Blunted Social Reward Responsiveness Moderates the Effect of Lifetime Social Stress Exposure on Depressive Symptoms

Frontiers in Behavioral Neuroscience

Volumn 13, Issue , 2019, Pages

  Pegg, Samantha ^a   Ethridge, Paige ^b   Shields, Grant S ^c   Slavich, George M ^d   Weinberg, Anna ^b   Kujawa, Autumn ^a  

^a VANDERBILT UNIVERSITY   (United States)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

depression; electroencephalogram; event related potentials; life stress; neurophysiology; reward responsiveness; social reward

Indexed keywords

ADULT; ARTICLE; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DEPRESSION; DISEASE COURSE; DISEASE SEVERITY; ELECTROENCEPHALOGRAM; EVENT RELATED POTENTIAL; EXPOSURE; FEEDBACK SYSTEM; FEMALE; HUMAN; MAJOR CLINICAL STUDY; MALE; REWARD; RISK; SELF REPORT; SOCIAL ACCEPTANCE; SOCIAL ADAPTATION; SOCIAL PHOBIA; SOCIAL REJECTION; SOCIAL STRESS; SOCIAL SUPPORT; STRESS AND ADVERSITY INVENTORY; STRESS ASSESSMENT; SYMPTOM;

EID: 85072726877     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2019.00178     Document Type: Article

References (51)

1. Bress J. N., Meyer A., Proudfit G. H., (2015). The stability of the feedback negativity and its relationship with depression during childhood and adolescence. Dev. Psychopathol. 17 1285–1294. 10.1017/S0954579414001400 26439074
2. Carlson J. M., Foti D., Mujica-Parodi L. R., Harmon-Jones E., Hajcak G., (2011). Ventral striatal and medial prefrontal BOLD activation is correlated with reward-related electrocortical activity: a combined ERP and fMRI study. Neuroimage. 57 1608–1616. 10.1016/j.neuroimage.2011.05.037 21624476
3. Chapman D. P., Whitfield C. L., Felitti V. J., Dube S. R., Edwards V. J., Anda R. F., (2004). Adverse childhood experiences and the risk of depressive disorders in adulthood. J. Affect. Disord. 82 217–225. 10.1016/j.jad.2003.12.013 15488250
4. Corral-Frías N. S., Nikolova Y. S., Michalski L. J., Baranger D. A., Hariri A. R., Bogdan R., (2015). Stress-related anhedonia is associated with ventral striatum reactivity to reward and transdiagnostic psychiatric symptomatology. Psychol. Med. 45 2605–2617. 10.1017/S0033291715000525 25853627
5. Davey C., Yücel M., Allen N., (2008). The emergence of depression in adolescence: development of the prefrontal cortex and the representation of reward. Neurosci. Biobehav. Rev. 32 1–19. 10.1016/j.neubiorev.2007.04.016 17570526
6. Epel E., Crosswell A., Mayer S., Prather A., Slavich G., Puterman E., (2018). More than a feeling: a unified view of stress measurement for population science. Front. Neuroendocrinol. 49:146–169. 10.1016/j.yfrne.2018.03.001 29551356
7. Ethridge P., Kujawa A., Dirks M. A., Arfer K. B., Kessel E. M., Klein D. N., (2017). Neural responses to social and monetary reward in early adolescence and emerging adulthood. Psychophysiology 54 1786–1799. 10.1111/psyp.12957 28700084
8. Ethridge P., Weinberg A., (2018). Psychometric properties of neural responses to monetary and social rewards across development. Int. J. Psychophysiol. 132 311–322. 10.1016/j.ijpsycho.2018.01.011 29402529
9. Forbes E. E., Dahl R. E., (2012). Altered reward function in adolescent depression: what, when, and how? J. Child Psychol. Psychiatry. 53 3–15. 10.1111/j.1469-7610.2011.02477.x 22117893
10. Goff B., Gee D. G., Telzer E. H., Humphreys K. L., Gabard-Durnam L., Flannery J., (2013). Reduced nucleus accumbens reactivity and adolescent depression following early-life stress. Neuroscience 249 129–138. 10.1016/j.neuroscience.2012.12.010 23262241
11. Goldstein B. L., Kessel E. M., Kujawa A., Finsaas M. C., Davila J., Hajcak G., (2019). Stressful life events moderate the effect of neural reward responsiveness in childhood on depressive symptoms in adolescence. Psychol. Med. 31274066 [Epub ahead of print].
12. Gratton G., Coles M. G., Donchin E., (1983). A new method for off-line removal of ocular artifact. Electroencephalogr. Clin. Neurophysiol. 55 468–484. 10.1016/0013-4694(83)90135-9 6187540
13. Hammen C., (2005). Stress and depression. Annu. Rev. Clin. Psychol. 1 293–319. 10.1146/annurev.clinpsy.1.102803.143938 17716090
14. Hammen C., (2009). Adolescent depression: stressful interpersonal contexts and risk for recurrence. Curr. Dir. Psychol. Sci. 18 200–204. 10.1111/j.1467-8721.2009.01636.x 20161119
15. Hanson J. L., Hariri A. R., Williamson D. E., (2015). Blunted ventral striatum development in adolescence reflects emotional neglect and predicts depressive symptoms. Biol. Psychiatr. 78 598–605. 10.1016/j.biopsych.2015.05.010 26092778
16. Hayes A., (2017). Introduction to Mediation, Moderation, and Conditional Process Analysis, 2nd Edn. New York, NY: Guilford Press.
17. Holroyd C. B., Coles M. G. H., (2002). The neural basis of human error processing: reinforcement learning, dopamine, and error-related negativity. Psychol. Rev. 109 679–709. 10.1037/0033-295X.109.4.679 12374324
18. Holroyd C. B., Coles M. G. H., (2008). Dorsal anterior cingulate cortex integrates reinforcement history to guide voluntary behavior. Cortex. 44 548–559. 10.1016/j.cortex.2007.08.013 18387587
19. Keenan K., Hipwell A., Feng X., Babinski D., Hinze A., Rischall M., (2008). Subthreshold symptoms of depression in preadolescent girls are stable and predictive of depressive disorders. J. Am. Acad. Child Adolesc. Psychiatr. 47 1433–1442. 10.1097/CHI.0b013e3181886eab 19034189
20. Kendler K. S., Gardner C. O., Prescott C. A., (2002). Toward a comprehensive developmental model for major depression in women. Am. J. Psychiatr. 159 1133–1145. 10.1176/appi.ajp.159.7.1133 12091191
21. Kendler K. S., Gardner C. O., Prescott C. A., (2006). Toward a comprehensive developmental model for major depression in men. Am. J. Psychiatr. 163 115–124. 10.1176/appi.ajp.163.1.115 16390898
22. Kendler K. S., Hettema J. M., Butera F., Gardner C. O., Prescott C. A., (2003). Life event dimensions of loss, humiliation, entrapment, and danger in the prediction of onsets of major depression and generalized anxiety. Arch. Gen. Psychiatr. 60 789–796. 10.1001/archpsyc.60.8.789 12912762
23. Kendler K. S., Karkowski L. M., Prescott C. A., (1999). Causal relationship between stressful life events and the onset of major depression. Am. J. Psychiatr. 156 837–841. 10.1176/ajp.156.6.837 10360120
24. Keren H., Callaghan G. O., Vidal-Ribas P., Buzzell G. A., Brotman M. A., Leibenluft E., (2018). Reward processing in depression: a conceptual and meta-analytic review across fMRI and EEG studies. Am. J. Psychiatr. 175 1111–1120. 10.1176/appi.ajp.2018.17101124 29921146
25. Kessler R. C., Avenevoli S., Merikangas K. R., (2001). Mood disorders in children and adolescents: an epidemiologic perspective. Biol. Psychiatr. 49 1002–1014. 10.1016/s0006-3223(01)01129-5 11430842
26. Kessler R. C., McLaughlin K. A., Green J. G., Gruber M. J., Sampson N. A., Zaslavsky A. M., (2010). Childhood adversities and adult psychopathology in the WHO World Mental Health Surveys. Br. J. Psychiatr. 197 378–385. 10.1192/bjp.bp.110.080499 21037215
27. Kujawa A., Arfer K. B., Klein D. N., Proudfit G. H., (2014). Electrocortical reactivity to social feedback in youth: a pilot study of the Island getaway task. Dev. Cogn. Neurosci. 10 140–147. 10.1016/j.dcn.2014.08.008 25212683
28. Kujawa A., Burkhouse K. L., (2017). Vulnerability to depression in youth: advances from affective neuroscience. Biol. Psychiatry. Cogn. Neurosci. Neuroimaging. 2 28–37. 10.1016/j.bpsc.2016.09.006 28497126
29. Kujawa A., Carroll A., Mumper E., Mukherjee D., Kessel E. M. M., Olino T., (2018). A longitudinal examination of event-related potentials sensitive to monetary reward and loss feedback from late childhood to middle adolescence. Int. J. Psychophysiol. 132 323–330. 10.1016/j.ijpsycho.2017.11.001 29113953
30. Kujawa A., Hajcak G., Danzig A. P., Black S. R., Bromet E. J., Carlson G. A., (2016). Neural reactivity to emotional stimuli prospectively predicts the impact of a natural disaster on psychiatric symptoms in children. Biol. Psychiatry. 80 381–389. 10.1016/j.biopsych.2015.09.008 26526228
31. Kujawa A., Hajcak G., Klein D. N., (2019). Reduced reward responsiveness moderates the effect of maternal depression on depressive symptoms in offspring: evidence across levels of analysis. J. Child. Psychol. Psychiatr. 60 82–90. 10.1111/jcpp.12944 29978904
32. Kujawa A., Smith E., Luhmann C., Hajcak G., (2013). The feedback negativity reflects favorable compared to nonfavorable outcomes based on global, not local, alternatives. Psychophyiology 50 134–138. 10.1111/psyp.12002 23241216
33. La Greca A., Harrison H., (2005). Adolescent peer relations, friendships, and romantic relationships: do they predict social anxiety and depression? J. Clin. Child Adolesc. Psychol. 34 49–61. 10.1207/s15374424jccp3401_5 15677280
34. McLaughlin K. A., Busso D. S., Duys A., Green J. G., Alves S., Way M., (2014). Amygdala response to negative stimuli predicts PTSD symptom onset following a terrorist attack. Depress. Anxiety. 31 834–842. 10.1002/da.22284 24995938
35. Meyer A., Lerner M., De Los Reyes A., Laird R., Hajcak G., (2017). Considering ERP difference scores as individual difference measures: issues with subtraction and alternative approaches. Psychophysiology 54 114–122. 10.1111/psyp.12664 28000251
36. National Institute of Mental Health. [NIMH] (2019). RDoC Matrix. Available at: http://www.nimh.nih.gov/research-priorities/rdoc/constructs/rdoc-matrix.shtml (accessed February 28, 2019).
37. Nelson B. D., Perlman G., Klein D. N., Kotov R., Hajcak G., (2016). Blunted neural response to rewards as a prospective predictor of the development of depression in adolescent girls. Am. J. Psychiatr. 173 1223–1230. 10.1176/appi.apj.2016.15121524 27363510
38. Nikolova Y. S., Bogdan R., Brigidi B. D., Hariri A. R., (2012). Ventral striatum reactivity to reward and recent life stress interact to predict positive affect. Biol. Psychiatr. 72 157–163. 10.1016/j.biopsych.2012.03.014 22534456
39. Proudfit G. H., (2015). The reward positivity: from basic research on reward to a biomarker for depression. Psychophysiology 50 449–459. 10.1111/psyp.12370 25327938
40. Sandre A., Bagot R. C., Weinberg A., (2019). Blunted neural response to appetitive images prospectively predicts symptoms of depression, and not anxiety, during the transition to university. Biol. Psychol. 145 31–41. 10.1016/j.biopsycho.2019.04.001 30974147
41. Setterfield M., Walsh M., Frey A., McCabe C., (2016). Increased social anhedonia and reduced helping behaviour in young people with high depressive symptomatology. J. Affect. Disord. 15 372–377. 10.1016/j.jad.2016.08.020 27568175
42. Silk J. S., Davis S., McMakin D. L., Dahl R. E., Forbes E. E., (2012). Why do anxious children become depressed teenagers? the role of social evaluative threat and reward processing. Psychol. Med. 42 2095–2107. 10.1017/S0033291712000207 22340187
43. Slavich G. M., (2016). Life stress and health: a review of conceptual issues and recent findings. Teach. Psychol. 43 346–355. 10.1177/0098628316662768 27761055
44. Slavich G. M., (2019). Stressnology: the primitive (and problematic) study of life stress exposure and pressing need for better measurement. Brain. Behav. Immun. 75 3–5. 10.1016/j.bbi.2018.08.011 30236597
45. Slavich G. M., Thornton T., Torres L., Monroe S., Gotlib I., (2009). Targeted rejection predicts hastened onset of major depression. J. Soc. Clin. Psychol. 28 223–243. 10.1521/jscp.2009.28.2.223 20357895
46. Slavich G. M., Shields G. S., (2018). Assessing lifetime stress exposure using the stress and adversity inventory for adults (Adult STRAIN): an overview and initial validation. Psychosom. Med. 80 17–27. 10.1097/PSY.0000000000000534 29016550
47. Slavich G. M., Tartter M. A., Brennan P. A., Hammen C., (2014). Endogenous opioid system influences depressive reactions to socially painful targeted rejection life events. Psychoneuroendocrinology 49 141–149. 10.1016/j.psyneuen.2014.07.009 25086307
48. Starr L. R., Davila J., (2008). Differentiating interpersonal correlates of depressive symptoms and social anxiety in adolescence: implications for models of comorbidity. J. Clin. Child. Adolesc. Psychol. 37 337–349. 10.1080/15374410801955854 18470771
49. Stasik-O’Brien S. M., Brock R. L., Chmielewski M., Naragon-Gainey K., Koffel E., McDade-Montez E., (2018). Clinical utility of the inventory of depression and anxiety symptoms (IDAS). Assessment 26 944–960. 10.1177/1073191118790036 30043620
50. Swartz J. R., Knodt A. R., Radtke S. R., Hariri A. R., (2015). A neural biomarker of psychological vulnerability to future life stress. Neuron 85 505–511. 10.1016/j.neuron.2014.12.055 25654256
51. Watson D., O’Hara M. W., Simms L. J., Kotov R., Chmielewski M., McDade-Montez E. A., (2007). Development and validation of the inventory of depression and anxiety symptoms (IDAS). Psychol. Assess. 19 253–268. 10.1037/1040-3590.19.3.253 17845118