Hostname: page-component-77c89778f8-n9wrp Total loading time: 0 Render date: 2024-07-17T14:11:31.102Z Has data issue: false hasContentIssue false
  • English
  • Français

Shifted inferior frontal laterality in women with major depressive disorder is related to emotion-processing deficits

Published online by Cambridge University Press:  08 January 2013

E. M. Briceño ,
S. L. Weisenbach ,
L. J. Rapport ,
K. E. Hazlett ,
L. A. Bieliauskas ,
B. D. Haase ,
M. T. Ransom ,
M. L. Brinkman ,
M. Peciña  and
D. E. Schteingart
...Show all authors
E. M. Briceño
Affiliation:
Department of Psychiatry, University of Michigan Medical Center, Ann Arbor, MI, USA Department of Psychology, Wayne State University, Detroit, MI, USA
S. L. Weisenbach
Affiliation:
Department of Psychiatry, University of Michigan Medical Center, Ann Arbor, MI, USA Ann Arbor VA Medical Center, Ann Arbor, MI, USA
L. J. Rapport
Affiliation:
Department of Psychology, Wayne State University, Detroit, MI, USA
K. E. Hazlett
Affiliation:
Department of Psychiatry, University of Michigan Medical Center, Ann Arbor, MI, USA
L. A. Bieliauskas
Affiliation:
Department of Psychiatry, University of Michigan Medical Center, Ann Arbor, MI, USA Ann Arbor VA Medical Center, Ann Arbor, MI, USA
B. D. Haase
Affiliation:
Department of Psychiatry, University of Michigan Medical Center, Ann Arbor, MI, USA
M. T. Ransom
Affiliation:
Department of Psychiatry, University of Michigan Medical Center, Ann Arbor, MI, USA
M. L. Brinkman
Affiliation:
Department of Psychiatry, University of Michigan Medical Center, Ann Arbor, MI, USA
M. Peciña
Affiliation:
Department of Psychiatry, University of Michigan Medical Center, Ann Arbor, MI, USA
D. E. Schteingart
Affiliation:
Department of Internal Medicine, University of Michigan Medical Center, Ann Arbor, MI, USA
M. N. Starkman
Affiliation:
Department of Psychiatry, University of Michigan Medical Center, Ann Arbor, MI, USA
B. Giordani
Affiliation:
Department of Psychiatry, University of Michigan Medical Center, Ann Arbor, MI, USA
R. C. Welsh
Affiliation:
Department of Psychiatry, University of Michigan Medical Center, Ann Arbor, MI, USA
D. C. Noll
Affiliation:
Department of Radiology, University of Michigan Medical Center, Ann Arbor, MI, USA Department of Biomedical Engineering, University of Michigan, Ann Arbor, MI, USA
J.-K. Zubieta
Affiliation:
Department of Psychiatry, University of Michigan Medical Center, Ann Arbor, MI, USA Department of Radiology, University of Michigan Medical Center, Ann Arbor, MI, USA
S. A. Langenecker*
Affiliation:
Department of Psychiatry, University of Michigan Medical Center, Ann Arbor, MI, USA
*
*Address for correspondence: S. A. Langenecker, Ph.D., Department of Psychiatry, University of Illinois at Chicago, 1601 West Taylor Street, Room 579, Chicago, IL 60126, USA. (Email: slangenenecker@psych.uic.edu)
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Facial emotion perception (FEP) is a critical human skill for successful social interaction, and a substantial body of literature suggests that explicit FEP is disrupted in major depressive disorder (MDD). Prior research suggests that weakness in FEP may be an important phenomenon underlying patterns of emotion-processing challenges in MDD and the disproportionate frequency of MDD in women.

Method

Women with (n = 24) and without (n = 22) MDD, equivalent in age and education, completed a FEP task during functional magnetic resonance imaging.

Results

The MDD group exhibited greater extents of frontal, parietal and subcortical activation compared with the control group during FEP. Activation in the inferior frontal gyrus (IFG) appeared shifted from a left >right pattern observed in healthy women to a bilateral pattern in MDD women. The ratio of left to right suprathreshold IFG voxels in healthy controls was nearly 3:1, whereas in the MDD group, there was a greater percentage of suprathreshold IFG voxels bilaterally, with no leftward bias. In MDD, relatively greater activation in right IFG compared with left IFG (ratio score) was present and predicted FEP accuracy (r = 0.56, p < 0.004), with an inverse relationship observed between FEP and subgenual cingulate activation (r = − 0.46, p = 0.02).

Conclusions

This study links, for the first time, disrupted IFG activation laterality and increased subgenual cingulate activation with deficient FEP in women with MDD, providing an avenue for imaging-to-assessment translational applications in MDD.

Keywords

Depressionemotionfaceslateralityidentificationneuroimagingwomen
Type
Original Articles
Information
Psychological Medicine , Volume 43 , Issue 7 , July 2013 , pp. 1433 - 1445
Copyright
Copyright © Cambridge University Press 2013 

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

Almeida, JRC, Versace, A, Hassel, S, Kupfer, DJ, Phillips, ML (2010). Elevated amygdala activity to sad facial expressions: a state marker of bipolar but not unipolar depression. Biological Psychiatry 67, 414–421.CrossRefGoogle Scholar
Almeida, JRC, Versace, A, Mechelli, A, Hassel, S, Quevedo, K, Kupfer, DJ, Phillips, ML (2009). Abnormal amygdala–prefrontal effective connectivity to happy faces differentiates bipolar from major depression, Biological Psychiatry 66, 451–459.CrossRefGoogle ScholarPubMed
Bouhuys, AL, Geerts, E, Gordijn, MCM (1999). Depressed patients' perceptions of facial emotions in depressed and remitted states are associated with relapse: a longitudinal study. Journal of Nervous and Mental Disease 187, 595–602.CrossRefGoogle ScholarPubMed
Brett, M, Anton, J-L, Valabreque, R, Poline, J-B (2002). Region of interest analysis using an SPM toolbox. Abstract presented at the 8th International Conference on Functional Mapping of the Human Brain, Sendai, Japan.Google Scholar
Canli, T, Cooney, RE, Goldin, P, Shah, M, Sivers, H, Thomason, ME, Whitfield-Gabrieli, S, Gabrieli, JDE, Gotlib, IH (2005). Amygdala reactivity to emotional faces predicts improvement in major depression. Neuroreport 16, 1267–1270.CrossRefGoogle ScholarPubMed
Costafreda, SG, Khanna, A, Mourao-Miranda, J, Fu, CHY (2009). Neural correlates of sad faces predict clinical remission to cognitive behavioural therapy in depression. Neuroreport 20, 637–641.CrossRefGoogle ScholarPubMed
Csukly, G, Czobor, P, Szily, E, Takacs, B, Simon, L (2009). Facial expression recognition in depressed subjects: the impact of intensity level and arousal dimension. Journal of Nervous and Mental Disease 197, 98–103.CrossRefGoogle ScholarPubMed
Dannlowski, U, Ohrmann, P, Bauer, J, Deckert, J, Hohoff, C, Kugel, H, Arolt, V, Heindel, W, Kersting, A, Baune, BT, Suslow, T (2008). 5-HTTLPR biases amygdala activity in response to masked facial expressions in major depression. Neuropsychopharmacology 33, 418–424.CrossRefGoogle ScholarPubMed
Dannlowski, U, Ohrmann, P, Bauer, J, Kugel, H, Arolt, V, Heindel, W, Kersting, A (2007). Amygdala reactivity to masked negative faces is associated with automatic judgmental bias in major depression: a 3 T fMR1 study. Journal of Psychiatry and Neuroscience 32, 423–429.Google Scholar
Davidson, RJ, Irwin, W, Anderle, MJ, Kalin, NH (2003). The neural substrates of affective processing in depressed patients treated with venlafaxine. American Journal of Psychiatry 160, 64–75.CrossRefGoogle ScholarPubMed
Delaveau, P, Jabourian, M, Lemogne, C, Guionnet, S, Bergouignan, L, Fossati, P (2011). Brain effects of antidepressants in major depression: a meta-analysis of emotional processing studies. Journal of Affective Disorders 130, 66–74.CrossRefGoogle ScholarPubMed
Demenescu, LR, Renken, R, Kortekaas, R, van Tol, MJ, Marsman, JBC, van Buchem, MA, van der Wee, NJA, Veltman, DJ, den Boer, A, Aleman, A (2011). Neural correlates of perception of emotional facial expressions in out-patients with mild-to-moderate depression and anxiety. A multicenter fMRI study. Psychological Medicine 41, 2253–2264.CrossRefGoogle ScholarPubMed
Egner, T, Etkin, A, Gale, S, Hirsch, J (2008). Dissociable neural systems resolve conflict from emotional versus nonemotional distracters. Cerebral Cortex 18, 1475–1484.CrossRefGoogle ScholarPubMed
Ekman, P, Friesen, WV (1976). Pictures of Facial Affect. Consulting Psychologists Press: Palo Alto, CA.Google Scholar
Elliott, R, Rubinsztein, JS, Sahakian, BJ, Dolan, RJ (2002). The neural basis of mood-congruent processing biases in depression. Archives of General Psychiatry 59, 597–604.CrossRefGoogle ScholarPubMed
Etkin, A, Egner, T, Kalisch, R (2011). Emotional processing in anterior cingulate and medial prefrontal cortex. Trends in Cognitive Sciences 15, 85–93.CrossRefGoogle ScholarPubMed
Eugene, F, Joormann, J, Cooney, RE, Atlas, LY, Gotlib, IH (2010). Neural correlates of inhibitory deficits in depression. Psychiatry Research – Neuroimaging 181, 30–35.CrossRefGoogle ScholarPubMed
First, MB, Spitzer, RL, Gibbon, M, Williams, JBW (1996). Structured Clinical Interview for DSM–IV Axis I Disorders. American Psychiatric Press: Washington, DC.Google Scholar
Frodl, T, Scheuerecker, J, Albrecht, J, Kleemann, AM, Muller-Schunk, S, Koutsouleris, N, Moller, HJ, Bruckmann, H, Wiesmann, M, Meisenzahl, E (2009). Neuronal correlates of emotional processing in patients with major depression. World Journal of Biological Psychiatry 10, 202–208.CrossRefGoogle ScholarPubMed
Fu, CHY, Williams, SCR, Cleare, AJ, Brammer, MJ, Walsh, ND, Kim, J, Andrew, CM, Pich, EM, Williams, PM, Reed, LJ, Mitterschiffthaler, MT, Suckling, J, Bullmore, ET (2004). Attenuation of the neural response to sad faces in major depression by antidepressant treatment – a prospective, event-related functional magnetic resonance imaging study. Archives of General Psychiatry 61, 877–889.CrossRefGoogle ScholarPubMed
Fusar-Poli, P, Placentino, A, Carletti, F, Landi, P, Allen, P, Surguladze, S, Benedetti, F, Abbamonte, M, Gasparotti, R, Barale, F, Perez, J, McGuire, P, Politi, P (2009). Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. Journal of Psychiatry and Neuroscience 34, 418–432.Google ScholarPubMed
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, 1731–1734.CrossRefGoogle ScholarPubMed
Grimm, S, Beck, J, Schuepbach, D, Hell, D, Boesiger, P, Bermpohl, F, Niehaus, L, Boeker, H, Northoff, G (2008). Imbalance between left and right dorsolateral prefrontal cortex in major depression is linked to negative emotional judgment: an fMRI study in severe major depressive disorder. Biological Psychiatry 63, 369–376.CrossRefGoogle ScholarPubMed
Gunning-Dixon, FM, Gur, RC, Perkins, AC, Schroeder, L, Turner, T, Turetsky, BI, Chan, RM, Loughead, JW, Alsop, DC, Maldjian, J, Gur, RE (2003). Age-related differences in brain activation during emotional face processing. Neurobiology of Aging 24, 285–295.CrossRefGoogle ScholarPubMed
Gur, RC, Erwin, RJ, Gur, RE, Zwil, AS, Heimberg, C, Kraemer, HC (1992). Facial emotion discrimination. 2. Behavioral findings in depression. Psychiatry Research 42, 241–251.CrossRefGoogle ScholarPubMed
Hamilton, M (1960). A rating scale for depression. Journal of Neurology, Neurosurgery, and Psychiatry 23, 56–62.CrossRefGoogle ScholarPubMed
Henriques, JB, Davidson, RJ (1991). Left frontal hypoactivation in depression. Journal of Abnormal Psychology 100, 535–545.CrossRefGoogle ScholarPubMed
Johnstone, T, van Reekum, CM, Urry, HL, Kalin, NH, Davidson, RJ (2007). Failure to regulate: counterproductive recruitment of top-down prefrontal-subcortical circuitry in major depression. Journal of Neuroscience 27, 8877–8884.CrossRefGoogle ScholarPubMed
Joormann, J, Gotlib, IH (2006). Is this happiness I see? Biases in the identification of emotional facial expressions in depression and social phobia. Journal of Abnormal Psychology 115, 705–714.CrossRefGoogle ScholarPubMed
Keedwell, P, Drapier, D, Surguladze, S, Giampietro, V, Brammer, M, Phillips, M (2009). Neural markers of symptomatic improvement during antidepressant therapy in severe depression: subgenual cingulate and visual cortical responses to sad, but not happy, facial stimuli are correlated with changes in symptom score. Journal of Psychopharmacology 23, 775–788.CrossRefGoogle Scholar
Keedwell, PA, Drapier, D, Surguladze, S, Giampietro, V, Brammer, M, Phillips, M (2010). Subgenual cingulate and visual cortex responses to sad faces predict clinical outcome during antidepressant treatment for depression. Journal of Affective Disorders 120, 120–125.CrossRefGoogle ScholarPubMed
Kohler, CG, Hoffman, LJ, Eastman, LB, Healey, K, Moberg, PJ (2011). Facial emotion perception in depression and bipolar disorder: a quantitative review. Psychiatry Research 188, 303–309.CrossRefGoogle ScholarPubMed
Langenecker, SA, Bieliauskas, LA, Rapport, LJ, Zubieta, JK, Wilde, EA, Berent, S (2005). Face emotion perception and executive functioning deficits in depression. Journal of Clinical and Experimental Neuropsychology 27, 320–333.CrossRefGoogle ScholarPubMed
Langenecker, SA, Caveney, AF, Giordani, B, Young, EA, Nielson, KA, Rapport, LJ, Biellauskas, LA, Mordhorst, MJ, Marcus, S, Yodkovik, N, Kerber, K, Berent, S, Zubieta, JK (2007 a). The sensitivity and psychometric properties of a brief computer-based cognitive screening battery in a depression clinic. Psychiatry Research 152, 143–154.CrossRefGoogle Scholar
Langenecker, SA, Kennedy, SE, Guidotti, LM, Briceno, EM, Own, LS, Hooven, T, Young, EA, Akil, H, Noll, DC, Zubieta, JK (2007 b). Frontal and limbic activation during inhibitory control predicts treatment response in major depressive disorder. Biological Psychiatry 62, 1272–1280.CrossRefGoogle ScholarPubMed
Langenecker, SA, Lee, HJ, Bieliauskas, LA (2009). Neuropsychology of depression and related mood disorders. In Neuropsychological Assessment of Neuropsychiatric Disorders (ed. Grant, I. and Adams, K. M.), pp. 523–559. Oxford University Press: New York.Google Scholar
Langenecker, SA, Weisenbach, SL, Giordani, B, Briceno, EM, Guidotti-Breting, LM, Schallmo, MP, Leon, HM, Noll, DC, Zubieta, JK, Schteingart, DE, Starkman, MN (2012). Impact of chronic hypercortisolemia on affective processing. Neuropharmacology 62, 217–225.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
Lee, BT, Seok, JH, Lee, BC, Cho, SW, Yoon, BJ, Lee, KU, Chae, JH, Choi, IG, Ham, BJ (2008). Neural correlates of affective processing in response to sad and angry facial stimuli in patients with major depressive disorder. Progress in Neuro-Psychopharmacology and Biological Psychiatry 32, 778–785.CrossRefGoogle ScholarPubMed
LeMoult, J, Joormann, J, Sherdell, L, Wright, Y, Gotlib, IH (2009). Identification of emotional facial expressions following recovery from depression. Journal of Abnormal Psychology 118, 828–833.CrossRefGoogle ScholarPubMed
Lozano, AM, Mayberg, HS, Giacobbe, P, Hamani, C, Craddock, RC, Kennedy, SH (2008). Subcallosal cingulate gyrus deep brain stimulation for treatment-resistant depression. Biological Psychiatry 64, 461–467.CrossRefGoogle ScholarPubMed
Mak, A, Hu, Z, Zhang, J, Xiao, Z, Lee, T (2009). Neural correlates of regulation of positive and negative emotions: an fMRI study. Neuroscience Letters 457, 101–106.CrossRefGoogle ScholarPubMed
Maldjian, JA, Laurienti, PJ, Kraft, RA, Burdette, JH (2003). An automated method for neuroanatomic and cytoarchitechtonic atlas-based interrogation of fMRI data sets. Neuroimage 19, 1233–1239.CrossRefGoogle Scholar
Mathersul, D, Williams, LM, Hopkinson, PJ, Kemp, AH (2008). Investigating models of affect: relationships among EEG alpha asymmetry, depression, and anxiety. Emotion 8, 560–572.CrossRefGoogle ScholarPubMed
Matsuo, K, Chen, S-HA, Tseng, W-YI (2012). AveLI: a robust lateralization index in functional magnetic resonance imaging using unbiased threshold-free computation. Journal of Neuroscience Methods 205, 119–129.CrossRefGoogle ScholarPubMed
Persad, SM, Polivy, J (1993). Differences between depressed and nondepressed individuals in the recognition of and response to facial emotional cues. Journal of Abnormal Psychology 102, 358–368.CrossRefGoogle ScholarPubMed
Phillips, ML, Drevets, WC, Rauch, SL, Lane, R (2003). Neurobiology of emotion perception I: the neural basis of normal emotion perception. Biological Psychiatry 54, 504–514.CrossRefGoogle ScholarPubMed
Phillips, ML, Ladouceur, CD, Drevets, WC (2008). A neural model of voluntary and automatic emotion regulation: implications for understanding the pathophysiology and neurodevelopment of bipolar disorder. Molecular Psychiatry 13, 833–857.CrossRefGoogle ScholarPubMed
Pizzagalli, DA (2010). Frontocingulate dysfunction in depression: toward biomarkers of treatment response. Neuropsychopharmacology 36, 183–206.CrossRefGoogle ScholarPubMed
Price, JL, Drevets, WC (2012). Neural circuits underlying the pathophysiology of mood disorders. Trends in Cognitive Sciences 16, 61–71.CrossRefGoogle ScholarPubMed
Rapport, LJ, Friedman, SL, Tzelepis, A, Van Voorhis, A (2002). Experienced emotion and affect recognition in adult attention-deficit hyperactivity disorder. Neuropsychology 16, 102–110.CrossRefGoogle ScholarPubMed
Rotenberg, VS (2004). The peculiarity of the right-hemisphere function in depression: solving the paradoxes. Progress in Neuro-Psychopharmacology and Biological Psychiatry 28, 1–13.CrossRefGoogle ScholarPubMed
Sheline, YI, Barch, DM, Donnelly, JM, Ollinger, JM, Snyder, AZ, Mintun, MA (2001). Increased amygdala response to masked emotional faces in depressed subjects resolves with antidepressant treatment: an fMRI study. Biological Psychiatry 50, 651–658.CrossRefGoogle ScholarPubMed
Surguladze, S, Brammer, MJ, Keedwell, P, Giampietro, V, Young, AW, Travis, MJ, Williams, SCR, 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
Tabachnick, BG, Fidell, LS (2007). Using Multivariate Statistics. Pearson Educational: Boston, MA.Google Scholar
Thomas, EJ, Elliott, R, McKie, S, Arnone, D, Downey, D, Juhasz, G, Deakin, JFW, Anderson, IM (2011). Interaction between a history of depression and rumination on neural response to emotional faces. Psychological Medicine 41, 1845–1855.CrossRefGoogle ScholarPubMed
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, 242–249.CrossRefGoogle ScholarPubMed
van Wingen, GA, van Eijndhoven, P, Tendolkar, I, Buitelaar, J, Verkes, RJ, Fernandez, G (2011). Neural basis of emotion recognition deficits in first-episode major depression. Psychological Medicine 41, 1397–1405.CrossRefGoogle ScholarPubMed
Watkins, PC, Vache, K, Verney, SP, Muller, S, Mathews, A (1996). Unconscious mood-congruent memory bias in depression. Journal of Abnormal Psychology 105, 34–41.CrossRefGoogle ScholarPubMed
Wright, SL, Langenecker, SA (2008). Differential risk for emotion processing difficulties by gender and age in major depresive disorder. In Women and Depression (ed. Hernandez, P. and Alonso, S.), pp. 1–33. Nova Science Publishers, Inc: New York.Google Scholar
Wright, SL, Langenecker, SA, Deldin, PJ, Rapport, LJ, Nielson, KA, Kade, AM, Own, LS, Akil, H, Young, EA, Zubieta, JK (2009). Gender-specific disruptions in emotion processing in younger adults with depression. Depression and Anxiety 26, 182–189.CrossRefGoogle ScholarPubMed
Supplementary material: File

Briceño Supplementary Material

Appendix

Download Briceño Supplementary Material(File)
File 496.6 KB