Augmenting serotonin neurotransmission with citalopram modulates emotional expression decoding but not structural encoding of moderate intensity sad facial emotional stimuli: An event-related potential (ERP) investigation

Journal of Psychopharmacology

Volumn 24, Issue 8, 2010, Pages 1153-1164

  Labuschagne, I ^a   Croft, R J ^b   Phan, K L ^c   Nathan, P J ^a,d  

^a MONASH UNIVERSITY   (Australia)

^b SWINBURNE UNIVERSITY OF TECHNOLOGY   (Australia)

^c UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

antidepressants; citalopram; emotion; evoked potentials; facial expression; late positive potential; N170; N250; serotonin

Indexed keywords

CITALOPRAM; PLACEBO; SEROTONIN;

ADULT; ARTICLE; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DOUBLE BLIND PROCEDURE; DRUG MECHANISM; EMOTION; EVENT RELATED POTENTIAL; FACIAL EXPRESSION; FACIAL RECOGNITION; HUMAN; HUMAN EXPERIMENT; MALE; MEASUREMENT; NEUROTRANSMISSION; NORMAL HUMAN; PRIORITY JOURNAL; RECOGNITION; STIMULUS;

ADOLESCENT; ADULT; AFFECT; CITALOPRAM; CROSS-OVER STUDIES; DEPRESSIVE DISORDER, MAJOR; DOUBLE-BLIND METHOD; ELECTROENCEPHALOGRAPHY; EMOTIONS; EVOKED POTENTIALS; FACIAL EXPRESSION; HUMANS; MALE; PSYCHIATRIC STATUS RATING SCALES; SEROTONIN; SEROTONIN UPTAKE INHIBITORS; SYNAPTIC TRANSMISSION; YOUNG ADULT;

EID: 77955145336     PISSN: 02698811     EISSN: 14617285     Source Type: Journal    
DOI: 10.1177/0269881108097878     Document Type: Article

References (82)

1. Adolphs, R., Tranel, D. (2004) Impaired judgments of sadness but not happiness following bilateral amygdala damage. J Cogn Neurosci 16: 453-462.
2. Amaral, DG (2002) The primate amygdala and the neurobiology of social behavior: implications for understanding social anxiety. Biol Psychiatry 51: 11-17.
3. Ashley, V., Vuilleumier, P., Swick, D. (2004) Time course and specificity of event-related potentials to emotional expressions. Neuroreport 15: 211-216.
4. Attenburrow, MJ, Williams, C., Odontiadis, J., Reed, A., Powell, J., Cowen, PJ, et al. (2003) Acute administration of nutritionally sourced tryptophan increases fear recognition. J Psychopharmacol 169: 104-107.
5. Balconi, M., Pozzoli, U. (2003) Face-selective processing and the effect of pleasant and unpleasant emotional expressions on ERP correlates. Int J Psychophysiol 49: 67-74.
6. Beck, AT, Rush, AJ, Shaw, BF, Emery, G. (1979) Cognitive Therapy of Depression. New York: Guildford Press.
7. Bentin, S., Allison, T., Puce, A., Perez, E., McCarthy, G. (1996) Electrophysiological studies of face perception in humans. J Cogn Neurosci 8: 551-565.
8. Bhagwagar, Z., Cowen, PJ, Goodwin, GM, Harmer, CJ (2004) Normalization of enhanced fear recognition by acute SSRI treatment in subjects with a previous history of depression. Am J Psychiatry 161: 166-168.
9. Bond, A., Lader, M. (1974) The use of analog scales in rating subjective feelings. Br J Med Psychol 47: 211-218.
10. Bouhuys, AL, Geerts, E., Gordijn, MC (1999) Gender-specific mechanisms associated with outcome of depression: perception of emotions, coping and interpersonal functioning. J Psychiatr Res 85: 247-261.
11. Bradley, BP, Mogg, K., Millar, N., White, J. (1995) Selective processing of negative information: effects of clinical anxiety, concurrent depression, and awareness. J Abnorm Psychol 104: 532-536.
12. Browning, M., Reid, C., Cowen, PJ, Goodwin, GM, Harmer, CJ (2007) A single dose of citalopram increases fear recognition in healthy subjects. Psychopharmacol 21: 11-20.
13. Bruce, V., Young, A. (1986) Understanding face recognition. Br J Psychol 77: 305-327.
14. Calder, AJ, Young, AW (2005) Understanding the recognition of facial identity and facial expression. Nat Rev Neurosci 6: 641-651.
15. Carmel, D., Bentin, S. (2002) Domain specificity versus expertise: factors influencing distinct processing of faces. Cognition 83: 1-29.
16. Carretié, L., Iglesias, J. (1995) An ERP study on the specificity of facial expression processing. Int J Psychophysiol 19: 183-192.
17. Croft, RJ, Barry, RJ (2000) EOG correction of blinks with saccade coefficients: a test and revision of the aligned-artefact average solution. Clin Neurophysiol 111: 444-451.
18. Cuthbert, BN, Schupp, HT, Bradley, MM, Birbaumer, N., Lang, PJ (2000) Brain potentials in affective picture processing: covariation with autonomic arousal and affective report. Biol Psychol 52: 95-111.
19. Del-Ben, CM, Deakin, JFW, McKie, S., Delvai, NA, Williams, SR, Elliott, R., et al. (2005) The effect of CIT pre-treatment on neuronal responses to neuropsychological tasks in normal volunteers: an fMRI study. Neuropsychopharmacology 30: 1724-1734.
20. Eimer, M. (1998) Does the face-specific N170 component reflect the activity of a specialized eye processor ? Neuroreport 9: 2945-2948.
21. Eimer, M. (2000) The face-specific N170 component reflects late stages in the structural encoding of faces. Neuroreport 11: 2319-2324.
22. Eimer, M., Holmes, A. (2002) An ERP study on the time course of emotional face processing. Neuroreport 13: 427-431.
23. Eimer, M., Holmes, A. (2006) Event-related brain potential correlates of emotional face processing. Neuropsychologia 45: 15-31.
24. Eimer, M., Holmes, A., McGlone, FP (2003) The role of spatial attention in the processing of facial expression: an ERP study of rapid brain responses to six basic emotions. Cogn Affect Behav Neurosci 3: 97-110.
25. Ekman, P., Friesen, WV (1976) Pictures of Facial Affect. Palo Alto: Consulting Psychologists Press.
26. Fu, CH, Williams, SC, Cleare, AJ, Brammer, MJ, Walsh, ND, Kim, J., et al. (2004) 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 61: 877-889.
27. Grillon, C., Levenson, J., Pine, DS (2007) A single dose of the selective serotonin reuptake inhibitor citalopram exacerbates anxiety in humans: a fear-potentiated startle study. Neuropsychopharmacology 32: 225-231.
28. Han, S., He, X., Woods, DL (2000) Hierarchical processing and level-repetition effect as indexed by early brain potentials. Psychophysiology 37: 817-830.
29. Harmer, CJ, Bhagwagar, Z., Perrett, DI, Vollm, BA, Cowen, PJ, Goodwin, GM (2003) Acute SSRI administration affects the processing of social cues in healthy volunteers. Neuropsychopharmacology 28: 148-152.
30. Harmer, CJ, Mackay, CE, Reid, CB, Cowen, PJ, Goodwin, GM (2006) Antidepressant drug treatment modifies the neural processing of nonconscious threat cues. Biol Psychiatry 59: 816-820.
31. Harmer, CJ, Shelley, NC, Cowen, PJ, Goodwin, GM (2004) Increased positive versus negative affective perception and memory in healthy volunteers following selective serotonin and norepinephrine reuptake inhibition. Am J Psychiatry 161: 1256-1263.
32. Haxby, JV, Hoffman, EA, Gobbini, IM (2000) The distributed human neural system for face perception. Trends Cogn Sci 4: 223-233.
33. Haxby, JV, Ungerleider, LG, Horwitz, B., Maisog, JM, Rapoport, SI, Grady, CL (1996) Face encoding and recognition in the human brain. Proc Nat Acad Sci U S A 93: 922-927.
34. Herrmann, MJ, Aranda, D., Ellgring, H., Mueller, TJ, Stirk, WK, Heidrich, A., et al. (2002) Face-specific event-related potential in humans is independent from facial expression. Int J Psychophysiol 45: 241-244.
35. Hyttel, J. (1994) Pharmacological characterization of selective serotonin reuptake inhibitors (SSRIs). Int Clin Psychopharmacol 9: 19-26.
36. Itier, RJ, Taylor, MJ (2004) N170 or N1? Spatiotemporal differences between object and face processing using ERPs. Cereb Cortex 14: 132-142.
37. Johnston, PJ, Stojanov, W., Devir, H., Schall, U. (2005) Functional MRI of facial emotion recognition deficits in schizophrenia and their electrophysiological correlates. Eur J Neurosci 22: 1221-1232.
38. Johnston, VS, Miller, DR, Burleson, MH (1986) Multiple P3s to emotional stimuli and their theoretical significance. Psychophysiology 23: 684-693.
39. Johnston, VS, Wang, XT (1991) The relationship between the menstrual phase and the P300 component of the ERP. Psychophysiology 28: 400-409.
40. Kemp, AH, Gray, MA, Silberstein, RB, Armstrong, SM, Nathan, PJ (2004 a) Augmentation of serotonin enhances pleasant and suppresses unpleasant cortical electrophysiological responses to visual emotional stimuli in humans. Neuroimage 22: 1084-1096.
41. Kemp, AH, Gray, MA, Silberstein, RB, Armstrong, SM, Nathan, PJ (2004 b) Gender differences in the cortical electrophysiological processing of visual emotional stimuli. Neuroimage 21: 632-646.
42. Kestenbaum, R., Nelson, CA (1992) Neural and behavioural correlates of emotion recognition in children and adults. J Exp Child Psychol 54: 1-18.
43. Kirita, T., Endo, M. (1995) Happy face advantage in recognizing facial expressions. Acta Psychol 89: 149-163.
44. Krolak-Salmon, P., Fischer, C., Vighetto, A., Mauguiere, F. (2001) Processing of facial emotional expression: spatio-temporal data as assessed by scalp event-related potentials. Eur J Neurosci 13: 987-994.
45. Laurian, S., Bader, M., Lanares, J., Oros, L. (1991) Topography of event-related potentials elicited by visual emotional stimuli. Int J Psychophysiol 10: 231-238.
46. Lennox, BR, Jacob, R., Calder, AJ, Lupson, V., Bullmore, ET (2004) Behavioural and neurocognitive responses to sad facial affect are attenuated in patients with mania. Psychol Med 34: 795-802.
47. Ley, RC, Bryden, MP (1979) Hemispheric differences in processing emotions and faces. Brain Lang 7: 127-138.
48. MacLeod, C., Mathews, A., Tata, P. (1986) Attentional bias in emotional disorders. J Abnorm Psychol 95: 15-20.
49. Mayberg, HS, Brannan, SK, Tekell, JL, Silva, JA, Mahurin, RK, McGinnis, S., et al. (2000) Regional metabolic effect of fluoxetine in major depression: serial changes and relationship to clinical response. Biol Psychiatry 48: 830-843.
50. Mayberg, HS, Liotti, M., Brannan, SK, McGinnis, S., Mahurin, RK, Jerabek, PA, et al. (1999) Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. Am J Psychiatry 156: 675-682.
51. Mercado, F., Carretie, L., Tapia, M., Gomez-Jarabo, G. (2006) The influence of emotional context on attention in anxious subjects: neurophysiological correlates. J Anxiety Disord 20: 72-84.
52. Mogg, K., Bradley, BP (2002) Selective orienting of attention to masked threat faces in social anxiety. Behav Res Ther 40: 1403-1414.
53. Mogg, K., Bradley, BP, Williams, R. (1995) Attentional bias in anxiety and depression: the role of awareness. Br J Clin Psychol 34: 17-36.
54. Monk, CS, Nelson, EE, McClure, EB, Mogg, K., Bradley, BP, Leibenluft, E., et al. (2006) Ventrolateral prefrontal cortex activation and attentional bias in response to angry faces in adolescents with generalized anxiety disorder. Am J Psychiatry 163: 1091-1097.
55. Murphy, SE, Longhitano, C., Ayres, RE, Cowen, PJ, Harmer, CJ (2006) Tryptophan supplementation induces a positive bias in the processing of emotional material in healthy female volunteers. Psychopharmacology 187: 121-130.
56. Noble, S., Benfield, P. (1997) CIT: a review of its pharmacology, clinical efficacy and tolerability in the treatment of depression. CNS Drugs 8: 410-431. (Pubitemid 27501764)
57. Orozco, S., Ehlers, CL (1998) Gender differences in electrophysiological responses to facial stimuli. Biol Psychiatry 15: 281-289.
58. Oya, H., Kawasaki, H., Howard III, MA, Adolphs, R. (2002) Electrophysiological responses in the human amygdala discriminate emotion categories of complex visual stimuli. J Neurosci 22: 9502-9512.
59. Phan, KL, Taylor, SF, Welsh, RC, Decker, LR, Noll, DC, Nichols, TE, et al. (2003) Activation of the medial prefrontal cortex and extended amygdala by individual ratings of emotional arousal: a functional magnetic resonance imaging study. Biol Psychiatry 53: 211-215.
60. Puce, A., Epling, JA, Thompson, JC, Carrick, OK (2006) Neural responses elicited to face motion and vocalisation pairings. J Neurophysiol 45: 93-106.
61. Roschmann, R., Wittling, W. (1992) Topographic brain mapping of emotion-related hemisphere asymmetries. Int J Neurosci 63: 5-16.
62. Rossignol, M., Philippot, P., Douilliez, C., Crommelinck, M., Campanella, S. (2005) The perception of fearful and happy facial expression is modulated by anxiety: an event-related potential study. Neurosci Lett 377: 115-120.
63. Sato, W., Kochiyama, T., Yoshikawa, S., Matsumura, M. (2001) Emotional expression boosts early visual processing of the face: ERP recording and its decomposition by independent component analysis. Neuroreport 12: 709-714.
64. Sato, W., Kochiyama, T., Yoshikawa, S., Naito, E., Matsumura, M. (2004) Enhanced neural activity in response to dynamic facial expressions of emotion: an fMRI study. Brain Res Cogn Brain Res 20: 81-91.
65. Schneider, F., Habel, U., Kessler, C., Salloum, JB, Posse, S. (2000) Gender differences in regions cerebral activity during sadness. Hum Brain Mapp 9: 226-238.
66. Schupp, HT, Cuthbert, BN, Bradley, MM, Cacioppo, JT, Ito, T., Lang, PJ (2000) Affective picture processing: the late positive potential is modulated by motivational relevance. Psychophysiology 37: 257-261.
67. Schupp, HT, Junghofer, M., Weike, AI, Hamm, AO (2003) Attention and emotion: an ERP analysis of facilitated emotional stimulus processing. Neuroreport 14: 1107-1110.
68. Schupp, HT, Ohman, A., Junghofer, M., Weike, AI, Stockburger, J., Hamm, AO (2004) The facilitated processing of threatening faces: an ERP analysis. Emotion 4: 189-200.
69. 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. Biol Psychiatry 50: 651-658.
70. Streit, M., Wöwler, W., Brinkmeyer, J., Ihl, R., Gaebel, W. (2000) Electrophysiological correlates of emotional and structural face processing in humans. Neurosci Lett 278: 13-16.
71. Surguladze, SA, Young, AW, Senior, C., Brebion, G., Travis, MJ, Phillips, ML (2004) Recognition accuracy and response bias to happy and sad facial expressions in patients with major depression. Neuropsychology 18: 212-218.
72. Tabachnick, BG, Fidell, LS (2001) Using multivariate statistics, fourth ed. Boston, MA: Allyn & Bacon.
73. Taylor, MJ (2002) Non-spatial attentional effects on P1. Clin Neurphysiol 113: 1903-1908.
74. Vanderploeg, RD, Brown, WS, Marsh, JT (1987) Judgements of emotion in words and faces: ERP correlates. Int J Psychophysiol 5: 193-205.
75. 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.
76. Werheid, K., Alpay, G., Jentzsche, I., Sommer, W. (2005) Priming emotional facial expressions as evidenced by event-related brain potentials. Int J Psychophysiol 55: 209-219.
77. Williams, LM (2006) An integrative neuroscience model of "significance" processing. J Integr Neurosci 5: 1-47.
78. Williams, LM, Das, P., Liddell, B., Olivieri, G., Peduto, A., Brammer, MJ, et al. (2005) Bold, sweat and fears: fMRI and skin conductance distinguish facial fear signals. Neuroreport 16: 49-52.
79. Williams, LM, Palmer, D., Liddell, BJ, Song, L., Gordon, E. (2006) The wheng and whereg of perceiving signals of threat versus non-threat. Neuroimage 31: 458-467.
80. Winston, JS, OgDoherty, J., Dolan, RJ (2003) Common and distinct neural responses during direct and incidental processing of multiple facial emotions. Neuroimage 20: 84-97.
81. Winston, JS, Strange, BA, OgDoherty, J., Dolan, RJ (2002) Automatic and intentional brain responses during evaluation of trustworthiness of faces. Nat Neurosci 5: 277-283.
82. Young, AW, Rowland, D., Calder, AJ, Etcoff, NL, Seth, A., Perrett, DI (1997) Facial expression megamix: tests of dimensional and category accounts of emotion recognition. Cognition 63: 271-313.