Facial emotion processing in major depression: A systematic review of neuroimaging findings

Biology of Mood and Anxiety Disorders

Volumn 1, Issue 1, 2011, Pages 1-10

  Stuhrmann, Anja ^a   Suslow, Thomas ^a,b   Dannlowski, Udo ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

Amygdala; Anterior cingulate; Depression; Emotion; Facial emotion processing; fMRI; Functional connectivity; Neuroimaging; Orbitofrontal cortex

Indexed keywords

EID: 84924658166     PISSN: None     EISSN: 20455380     Source Type: Journal    
DOI: 10.1186/2045-5380-1-10     Document Type: Article

References (104)

1. World Health Organization: Mental Health: New Understanding, New Hope Geneva, Switzerland: WHO; 2001.
2. Leppänen JM: Emotional information processing in mood disorders: a review of behavioral and neuroimaging findings. Curr Opin Psychiatry 2006, 19:34-39.
3. Mathews A, MacLeod C: Cognitive vulnerability to emotional disorders. Annu Rev Clin Psychol 2005, 1:167-195.
4. Ridout N, Astell AJ, Reid IC, Glen T, O'Carroll RE: Memory bias for emotional facial expressions in major depression. Cognition Emotion 2003, 17:101-122.
5. Williams JMG, Watts FN, MacLeod C, Mathews A: Cognitive psychology and emotional disorders. 2 edition. Chichester, UK: John Wiley & Sons; 1997.
6. Bourke C, Douglas K, Porter R: Processing of facial emotion expression in major depression: a review. Aust N Z J Psychiatry 2010, 44:681-96.
7. Elliott R, Zahn R, Deakin JFW, Anderson IM: Affective cognition and its disruption in mood disorders. Neuropsychopharmacol 2010, 36:153-182.
8. Gotlib IH, Krasnoperova E, Yue DN, Joormann J: Attentional biases for negative interpersonal stimuli in clinical depression. J Abnorm Psychol 2004, 113:127-135.
9. Leyman L, De Raedt R, Schacht R, Koster EHW: Attentional biases for angry faces in unipolar depression. Psychol Med 2007, 37:393-402.
10. Suslow T, Dannlowski U, Lalee-Mentzel J, Donges U-S, Arolt V: Spatial processing of facial emotion in patients with unipolar depression: a longitudinal study. J Affect Disord 2004, 83:59-63.
11. Joormann J, Gotlib IH: Selective attention to emotional faces following recovery from depression. J Abnorm Psychol 2007, 116:80-85.
12. Bouhuys AL, Geerts E, Gordijn M: Depressed patients' perceptions of facial emotions in depressed and remitted states are associated with relapse: a longitudinal study. J Nerv Ment Dis 1999, 187:595-692.
13. Dannlowski U, Kersting A, Donges U-S, Lalee-Mentzel J, Arolt V, Suslow T: Masked facial affect priming is associated with therapy response in clinical depression. Eur Arch Psychiatry Clin Neurosci 2006, 256:215-221.
14. Dannlowski U, Kersting A, Lalee-Mentzel J, Donges U-S, Arolt V, Suslow T: Subliminal affective priming in clinical depression and comorbid anxiety: a longitudinal investigation. Psychiatry Res 2006, 143:63-75.
15. Phillips M: Neurobiology of emotion perception I: the neural basis of normal emotion perception. Biol Psychiatry 2003, 54:504-514.
16. Blair RJR: Facial expressions, their communicatory functions and neurocognitive substrates. Philos Trans R Soc Lond B Biol Sci 2003, 358:561-572.
17. Suslow T, Dannlowski U: Detection of facial emotion in depression. In Mood State and Health. Edited by: Clark AV. Hauppauge, NY: Nova Biomedical Books; 2005:1-32.
18. 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: Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. J Psychiatr Neurosci 2009, 34:418-432.
19. Haxby J, Gobbini MI: The perception of emotion and social cues in faces. Neuropsychologia 2007, 45:1.
20. Haxby J, Hoffman E, Gobbini MI: The distributed human neural system for face perception. Trends Cogn Sci 2000, 4:223-233.
21. Posamentier MT, Abdi H: Processing faces and facial expressions. Neuropsychol Rev 2003, 13:113-143.
22. Haxby J, Hoffman E, Gobbini MI: Human neural systems for face recognition and social communication. Biol Psychiatry 2002, 51:59-67.
23. Mayberg HS: Limbic-cortical dysregulation: a proposed model of depression. J Neuropsychiatry Clin Neurosci 1997, 9:471-481.
24. Phillips ML, Ladouceur CD, Drevets WC: A neural model of voluntary and automatic emotion regulation: implications for understanding the pathophysiology and neurodevelopment of bipolar disorder. Mol Psychiatry 2008, 13:829, 833-857.
25. Phillips ML, Drevets WC, Rauch SL, Lane R: Neurobiology of emotion perception II: Implications for major psychiatric disorders. Biol Psychiatry 2003, 54:515-528.
26. Mayberg HS: Defining the neural circuitry of depression: toward a new nosology with therapeutic implications. Biol Psychiatry 2007, 61:729-730.
27. Frodl T, Scheuerecker J, Schoepf V, Linn J, Koutsouleris N, Bokde A, Hampel H, Möller H-J, Brückmann H, Wiesmann M, Meisenzahl E: Different effects of mirtazapine and venlafaxine on brain activation: an open randomized controlled fMRI study. J Clin Psychiatry 2011, 72:448-457.
28. Matthews SC, Strigo IA, Simmons AN, Yang TT, Paulus MP: Decreased functional coupling of the amygdala and supragenual cingulate is related to increased depression in unmedicated individuals with current major depressive disorder. J Affect Disord 2008, 111:13-20.
29. Victor TA, Furey ML, Fromm S, Ohman A, Drevets WC: Relationship between amygdala responses to masked faces and mood state and treatment in major depressive disorder. Arch Gen Psychiatry 2010, 67:1128-1138.
30. Suslow T, Konrad C, Kugel H, Rumstaedt D, Zwitserlood P, Schöning S, Ohrmann P, Bauer J, Pyka M, Kersting A, Arolt V, Heindel W, Dannlowski U: Automatic mood-congruent amygdala responses to masked facial expressions in major depression. Biol Psychiatry 2010, 67:155-160.
31. Surguladze S, Brammer M, Keedwell P, Giampietro V, Young AW, Travis MJ, Williams SCR, Phillips ML: A differential pattern of neural response toward sad versus happy facial expressions in major depressive disorder. Biol Psychiatry 2005, 57:201-209.
32. Fu CHY, Williams SCR, Cleare AJ, Brammer M, Walsh ND, Kim J, Andrew CM, Pich EM, Williams PM, Reed LJ, Mitterschiffthaler MT, Suckling J, Bullmore ET: Attenuation of the neural response to sad faces in major depression by antidepressant treatment: a prospective, event-related functional magnetic resonance imaging study. Arch Gen Psychiatry 2004, 61:877-889.
33. Fu CHY, Williams SCR, Cleare AJ, Scott J, Mitterschifthaler MT, Walsh ND, Donaldson C, Suckling J, Andrew CM, Steiner H, Murray RM: Neural responses to sad facial expressions in major depression following cognitive behavioral therapy. Biol Psychiatry 2008, 64:505-512.
34. Sheline YI, Barch DM, Donnelly JM, Ollinger JM, Snyder AZ, Mintun MA: Increased amygdala response to masked emotional faces in depressed subjects resolves with antidepressant treatment: an fMRI study. Biol Psychiatry 2001, 50:651-658.
35. Peluso MAM, Glahn DC, Matsuo K, Monkul ES, Najt P, Zamarripa F, Li J, Lancaster JL, Fox PT, Gao J-H, Soares JC: Amygdala hyperactivation in untreated depressed individuals. Psychiatry Res 2009, 173:158-161.
36. Zhong M, Wang X, Xiao J, Yi J, Zhu X, Liao J, Wang W, Yao S: Amygdala hyperactivation and prefrontal hypoactivation in subjects with cognitive vulnerability to depression. Biol Psychiatry 2011, 88:233-242.
37. Lawrence NS, Williams AM, Surguladze S, Giampietr V, Brammer M, Andrew CM, Frangou S, Ecker C, Phillips ML: Subcortical and ventral prefrontal cortical neural responses to facial expressions distinguish patients with bipolar disorder and major depression. Biol Psychiatry 2004, 55:578-87.
38. Lee B-T, Seok J-H, Lee B-C, Cho SW, Yoon B-J, Lee K-U, Chae J-H, Choi I-G, Ham B-J: Neural correlates of affective processing in response to sad and angry facial stimuli in patients with major depressive disorder. Prog Neuropsychopharmacol Biol Psychiatry 2008, 32:778-785.
39. Surguladze S, El-Hage W, Dalgleish T, Radua J, Gohier B, Phillips ML: Depression is associated with increased sensitivity to signals of disgust: a functional magnetic resonance imaging study. J Psychiatr Res 2010, 44:894-902.
40. Townsend JD, Eberhart NK, Bookheimer SY, Eisenberger NI, Foland-Ross LC, Cook IA, Sugar CA, Altshuler LL: fMRI activation in the amygdala and the orbitofrontal cortex in unmedicated subjects with major depressive disorder. Psychiatry Res 2010, 183:209-217.
41. Scheuerecker J, Meisenzahl EM, Koutsouleris N, Roesner M, Schöpf V, Linn J, Wiesmann M, Brückmann H, Möller HJ, Frodl T: Orbitofrontal volume reductions during emotion recognition in patients with major depression. J Psychiatr Neurosci 2010, 35:311-320.
42. Keedwell P, Andrew CM, Williams SCR, Brammer M, Phillips ML: A double dissociation of ventromedial prefrontal cortical responses to sad and happy stimuli in depressed and healthy individuals. Biol Psychiatry 2005, 58:495-503.
43. Frodl T, Scheuerecker J, Albrecht J, Kleemann AM, Müller-Schunk S, Koutsouleris N, Möller HJ, Brückmann H, Wiesmann M, Meisenzahl EM: Neuronal correlates of emotional processing in patients with major depression. World J Biol Psychiatry 2009, 10:202-208.
44. Mayberg HS, Lozano AM, Voon V, McNeely HE, Seminowicz DA, Hamani C, Schwalb JM, Kennedy S: Deep brain stimulation for treatment-resistant depression. Neuron 2005, 45:651-660.
45. Gotlib IH, Sivers H, Gabrieli JDE, Whitfield-Gabrieli S, Goldin P, Minor KL, Canli T: Subgenual anterior cingulate activation to valenced emotional stimuli in major depression. Neuroreport 2005, 16:1731-1734.
46. Friston KJ: Functional and effective connectivity in neuroimaging: a synthesis. Hum Brain Mapp 1994, 2:56-78.
47. Almeida JRC, Versace A, Mechelli A, Hassel S, Quevedo K, Kupfer DJ, Phillips ML: Abnormal amygdala-prefrontal effective connectivity to happy faces differentiates bipolar from major depression. Biol Psychiatry 2009, 66:451-459.
48. Carballedo A, Scheuerecker J, Meisenzahl E, Schoepf V, Bokde A, Möller H-J, Doyle M, Wiesmann M, Frodl T: Functional connectivity of emotional processing in depression. J Affect Disord 2011, 134:272-279.
49. Chen C-H, Suckling J, Ooi C, Fu CHY, Williams SCR, Walsh ND, Mitterschiffthaler MT, Pich EM, Bullmore E: Functional coupling of the amygdala in depressed patients treated with antidepressant medication. Neuropsychopharmacol 2008, 33:1909-1918.
50. Dannlowski U, Ohrmann P, Konrad C, Domschke K, Bauer J, Kugel H, Hohoff C, Schöning S, Kersting A, Baune BT, Mortensen LS, Arolt V, Zwitserlood P, Deckert J, Heindel W, Suslow T: Reduced amygdalaprefrontal coupling in major depression: association with MAOA genotype and illness severity. Int J Neuropsychopharmacol 2009, 12:11-22.
51. Frodl T, Bokde ALW, Scheuerecker J, Lisiecka D, Schoepf V, Hampel H, Möller H-J, Brückmann H, Wiesmann M, Meisenzahl EM: Functional connectivity bias of the orbitofrontal cortex in drug-free patients with major depression. Biol Psychiatry 2010, 67:161-167.
52. Adolphs R, Spezio M: Role of the amygdala in processing visual social stimuli. Brain 2006, 156:363-78.
53. Davis M, Whalen PJ: The amygdala: vigilance and emotion. Mol Psychiatry 2001, 6:13-34.
54. Phan KL, Wager T, Taylor SF, Liberzon I: Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. NeuroImage 2002, 16:331-348.
55. Dannlowski U, Ohrmann P, Bauer J, Kugel H, Arolt V, Heindel W, Kersting A, Baune BT, Suslow T: Amygdala reactivity to masked negative faces is associated with automatic judgmental bias in major depression: a 3 T fMRI study. J Psychiatr Neurosci 2007, 32:423-429.
56. Dannlowski U, Ohrmann P, Bauer J, Kugel H, Arolt V, Heindel W, Suslow T: Amygdala reactivity predicts automatic negative evaluations for facial emotions. Psychiatry Res 2007, 154:13-20.
57. Siegle GJ, Steinhauer SR, Thase ME, Stenger VA, Carter CS: Can't shake that feeling: event-related fMRI assessment of sustained amygdala activity in response to emotional information in depressed individuals. Biol Psychiatry 2002, 51:693-707.
58. Siegle GJ, Thompson WK, Carter CS, Steinhauer SR, Thase ME: Increased amygdala and decreased dorsolateral prefrontal BOLD responses in unipolar depression: related and independent features. Biol Psychiatry 2007, 61:198-209.
59. Kessler H, Taubner S, Buchheim A, Münte TF, Stasch M, Kächele H, Roth G, Heinecke A, Erhard P, Cierpka M, Wiswede D: Individualized and clinically derived stimuli activate limbic structures in depression: an fMRI study. PLoS ONE 2011, 6:e15712.
60. Abler B, Erk S, Herwig U, Walter H: Anticipation of aversive stimuli activates extended amygdala in unipolar depression. J Psychiat Res 2007, 41:511-522.
61. Yang TT, Simmons AN, Matthews SC, Tapert SF, Frank GK, May JE, Bischoff-Grethe A, Lansing AE, Brown G, Strigo IA, Wu J, Paulus MP: Adolescents with major depression demonstrate increased amygdala activation. J Am Acad Child Psy 2010, 49:42-51.
62. Almeida JRC, Versace A, Hassel S, Kupfer DJ, Phillips ML: Elevated amygdala activity to sad facial expressions: a state marker of bipolar but not unipolar depression. Biol Psychiatry 2010, 67:414-421.
63. Fu CHY, Williams SCR, Brammer M, Suckling J, Cleare AJ, Walsh ND, Mitterschiffthaler MT, Andrew CM, Pich EM, Bullmore ET: Neural responses to happy facial expressions in major depression following antidepressant treatment. Am J Psychiatry 2007, 164:599-607.
64. Fitzgerald DA, Angstadt M, Jelsone LM, Nathan PJ, Phan KL: Beyond threat: amygdala reactivity across multiple expressions of facial affect. NeuroImage 2006, 30:1441-1448.
65. Neumeister A, Drevets WC, Belfer I, Luckenbaugh DA, Henry S, Bonne O, Herscovitch P, Goldman D, Charney DS: Effects of a alpha 2Cadrenoreceptor gene polymorphism on neural responses to facial expressions in depression. Neuropsychopharmacol 2006, 31:1750-1756.
66. Norbury R, Selvaraj S, Taylor MJ, Harmer C, Cowen PJ: Increased neural response to fear in patients recovered from depression: a 3T functional magnetic resonance imaging study. Psychol Med 2010, 40:425-432.
67. Thomas EJ, Elliott R, McKie S, Arnone D, Downey D, Juhasz G, Deakin JFW, Anderson IM: Interaction between a history of depression and rumination on neural response to emotional faces. Psychol Med 2011, 41:1-11.
68. van der Veen FM, Evers EA, Deutz NE, Schmitt JA: Effects of acute tryptophan depletion on mood and facial emotion perception related brain activation and performance in healthy women with and without a family history of depression. Neuropsychopharmacol 2007, 32:216-224.
69. Monk CS, Klein RG, Telzer EH, Schroth EA, Mannuzza S, Moulton JL, Guardino M, Masten CL, McClure EB, Fromm SJ, Blair RJ, Pine DS, Ernst M: Amygdala and nucleus accumbens activation to emotional facial expressions in children and adolescents at risk for major depression. Am J Psychiatry 2008, 165:90-98.
70. Mannie ZN, Taylor MJ, Harmer CJ, Cowen PJ, Norbury R: Frontolimbic responses to emotional faces in young people at familial risk of depression. J Affect Disord 2011, 130:127-132.
71. Cremers HR, Demenescu LR, Aleman A, Renken R, van Tol MJ, van der Wee NJ, Veltman DJ, Roelofs K: Neuroticism modulates amygdalaprefrontal connectivity in response to negative emotional facial expressions. NeuroImage 2010, 49:963-970.
72. Dannlowski U, Stuhrmann A, Beutelmann V, Zwanzger P, Lenzen T, Grotegerd D, Domschke K, Hohoff C, Ohrmann P, Bauer J, Lindner C, Posterts C, Konrad C, Arolt V, Heindel W, Kugel H: Limbic scars: Long-term consequences of childhood maltreatment revealed by functional and structural MRI. Biol Psychiatry.
73. Dannlowski U, Ohrmann P, Bauer J, Kugel H, Baune BT, Hohoff C, Kersting A, Arolt V, Heindel W, Deckert J, Suslow T: Serotonergic genes modulate amygdala activity in major depression. Genes Brain Behav 2007, 6:672-676.
74. Dannlowski U, Konrad C, Kugel H, Zwitserlood P, Domschke K, Schöning S, Ohrmann P, Bauer J, Pyka M, Hohoff C, Zhang W, Baune BT, Heindel W, Arolt V, Suslow T: Emotion specific modulation of automatic amygdala responses by 5-HTTLPR genotype. NeuroImage 2009, 53:893-898.
75. Dannlowski U, Ohrmann P, Bauer J, Deckert J, Hohoff C, Kugel H, Arolt V, Heindel W, Kersting A, Baune BT, Suslow T: 5-HTTLPR biases amygdala activity in response to masked facial expressions in major depression. Neuropsychopharmacol 2008, 33:418-424.
76. Hariri AR, Weinberger DR: Imaging genomics. Br Med Bull 2003, 65:259-270.
77. Munafò MR, Brown SM, Hariri AR: Serotonin transporter (5-HTTLPR) genotype and amygdala activation: a meta-analysis. Biol Psychiatry 2008, 63:852-857.
78. Wolfensberger SPA, Veltman DJ, Hoogendijk WJG, Boomsma DI, Geus EJC de: Amygdala responses to emotional faces in twins discordant or concordant for the risk for anxiety and depression. NeuroImage 2008, 41:544-552.
79. Delaveau P, Jabourian M, Lemogne C, Jabourian M, Lemogne C, Guionnet S, Bergouignan L, Fossati P: Brain effects of antidepressants in major depression: a meta-analysis of emotional processing studies. J Affect Disord 2010, 130:66-74.
80. Davidson R, Irwin W: The functional neuroanatomy of emotion and affective style. Trends Cogn Sci 1999, 3:11-21.
81. Drevets WC: Neuroimaging studies of mood disorders. Biol Psychiatry 2000, 48:813-829.
82. Drevets WC: Neuroimaging and neuropathological studies of depression: implications for the cognitive-emotional features of mood disorders. Curr Opin Neurobiol 2001, 11:240-249.
83. Drevets WC, Raichle ME: Neuroanatomical circuits in depression: implications for treatment mechanisms. Psychopharmacol Bull 1992, 28:261-274.
84. Grady CL, Keightley ML: Studies of altered social cognition in neuropsychiatric disorders using functional neuroimaging. Can J Psychiat 2002, 47:327-336.
85. Stein JL, Wiedholz LM, Bassett DS, Weinberger DR, Zink CF, Matty VS, Meyer-Lindenberg A: A validated network of effective amygdala connectivity. Neuroimage 2007, 36:736-745.
86. Calder AJ, Lawrence AD, Young AW: Neuropsychology of fear and loathing. Nat Rev Neurosci 2001, 2:352-363.
87. Critchley H, Daly E, Phillips ML, Brammer M, Bullmore E, Williams S, Van Amelsvoort T, Robertson D, David A, Murphy D: Explicit and implicit neural mechanisms for processing of social information from facial expressions: a functional magnetic resonance imaging study. Hum Brain Mapp 2000, 9:93-105.
88. Vuilleumier P, Pourtois G: Distributed and interactive brain mechanisms during emotion face perception: evidence from functional neuroimaging. Neuropsychologia 2007, 45:174-194.
89. Amaral D: Topographic organization of projections from the amygdala to the visual cortex in the macaque monkey. Neuroscience 2003, 118:1099-1120.
90. Davidson R, Irwin W, Anderle MJ, Kalin NH: The neural substrates of affective processing in depressed patients treated with venlafaxine. Am J Psychiatry 2003, 160:64-75.
91. Keedwell P, Drapier D, Surguladze S, Giampietro V, Brammer M, Phillips ML: Subgenual cingulate and visual cortex responses to sad faces predict clinical outcome during antidepressant treatment for depression. J Affect Disord 2010, 120:120-125.
92. Mayberg HS: Modulating dysfunctional limbic-cortical circuits in depression: towards development of brain-based algorithms for diagnosis and optimised treatment. Br Med Bull 2003, 65:193-207.
93. Bush G, Luu P, Posner M: Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn Sci 2000, 4:215-222.
94. Devinsky O, Morrell MJ, Vogt BA: Contributions of anterior cingulate cortex to behaviour. Brain 1995, 118:279-306.
95. Almeida JRC, Phillips ML, Cerqueira CT, Zilberman M, Lobo D, Henna E, Tavares H, Amaro E, Gorenstein C, Gentil V, Busatto GF: Neural activity changes to emotional stimuli in healthy individuals under chronic use of clomipramine. J Psychopharmacol 2010, 24:1165-1174.
96. Pizzagalli DA: Frontocingulate dysfunction in depression: toward biomarkers of treatment response. Neuropsychopharmacol 2010, 36:183-206.
97. Seminowicz DA, Mayberg HS, McIntosh AR, Goldapple K, Kennedy S, Segal Z, Rafi-Tari S: Limbic-frontal circuitry in major depression: a path modeling metanalysis. NeuroImage 2004, 22:409-418.
98. Tekin S, Cummings JL: Frontal-subcortical neuronal circuits and clinical neuropsychiatry: an update. J Psychosom Res 2002, 53:647-654.
99. Price JL, Drevets WC: Neurocircuitry of mood disorders. Neuropsychopharmacol 2010, 35:192-216.
100. Harmer CJ, Mackay CE, Reid CB, Cowen PJ, Goodwin GM: Antidepressant drug treatment modifies the neural processing of nonconscious threat cues. Biol Psychiatry 2006, 59:816-820.
101. Harmer CJ, Shelley NC, Cowen PJ, Goodwin GM: Increased positive versus negative affective perception and memory in healthy volunteers following selective serotonin and norepinephrine reuptake inhibition. Am J Psychiatry 2004, 161:1256-1263.
102. Norbury R, Taylor MJ, Selvaraj S, Taylor MJ, Harmer C, Cowen PJ: Short-term antidepressant treatment modulates amygdala response to happy faces. Psychopharmacol 2009, 206:197-204.
103. Joormann J, Cooney RE, Henry ML, Gotlib IH: Neural correlates of automatic mood regulation in girls at high risk for depression. J Abnorm Psychol 2011.
104. Gotlib IH, Joormann J: Cognition and depression: current status and future directions. Annu Rev Clin Psychol 2010, 6:285-312.