Effects of acute psychosocial stress on neural activity to emotional and neutral faces in a face recognition memory paradigm

Brain Imaging and Behavior

Volumn 8, Issue 4, 2014, Pages 598-610

  Li, Shijia ^a,c,d   Weerda, Riklef ^a   Milde, Christopher ^a   Wolf, Oliver T ^b   Thiel, Christiane M ^a  

^a UNIVERSITY OF OLDENBURG   (Germany)

^b RUHR UNIVERSITY BOCHUM   (Germany)

^c LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

^d Center for Behavioral Brain Sciences   (Germany)

Author keywords

Acute stress; Emotion; fMRI; Recognition memory

Indexed keywords

HYDROCORTISONE; OXYGEN;

ADULT; AMYGDALOID NUCLEUS; ARTICLE; BLOOD PRESSURE; CONTROLLED STUDY; EMOTION; FACE; FRONTAL CORTEX; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; FUSIFORM GYRUS; HIPPOCAMPUS; HUMAN; INFERIOR FRONTAL GYRUS; MALE; MENTAL STRESS; NORMAL HUMAN; PSYCHOLOGIC TEST; PULSE RATE; RECOGNITION; TASK PERFORMANCE; TRIER SOCIAL STRESS TEST; ACUTE DISEASE; ADOLESCENT; BLOOD; BRAIN; BRAIN CIRCULATION; BRAIN MAPPING; FACIAL EXPRESSION; FEAR; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PATTERN RECOGNITION; PERCEPTION; PERCEPTIVE DISCRIMINATION; PHYSIOLOGY; REACTION TIME; YOUNG ADULT;

ACUTE DISEASE; ADOLESCENT; ADULT; BRAIN; BRAIN MAPPING; CEREBROVASCULAR CIRCULATION; DISCRIMINATION (PSYCHOLOGY); FACE; FACIAL EXPRESSION; FEAR; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; NEUROPSYCHOLOGICAL TESTS; OXYGEN; PATTERN RECOGNITION, VISUAL; REACTION TIME; RECOGNITION (PSYCHOLOGY); SOCIAL PERCEPTION; STRESS, PSYCHOLOGICAL; YOUNG ADULT;

EID: 84911808170     PISSN: 19317557     EISSN: 19317565     Source Type: Journal    
DOI: 10.1007/s11682-013-9287-3     Document Type: Article

References (63)

1. Augustine, J. R. (1996). Circuitry and functional aspects of the insular lobe in primates including humans. Brain Research. Brain Research Reviews, 22(3), 229–244.
2. Badre, D., & Wagner, A. D. (2007). Left ventrolateral prefrontal cortex and the cognitive control of memory. Neuropsychologia, 45(13), 2883–2901. doi:10.1016/j.neuropsychologia.2007.06.015.
3. Bayle, D. J., & Taylor, M. J. (2010). Attention inhibition of early cortical activation to fearful faces. Brain Research, 1313, 113–123. doi:10.1016/j.brainres.2009.11.060.
4. Brown, M. W. (2009). Recognition memory: what’s new in novelty signals? Current Biology, 19(15), R645–R647. doi:10.1016/j.cub.2009.06.031.
5. Buchanan, T. W., Tranel, D., & Adolphs, R. (2006). Impaired memory retrieval correlates with individual differences in cortisol response but not autonomic response. Learning and Memory, 13(3), 382–387. doi:10.1101/lm.206306.
6. Cisler, J. M., Steele, J. S., Lenow, J. K., Smitherman, S., Everett, B., Messias, E., et al. (2013). Functional reorganization of neural networks during repeated exposure to the traumatic memory in posttraumatic stress disorder: an exploratory fMRI study. Journal of Psychiatric Research. doi:10.1016/j.jpsychires.2013.09.013.
7. Craig, A. D. (2009). How do you feel—now? The anterior insula and human awareness. Nature Reviews Neuroscience, 10(1), 59–70. doi:10.1038/nrn2555.
8. Craig, A. D. (2010). The sentient self. Brain Structure and Function, 214(5–6), 563–577. doi:10.1007/s00429-010-0248-y.
9. de Quervain, D. J., Roozendaal, B., Nitsch, R. M., McGaugh, J. L., & Hock, C. (2000). Acute cortisone administration impairs retrieval of long-term declarative memory in humans. Nature Neuroscience, 3(4), 313–314. doi:10.1038/73873.
10. de Quervain, D. J., Henke, K., Aerni, A., Treyer, V., McGaugh, J. L., Berthold, T., et al. (2003). Glucocorticoid-induced impairment of declarative memory retrieval is associated with reduced blood flow in the medial temporal lobe. European Journal of Neuroscience, 17(6), 1296–1302. doi:10.1046/j.1460-9568.2003.02542.x.
11. Dickerson, S. S., & Kemeny, M. E. (2004). Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychological Bulletin, 130(3), 355–391. doi:10.1037/0033-2909.130.3.355.
12. Dolcos, F., LaBar, K. S., & Cabeza, R. (2005). Remembering one year later: role of the amygdala and the medial temporal lobe memory system in retrieving emotional memories. Proceedings of the National Academy of Sciences of the United States of America, 102(7), 2626–2631. doi:10.1073/pnas.0409848102.
13. Ekman, P., & Friesen, W. V. (1976). Pictures of facial affect. Palo Alto: Consulting Psychologists Press.
14. Fairhall, S. L., & Ishai, A. (2007). Effective connectivity within the distributed cortical network for face perception. Cerebral Cortex, 17(10), 2400–2406. doi:10.1093/cercor/bhl148.
15. Fiddick, L. (2011). There is more than the amygdala: potential threat assessment in the cingulate cortex. Neuroscience & Biobehavioral Reviews, 35(4), 1007–1018. doi:10.1016/j.neubiorev.2010.09.014.
16. Friston, K. J., Buechel, C., Fink, G. R., Morris, J., Rolls, E., & Dolan, R. J. (1997). Psychophysiological and modulatory interactions in neuroimaging. NeuroImage, 6(3), 218–229. doi:10.1006/nimg.1997.0291.
17. Fusar-Poli, P., Allen, P., Lee, F., Surguladze, S., Tunstall, N., Fu, C. H., et al. (2007). Modulation of neural response to happy and sad faces by acute tryptophan depletion. Psychopharmacology, 193(1), 31–44. doi:10.1007/s00213-007-0757-4.
18. Gendelman, H. E., Sehlmeyer, C., Schöning, S., Zwitserlood, P., Pfleiderer, B., Kircher, T., et al. (2009). Human fear conditioning and extinction in neuroimaging: a systematic review. PLoS One, 4(6), e5865. doi:10.1371/journal.pone.0005865.
19. Gur, R. C., Sara, R., Hagendoorn, M., Marom, O., Hughett, P., Macy, L., et al. (2002). A method for obtaining 3-dimensional facial expressions and its standardization for use in neurocognitive studies. Journal of Neuroscience Methods, 115(2), 137–143. doi:10.1016/S0165-0270(02)00006-7.
20. Harvey, P. O., Fossati, P., & Lepage, M. (2007). Modulation of memory formation by stimulus content: specific role of the medial prefrontal cortex in the successful encoding of social pictures. Journal of Cognitive Neuroscience, 19(2), 351–362. doi:10.1162/jocn.2007.19.2.351.
21. Hayes, J. P., Morey, R. A., Petty, C. M., Seth, S., Smoski, M. J., McCarthy, G., et al. (2010). Staying cool when things get hot: emotion regulation modulates neural mechanisms of memory encoding. Frontiers in Human Neuroscience, 4, 230. doi:10.3389/fnhum.2010.00230.
22. Henckens, M. J., van Wingen, G. A., Joels, M., & Fernandez, G. (2011). Time-dependent corticosteroid modulation of prefrontal working memory processing. Proceedings of the National Academy of Sciences of the United States of America, 108(14), 5801–5806. doi:10.1073/pnas.1019128108.
23. Het, S., Rohleder, N., Schoofs, D., Kirschbaum, C., & Wolf, O. T. (2009). Neuroendocrine and psychometric evaluation of a placebo version of the ‘Trier Social Stress Test’. Psychoneuroendocrinology, 34(7), 1075–1086. doi:10.1016/j.psyneuen.2009.02.008.
24. Johansson, M., Mecklinger, A., & Treese, A. (2004). Recognition memory for emotional and neutral faces: an event-related potential study. Journal of Cognitive Neuroscience, 16(10), 1840–1853. doi:10.1162/0898929042947883.
25. Keightley, M. L., Chiew, K. S., Anderson, J. A., & Grady, C. L. (2011). Neural correlates of recognition memory for emotional faces and scenes. Social Cognitive and Affective Neuroscience, 6(1), 24–37. doi:10.1093/scan/nsq003.
26. Kim, J. J., & Diamond, D. M. (2002). The stressed hippocampus, synaptic plasticity and lost memories. Nature Reviews Neuroscience, 3(6), 453–462. doi:10.1038/nrn849.
27. Kirschbaum, C., Pirke, K.-M., & Hellhammer, D. H. (1993). The ‘Trier Social Stress Test’—a tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology, 28(1–2), 76–81. doi:10.1159/000119004.
28. Klumpp, H., Angstadt, M., & Phan, K. L. (2012). Insula reactivity and connectivity to anterior cingulate cortex when processing threat in generalized social anxiety disorder. Biological Psychology, 89(1), 273–276. doi:10.1016/j.biopsycho.2011.10.010.
29. Kuhlmann, S., Piel, M., & Wolf, O. T. (2005). Impaired memory retrieval after psychosocial stress in healthy young men. Journal of Neuroscience, 25(11), 2977–2982. doi:10.1523/JNEUROSCI.5139-04.2005.
30. Kukolja, J., Schlapfer, T. E., Keysers, C., Klingmuller, D., Maier, W., Fink, G. R., et al. (2008). Modeling a negative response bias in the human amygdala by noradrenergic-glucocorticoid interactions. Journal of Neuroscience, 28(48), 12868–12876. doi:10.1523/JNEUROSCI.3592-08.2008.
31. Kumaran, D., & Maguire, E. A. (2009). Novelty signals: a window into hippocampal information processing. Trends in Cognitive Science, 13(2), 47–54. doi:10.1016/j.tics.2008.11.004.
32. Lepage, M., Ghaffar, O., Nyberg, L., & Tulving, E. (2000). Prefrontal cortex and episodic memory retrieval mode. Proceedings of the National Academy of Sciences of the United States of America, 97(1), 506–511. doi:10.1073/pnas.97.1.506.
33. Li, S., Weerda, R., Guenzel, F., Wolf, O. T., & Thiel, C. M. (2013). ADRA2B genotype modulates effects of acute psychosocial stress on emotional memory retrieval in healthy young men. Neurobiology of Learning and Memory, 103, 11–18. doi:10.1016/j.nlm.2013.03.006.
34. Lundqvist, D., Flykt, A., & Oehman, A. (1998). The Karolinska Directed Emotional Faces (KDEF). CD ROM from Department of Clinical Neuroscience, Psychology section, Karolinska Institutet. 91-630-7164-9.
35. Maldjian, J. A., Laurienti, P. J., Kraft, R. A., & Burdette, J. H. (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. NeuroImage, 19(3), 1233–1239. doi:10.1016/S1053-8119(03)00169-1.
36. McGaugh, J. L. (2000). Memory—a century of consolidation. Science, 287(5451), 248–251. doi:10.1126/science.287.5451.248.
37. Merz, C. J., Wolf, O. T., & Hennig, J. (2010). Stress impairs retrieval of socially relevant information. Behavioral Neuroscience, 124(2), 288–293. doi:10.1037/a0018942.
38. Oei, N. Y., Elzinga, B. M., Wolf, O. T., de Ruiter, M. B., Damoiseaux, J. S., Kuijer, J. P., et al. (2007). Glucocorticoids decrease hippocampal and prefrontal activation during declarative memory retrieval in young men. Brain Imaging and Behavior, 1(1–2), 31–41. doi:10.1007/s11682-007-9003-2.
39. Oei, N. Y., Veer, I. M., Wolf, O. T., Spinhoven, P., Rombouts, S. A., & Elzinga, B. M. (2012). Stress shifts brain activation towards ventral ‘affective’ areas during emotional distraction. Social Cognitive and Affective Neuroscience, 7(4), 403–412. doi:10.1093/scan/nsr024.
40. Ossewaarde, L., Qin, S., Van Marle, H. J., van Wingen, G. A., Fernandez, G., & Hermans, E. J. (2011). Stress-induced reduction in reward-related prefrontal cortex function. NeuroImage, 55(1), 345–352. doi:10.1016/j.neuroimage.2010.11.068.
41. Qin, S., Hermans, E. J., van Marle, H. J., Luo, J., & Fernandez, G. (2009). Acute psychological stress reduces working memory-related activity in the dorsolateral prefrontal cortex. Biological Psychiatry, 66(1), 25–32. doi:10.1016/j.biopsych.2009.03.006.
42. Roozendaal, B. (2002). Stress and memory: opposing effects of glucocorticoids on memory consolidation and memory retrieval. Neurobiology of Learning and Memory, 78(3), 578–595. doi:10.1006/nlme.2002.4080.
43. Roozendaal, B., & McGaugh, J. L. (2011). Memory modulation. Behavioral Neuroscience, 125(6), 797–824. doi:10.1037/a0026187.
44. Roozendaal, B., Griffith, Q. K., Buranday, J., De Quervain, D. J.-F., & McGaugh, J. L. (2003). The hippocampus mediates glucocorticoid-induced impairment of spatial memory retrieval: dependence on the basolateral amygdala. Proceedings of the National Academy of Sciences of the United States of America, 100(3), 1328–1333. doi:10.1073/pnas.0337480100.
45. Roozendaal, B., Hahn, E. L., Nathan, S. V., de Quervain, D. J., & McGaugh, J. L. (2004). Glucocorticoid effects on memory retrieval require concurrent noradrenergic activity in the hippocampus and basolateral amygdala. Journal of Neuroscience, 24(37), 8161–8169. doi:10.1523/JNEUROSCI.2574-04.2004.
46. Roozendaal, B., Okuda, S., de Quervain, D. J.-F., & McGaugh, J. L. (2006). Glucocorticoids interact with emotion-induced noradrenergic activation in influencing different memory functions. Neuroscience, 138(3), 901–910. doi:10.1016/j.neuroscience.2005.07.049.
47. Roozendaal, B., McEwen, B. S., & Chattarji, S. (2009). Stress, memory and the amygdala. Nature Reviews Neuroscience, 10(6), 423–433. doi:10.1038/nrn2651.
48. Sandi, C., Venero, C., & Guaza, C. (1996). Novelty-related rapid locomotor effects of corticosterone in rats. European Journal of Neuroscience, 8(4), 794–800.
49. Schwabe, L., Joëls, M., Roozendaal, B., Wolf, O. T., & Oitzl, M. S. (2012). Stress effects on memory: an update and integration. Neuroscience & Biobehavioral Reviews, 36(7), 1740–1749. doi:10.1016/j.neubiorev.2011.07.002.
50. Simons, J. S., & Spiers, H. J. (2003). Prefrontal and medial temporal lobe interactions in long-term memory. Nature Reviews Neuroscience, 4(8), 637–648. doi:10.1038/nrn1178.
51. Smeets, T., Otgaar, H., Candel, I., & Wolf, O. T. (2008). True or false? Memory is differentially affected by stress-induced cortisol elevations and sympathetic activity at consolidation and retrieval. Psychoneuroendocrinology, 33(10), 1378–1386. doi:10.1016/j.psyneuen.2008.07.009.
52. Steyer, R., Schwenkmezger, P., Notz, P., & Eid, M. (1994). Der Mehrdimensionale Befindlichkeitsfragebogen (MDBF) [German]. Diagnostica, 40(4), 320–328.
53. Tottenham, N., Tanaka, J. W., Leon, A. C., McCarry, T., Nurse, M., Hare, T. A., et al. (2009). The NimStim set of facial expressions: judgments from untrained research participants. Psychiatry Research, 168(3), 242–249. doi:10.1016/j.psychres.2008.05.006.
54. Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., et al. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage, 15(1), 273–289. doi:10.1006/nimg.2001.0978.
55. van Marle, H. J., Hermans, E. J., Qin, S., & Fernandez, G. (2009). From specificity to sensitivity: how acute stress affects amygdala processing of biologically salient stimuli. Biological Psychiatry, 66(7), 649–655. doi:10.1016/j.biopsych.2009.05.014.
56. Veer, I. M., Oei, N. Y., Spinhoven, P., van Buchem, M. A., Elzinga, B. M., & Rombouts, S. A. (2012). Endogenous cortisol is associated with functional connectivity between the amygdala and medial prefrontal cortex. Psychoneuroendocrinology, 37(7), 1039–1047. doi:10.1016/j.psyneuen.2011.12.001.
57. Vuilleumier, P. (2005). How brains beware: neural mechanisms of emotional attention. Trends in Cognitive Science, 9(12), 585–594. doi:10.1016/j.tics.2005.10.011.
58. Weerda, R., Muehlhan, M., Wolf, O. T., & Thiel, C. M. (2010). Effects of acute psychosocial stress on working memory related brain activity in men. Human Brain Mapping, 31(9), 1418–1429. doi:10.1002/hbm.20945.
59. Weyrauch, B., Huang, J., Heisele, B., & Blanz, V. (2004). Component-based face recognition with 3D morphable models, First IEEE Workshop on Face Processing in Video. Washington, DC: IEEE Computer Society. 0-7695-2158-4.
60. Wingenfeld, K., Driessen, M., Schlosser, N., Terfehr, K., Carvalho Fernando, S., & Wolf, O. T. (2013). Cortisol effects on autobiographic memory retrieval in PTSD: an analysis of word valence and time until retrieval. Stress. doi:10.3109/10253890.2013.796925.
61. Wolf, O. T. (2008). The influence of stress hormones on emotional memory: relevance for psychopathology. Acta Psychologica, 127(3), 513–531. doi:10.1016/j.actpsy.2007.08.002.
62. Wolf, O. T. (2009). Stress and memory in humans: twelve years of progress? Brain Research, 1293, 142–154. doi:10.1016/j.brainres.2009.04.013.
63. Wolf, O. T., Kuhlmann, S., Buss, C., Hellhammer, D. H., & Kirschbaum, C. (2004). Cortisol and memory retrieval in humans: influence of emotional valence. Annals of the New York Academy of Sciences, 1032, 195–197. doi:10.1196/annals.1314.019.