E (2010). Altered neural function in pediatric bipolar disorder during reversal learning. Bipolar Disorders 12, 707–719.CrossRefGoogle ScholarPubMed
Etkin, A, Egner, T, Kalisch, R (2011). Emotional processing in anterior cingulate and medial prefrontal cortex. Trends in Cognitive Science 15, 85–93.CrossRefGoogle ScholarPubMed
Friston, KJ, Buechel, C, Fink, GR, Morris, J, Rolls, E, Dolan, RJ (1997). Psychophysiological and modulatory interactions in neuroimaging. NeuroImage 6, 218–229.CrossRefGoogle ScholarPubMed
Giesecke, T, Gracely, RH, Williams, DA, Geisser, ME, Petzke, FW, Clauw, DJ (2005). The relationship between depression, clinical pain, and experimental pain in a chronic pain cohort. Arthritis and Rheumatism 52, 1577–1584.CrossRefGoogle Scholar
Gilbert, AR, Akkal, D, Almeida, JRC, Mataix-Cols, D, Kalas, C, Devlin, B, Birmaher, B, Phillips, ML (2005). Neural correlates of symptom dimensions in pediatric obsessive-compulsive disorder: a functional magnetic resonance imaging study. Journal of the American Academy of Child and Adolescent Psychiatry 48, 936–944.CrossRefGoogle Scholar
Grabenhorst, F, Rolls, ET (2011). Value, pleasure and choice in the ventral prefrontal cortex. Trends in Cognitive Science 15, 56–67.CrossRefGoogle ScholarPubMed
Hassel, S, Almeida, JR, Kerr, N, Nau, S, Ladouceur, CD, Fissell, K, Kupfer, DJ, Phillips, ML (2008). Elevated striatal and decreased dorsolateral prefrontal cortical activity in response to emotional stimuli in euthymic bipolar disorder: no associations with psychotropic medication load. Bipolar Disorders 10, 916–927.CrossRefGoogle ScholarPubMed
Haxby, JV, Hoffman, EA, Gobbini, MI (2000). The distributed human neural system for face perception. Trends in Cognitive Science 4, 223–233.CrossRefGoogle ScholarPubMed
Hulvershorn, LA, Cullen, K, Anand, A (2011). Toward dysfunctional connectivity: a review of neuroimaging findings in pediatric major depressive disorder. Brain Imaging and Behavior 5, 307–328.CrossRefGoogle ScholarPubMed
Jollant, F, Bellivier, F, Leboyer, M, Astruc, B, Torres, S, Verdier, R, Castelnau, D, Malafosse, A, Courtet, P (2005). Impaired decision making in suicide attempters. American Journal of Psychiatry 162, 304–310.CrossRefGoogle ScholarPubMed
Jollant, F, Lawrence, NS, Giampietro, V, Brammer, MJ, Fullana, MA, Drapier, D, Courtet, P, Phillips, ML (2008). Orbitofrontal cortex response to angry faces in men with histories of suicide attempts. American Journal of Psychiatry 165, 740–748.CrossRefGoogle ScholarPubMed
Kaller, CP, Heinze, K, Frenkel, A, Läppchen, CH, Unterrainer, JM, Weiller, C, Lange, R, Rahm, B (2011). Differential impact of continuous theta-burst stimulation over left and right DLPFC on planning. Human Brain Mapping. Published online: 14 October 2011. 10.1002/hbm.21423.Google ScholarPubMed
Kaufman, J, Birmaher, B, Brent, D, Rao, U, Flynn, C, Moreci, P, Williamson, D, Ryan, N (1997). Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL): initial reliability and validity data. Journal of the American Academy of Child and Adolescent Psychiatry 36, 980–988.CrossRefGoogle ScholarPubMed
Keilp, JG, Sackeim, HA, Brodsky, BS, Oquendo, MA, Malone, KM, Mann, JJ (2001). Neuropsychological dysfunction in depressed suicide attempters. American Journal of Psychiatry 158, 735–741.CrossRefGoogle ScholarPubMed
Killgore, WD, Yurgelun-Todd, DA (2006). Ventromedial prefrontal activity correlates with depressed mood in adolescent children. NeuroReport 17, 167–171.CrossRefGoogle ScholarPubMed
Kim, P, Thomas, LA, Rosen, BH, Moscicki, AM, Brotman, MA, Zarate, CA, Blair, RJ, Pine, DS, Liebenluft, E (2012). Differing amygdale responses to facial expressions in children and adults with bipolar disorder. American Journal of Psychiatry 169, 642–649.CrossRefGoogle Scholar
Ladouceur, CD, Farchione, T, Diwadkar, V, Pruitt, P, Radwan, J, Axelson, DA, Birmaher, B, Phillips, ML (2011). Differential patterns of abnormal activity and connectivity in the amygdala-prefrontal circuitry in bipolar-I and bipolar-NOS youth. Journal of the American Academy of Child and Adolescent Psychiatry 50, 1275–1289.CrossRefGoogle ScholarPubMed
Lau, JY, Goldman, D, Buzas, B, Hodgkinson, C, Leibenluft, E, Nelson, E, Sankin, L, Pine, DS, Ernst, M (2010). BDNF gene polymorphism (Val66Met) predicts amygdala and anterior hippocampus responses to emotional faces in anxious and depressed adolescents. NeuroImage 53, 952–961.CrossRefGoogle ScholarPubMed
Lawrence, NS, Williams, AM, Surguladze, S, Giampietro, V, Brammer, MJ, Andrew, C, Frangou, S, Ecker, C, Phillips, ML (2004). Subcortical and ventral prefrontal cortical neural responses to facial expressions distinguish patients with bipolar disorder and major depression. Biological Psychiatry 55, 578–587.CrossRefGoogle ScholarPubMed
Lubell, KM, Kegler, SR, Crosby, AE, Karch, D (2007). Suicide trends among youths and young adults aged 10–24 years – United States, 1990–2004. MMWR Morbidity and Mortality Weekly Report 56, 905–908.Google Scholar
Mann, JJ, Huang, YY, Underwood, MD, Kassir, SA, Oppenheim, S, Kelly, TM, Dwork, AJ, Arango, V (2000). A serotonin transporter gene promoter polymorphism (5-HTTLPR) and prefrontal cortical binding in major depression and suicide. Archives of General Psychiatry 57, 729–738.CrossRefGoogle ScholarPubMed
Monk, CS, McClure, EB, Nelson, EE, Zarahn, E, Bilder, RM, Leibenluft, E, Charney, DS, Ernst, M, Pine, DS (2003). Adolescent immaturity in attention-related brain engagement to emotional facial expressions. NeuroImage 20, 420–428.CrossRefGoogle ScholarPubMed
Monk, CS, Telzer, EH, Mogg, K, Bradley, BP, Mai, X, Louro, HM, Chen, G, McClure-Tone, EB, Ernst, M, Pine, DS (2008). Amygdala and ventrolateral prefrontal cortex activation to masked angry faces in children and adolescents with generalized anxiety disorder. Archives of General Psychiatry 65, 568–576.CrossRefGoogle ScholarPubMed
Nummenmaa, L, Hirvonen, J, Parkkola, R, Hietanen, JK (2008). Is emotional contagion special? An fMRI study on neural systems for affective and cognitive empathy. NeuroImage 43, 571–580.CrossRefGoogle Scholar
Oquendo, MA, Halberstam, B, Mann, JJ (2003 a). Risk factors for suicidal behavior: utility and limitations of research instruments. In Standardized Evaluation in Clinical Practice (ed. First, M. B.), pp. 103–130. American Psychiatric Press: Washington, DC.Google Scholar
Oquendo, MA, Placidi, GP, Malone, KM, Campbell, C, Keilp, J, Brodsky, B, Kegeles, LS, Cooper, TB, Parsey, RV, van Heertum, RL, Mann, JJ (2003 b). Positron emission tomography of regional brain metabolic responses to a serotonergic challenge and lethality of suicide attempts in major depression. Archives of General Psychiatry 60, 14–22.CrossRefGoogle ScholarPubMed
Pan, LA, Batezati-Alves, SC, Almeida, JR, Segreti, A, Akkal, D, Hassel, S, Lakdawala, S, Brent, DA, Phillips, ML (2011). Dissociable patterns of neural activity during response inhibition in depressed adolescents with and without suicidal behavior. Journal of the American Academy of Child and Adolescent Psychiatry 50, 602–611.CrossRefGoogle ScholarPubMed
Petersen, AC, Crockett, L, Richards, M, Boxer, A (1988). A self-report measure of pubertal status: reliability, validity, and initial norms. Journal of Youth and Adolescence 17, 117–133.CrossRefGoogle ScholarPubMed
Posner, K, Oquendo, MA, Gould, M, Stanley, B, Davies, M (2007). Columbia Classification Algorithm of Suicide Assessment (C-CASA): classification of suicidal events in the FDA's pediatric suicidal risk analysis of antidepressants. American Journal of Psychiatry 164, 1035–1043.CrossRefGoogle ScholarPubMed
Reynolds, WM (1987). Suicidal Ideation Questionnaire: Professional Manual. Psychological Assessment Resources: Odessa, FL.Google Scholar
Sugiura, M, Kawashima, R, Nakagawa, M, Okada, K, Sato, T, Goto, R, Sato, K, Ono, S, Schormann, T, Zilles, K, Fukuda, H (2000). Correlation between human personality and neural activity in cerebral cortex. NeuroImage 11, 541–546.CrossRefGoogle ScholarPubMed
Surguladze, S, Brammer, MJ, Keedwell, P, Giampietro, V, Young, AW, Travis, MJ, Williams, SC, Phillips, ML (2005). A differential pattern of neural response toward sad versus happy facial expressions in major depressive disorder. Biological Psychiatry 57, 201–209.CrossRefGoogle ScholarPubMed
Taylor, KS, Seminowicz, DA, Davis, KD (2009). Two systems of resting state connectivity between the insula and cingulate cortex. Human Brain Mapping 30, 2731–2745.CrossRefGoogle ScholarPubMed
Versace, A, Thompson, WK, Zhou, D, Almeida, JR, Hassel, S, Klein, CR, Kupfer, DJ, Phillips, ML (2010). Abnormal left and right amygdala–orbitofrontal cortical functional connectivity to emotional faces: state versus trait vulnerability markers of depression in bipolar disorder. Biological Psychiatry 67, 422–431.CrossRefGoogle ScholarPubMed
Wechsler, D (1999). Wechsler Abbreviated Scale of Intelligence. Harcourt Assessment: San Antonio, TX.Google Scholar
Young, AW, Perrett, D, Calder, A (2002). Facial Expressions of Emotions: Stimuli and Test (FEEST). Thames Valley Test Company: Bury St Edmunds.Google Scholar
Yurgelun-Todd, DA, Killgore, WD (2006). Fear-related activity in the prefrontal cortex increases with age during adolescence: a preliminary fMRI study. Neuroscience Letters 406, 194–199.CrossRefGoogle ScholarPubMed
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