Elevated cortisol awakening response associated with early life stress and impaired executive function in healthy adult males

Hormones and Behavior

Volumn 95, Issue , 2017, Pages 13-21

  Butler, Kevin ^a   Klaus, Kristel ^a   Edwards, Laura ^a   Pennington, Kyla ^a  

^a UNIVERSITY OF LINCOLN   (United Kingdom)

Author keywords

Cortisol awakening response; Early life stress; Executive function; Healthy adults; Planning; Problem solving

Indexed keywords

HYDROCORTISONE;

ADULT; ARTICLE; CORTISOL AWAKENING RESPONSE; DESCRIPTIVE RESEARCH; EARLY LIFE STRESS; EDUCATIONAL STATUS; ENDOCRINE FUNCTION; ENDOCRINE FUNCTION TEST; EXECUTIVE FUNCTION; HUMAN; HUMAN EXPERIMENT; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; MALE; NORMAL HUMAN; PRIORITY JOURNAL; RETROSPECTIVE STUDY; SALIVA LEVEL; SELF REPORT; SLEEP QUALITY; ANXIETY; AROUSAL; CHEMISTRY; ETIOLOGY; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; LIFE EVENT; MENTAL DISEASE; MENTAL STRESS; METABOLISM; MIDDLE AGED; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY; RISK FACTOR; SALIVA; WAKEFULNESS; YOUNG ADULT;

ADULT; ANXIETY; AROUSAL; EXECUTIVE FUNCTION; HUMANS; HYDROCORTISONE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; LIFE CHANGE EVENTS; MALE; MENTAL DISORDERS; MIDDLE AGED; PITUITARY-ADRENAL SYSTEM; RISK FACTORS; SALIVA; STRESS, PSYCHOLOGICAL; WAKEFULNESS; YOUNG ADULT;

EID: 85026540058     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2017.07.013     Document Type: Article

References (85)

1. Aardal, E., Holm, A.C., Cortisol in saliva–reference ranges and relation to cortisol in serum. Eur. J. Clin. Chem. Clin. Biochem. 33 (1995), 927–932.
2. Adam, E.K., Doane, L.D., Zinbarg, R.E., Mineka, S., Craske, M.G., Griffith, J.W., Prospective prediction of major depressive disorder from cortisol awakening responses in adolescence. Psychoneuroendocrinology 35 (2010), 921–931.
3. Adam, E.K., Vrshek-Schallhorn, S., Kendall, A.D., Mineka, S., Zinbarg, R.E., Craske, M.G., Prospective associations between the cortisol awakening response and first onsets of anxiety disorders over a six-year follow-up–2013 Curt Richter award winner. Psychoneuroendocrinology 44 (2014), 47–59.
4. Alexander, W.H., Brown, J.W., Computational models of performance monitoring and cognitive control. Top. Cogn. Sci. 2 (2010), 658–677.
5. Almasy, L., Blangero, J., Endophenotypes as quantitative risk factors for psychiatric disease: rationale and study design. Am. J. Med. Genet. 105 (2001), 42–44.
6. Almela, M., van der Meij, L., Hidalgo, V., Villada, C., Salvador, A., The cortisol awakening response and memory performance in older men and women. Psychoneuroendocrinology 37 (2012), 1929–1940.
7. Arnsten, A.F., Stress signalling pathways that impair prefrontal cortex structure and function. Nat. Rev. Neurosci. 10 (2009), 410–422.
8. Banihashemi, L., Sheu, L.K., Midei, A.J., Gianaros, P.J., Childhood physical abuse predicts stressor-evoked activity within central visceral control regions. Soc. Cogn. Affect. Neurosci. 10 (2015), 474–485.
9. Barter, C., Stanley, N., Inter-personal violence and abuse in adolescent intimate relationships: mental health impact and implications for practice. Int Rev Psychiatry, 2016, 1–19.
10. Bauer, P.M., Hanson, J.L., Pierson, R.K., Davidson, R.J., Pollak, S.D., Cerebellar volume and cognitive functioning in children who experienced early deprivation. Biol. Psychiatry 66 (2009), 1100–1106.
11. Berger, M., Kraeuter, A.K., Romanik, D., Malouf, P., Amminger, G.P., Sarnyai, Z., Cortisol awakening response in patients with psychosis: systematic review and meta-analysis. Neurosci. Biobehav. Rev. 68 (2016), 157–166.
12. Boehringer, A., Tost, H., Haddad, L., Lederbogen, F., Wust, S., Schwarz, E., Meyer-Lindenberg, A., Neural correlates of the cortisol awakening response in humans. Neuropsychopharmacology 40 (2015), 2278–2285.
13. Bos, K.J., Fox, N., Zeanah, C.H., Nelson, C.A. III, Effects of early psychosocial deprivation on the development of memory and executive function. Front. Behav. Neurosci., 3, 2009, 16.
14. Brown, S.M., Henning, S., Wellman, C.L., Mild, short-term stress alters dendritic morphology in rat medial prefrontal cortex. Cereb. Cortex 15 (2005), 1714–1722.
15. Cardona, J.F., Manes, F., Escobar, J., Lopez, J., Ibanez, A., Potential consequences of abandonment in preschool-age: neuropsychological findings in institutionalized children. Behav. Neurol. 25 (2012), 291–301.
16. Carnegie, R., Araya, R., Ben-Shlomo, Y., Glover, V., O'Connor, T.G., O'Donnell, K.J., Pearson, R., Lewis, G., Cortisol awakening response and subsequent depression: prospective longitudinal study. Br. J. Psychiatry 204 (2014), 137–143.
17. Carpenter, L.L., Shattuck, T.T., Tyrka, A.R., Geracioti, T.D., Price, L.H., Effect of childhood physical abuse on cortisol stress response. Psychopharmacology 214 (2011), 367–375.
18. Carr, C.P., Martins, C.M., Stingel, A.M., Lemgruber, V.B., Juruena, M.F., The role of early life stress in adult psychiatric disorders: a systematic review according to childhood trauma subtypes. J. Nerv. Ment. Dis. 201 (2013), 1007–1020.
19. Chida, Y., Steptoe, A., Cortisol awakening response and psychosocial factors: a systematic review and meta-analysis. Biol. Psychol. 80 (2009), 265–278.
20. Cicchetti, D., Rogosch, F.A., Diverse patterns of neuroendocrine activity in maltreated children. Dev. Psychopathol. 13 (2001), 677–693.
21. Cicchetti, D., Rogosch, F.A., Gunnar, M.R., Toth, S.L., The differential impacts of early physical and sexual abuse and internalizing problems on daytime cortisol rhythm in school-aged children. Child Dev. 81 (2010), 252–269.
22. Clow, A., Thorn, L., Evans, P., Hucklebridge, F., The awakening cortisol response: methodological issues and significance. Stress 7 (2004), 29–37.
23. Cohen, S., Kamarck, T., Mermelstein, R., A global measure of perceived stress. J. Health Soc. Behav. 24 (1983), 385–396.
24. Corbett, B.A., Schupp, C.W., The cortisol awakening response (CAR) in male children with autism spectrum disorder. Horm. Behav. 65 (2014), 345–350.
25. Crozier, J.C., Wang, L., Huettel, S.A., De Bellis, M.D., Neural correlates of cognitive and affective processing in maltreated youth with posttraumatic stress symptoms: does gender matter?. Dev. Psychopathol. 26 (2014), 491–513.
26. Davidovich, S., Collishaw, S., Thapar, A.K., Harold, G., Thapar, A., Rice, F., Do better executive functions buffer the effect of current parental depression on adolescent depressive symptoms?. J. Affect. Disord. 199 (2016), 54–64.
27. De Bellis, M.D., Zisk, A., The biological effects of childhood trauma. Child Adolesc. Psychiatr. Clin. N. Am., 23(185–222), 2014, vii.
28. De Bellis, M.D., Keshavan, M.S., Clark, D.B., Casey, B.J., Giedd, J.N., Boring, A.M., Frustaci, K., Ryan, N.D., A.E. Bennett research award. Developmental traumatology. Part II: brain development. Biol. Psychiatry 45 (1999), 1271–1284.
29. DeSantis, S.M., Baker, N.L., Back, S.E., Spratt, E., Ciolino, J.D., Moran-Santa Maria, M., Dipankar, B., Brady, K.T., Gender differences in the effect of early life trauma on hypothalamic-pituitary-adrenal axis functioning. Depress Anxiety 28 (2011), 383–392.
30. Diamond, A., Executive functions. Annu. Rev. Psychol. 64 (2013), 135–168.
31. Doom, J.R., Gunnar, M.R., Stress physiology and developmental psychopathology: past, present, and future. Dev. Psychopathol. 25 (2013), 1359–1373.
32. Engert, V., Efanov, S.I., Dedovic, K., Dagher, A., Pruessner, J.C., Increased cortisol awakening response and afternoon/evening cortisol output in healthy young adults with low early life parental care. Psychopharmacology 214 (2011), 261–268.
33. Ennis, G.E., Moffat, S.D., Hertzog, C., The cortisol awakening response and cognition across the adult lifespan. Brain Cogn. 105 (2016), 66–77.
34. Enoch, M.A., The role of early life stress as a predictor for alcohol and drug dependence. Psychopharmacology 214 (2011), 17–31.
35. Evans, P., Hucklebridge, F., Loveday, C., Clow, A., The cortisol awakening response is related to executive function in older age. Int. J. Psychophysiol. 84 (2012), 201–204.
36. Finkelhor, D., Ormrod, R.K., Turner, H.A., Poly-victimization: a neglected component in child victimization. Child Abuse Negl. 31 (2007), 7–26.
37. Fossati, P., Ergis, A.M., Allilaire, J.F., Executive functioning in unipolar depression: a review. Encéphale 28 (2002), 97–107.
38. Franz, C.E., O'Brien, R.C., Hauger, R.L., Mendoza, S.P., Panizzon, M.S., Prom-Wormley, E., Eaves, L.J., Jacobson, K., Lyons, M.J., Lupien, S., Hellhammer, D., Xian, H., Kremen, W.S., Cross-sectional and 35-year longitudinal assessment of salivary cortisol and cognitive functioning: the Vietnam era twin study of aging. Psychoneuroendocrinology 36 (2011), 1040–1052.
39. Fuster, J.M., Bressler, S.L., Past makes future: role of pFC in prediction. J. Cogn. Neurosci. 27 (2015), 639–654.
40. Gonzalez, A., Jenkins, J.M., Steiner, M., Fleming, A.S., The relation between early life adversity, cortisol awakening response and diurnal salivary cortisol levels in postpartum women. Psychoneuroendocrinology 34 (2009), 76–86.
41. Gottesman, II., Gould, T.D., The endophenotype concept in psychiatry: etymology and strategic intentions. Am. J. Psychiatry 160 (2003), 636–645.
42. Gunnar, M., Quevedo, K., The neurobiology of stress and development. Annu. Rev. Psychol. 58 (2007), 145–173.
43. Gustafsson, P.E., Anckarsater, H., Lichtenstein, P., Nelson, N., Gustafsson, P.A., Does quantity have a quality all its own? Cumulative adversity and up- and down-regulation of circadian salivary cortisol levels in healthy children. Psychoneuroendocrinology 35 (2010), 1410–1415.
44. Hidalgo, V., Almela, M., Pulopulos, M.M., Salvador, A., Memory performance is related to the cortisol awakening response in older people, but not to the diurnal cortisol slope. Psychoneuroendocrinology 71 (2016), 136–146.
45. Inslicht, S.S., Otte, C., McCaslin, S.E., Apfel, B.A., Henn-Haase, C., Metzler, T., Yehuda, R., Neylan, T.C., Marmar, C.R., Cortisol awakening response prospectively predicts peritraumatic and acute stress reactions in police officers. Biol. Psychiatry 70 (2011), 1055–1062.
46. Izquierdo, A., Wellman, C.L., Holmes, A., Brief uncontrollable stress causes dendritic retraction in infralimbic cortex and resistance to fear extinction in mice. J. Neurosci. 26 (2006), 5733–5738.
47. Kidd, T., Carvalho, L.A., Steptoe, A., The relationship between cortisol responses to laboratory stress and cortisol profiles in daily life. Biol. Psychol. 99 (2014), 34–40.
48. Kim, H.Y., Statistical notes for clinical researchers: assessing normal distribution (2) using skewness and kurtosis. Restor Dent Endod 38 (2013), 52–54.
49. Klaus, K., Butler, K., Durrant, S. J., Ali, M., Inglehearn, C. F., Hodgson, T. L., Gutierrez, H. & Pennington, K. 2017. The effect of COMT Val158Met and DRD2 C957T polymorphisms on executive function and the impact of early life stress. Brain and Behavior, e00695-n/a.
50. Knouse, L.E., Barkley, R.A., Murphy, K.R., Does executive functioning (EF) predict depression in clinic-referred adults?. EF tests vs. rating scales. J Affect Disord 145 (2013), 270–275.
51. Kudielka, B.M., Kirschbaum, C., Awakening cortisol responses are influenced by health status and awakening time but not by menstrual cycle phase. Psychoneuroendocrinology 28 (2003), 35–47.
52. Kudielka, B.M., Kirschbaum, C., Sex differences in HPA axis responses to stress: a review. Biol. Psychol. 69 (2005), 113–132.
53. Kuhlman, K.R., Geiss, E.G., Vargas, I., Lopez-Duran, N.L., Differential associations between childhood trauma subtypes and adolescent HPA-axis functioning. Psychoneuroendocrinology 54 (2015), 103–114.
54. Kuhlman, K.R., Vargas, I., Geiss, E.G., Lopez-Duran, N.L., Age of trauma onset and HPA Axis Dysregulation among trauma-exposed youth. J. Trauma. Stress. 28 (2015), 572–579.
55. Law, R., Evans, P., Thorn, L., Hucklebridge, F., Clow, A., The cortisol awakening response predicts same morning executive function: results from a 50-day case study. Stress 18 (2015), 616–621.
56. Loman, M.M., Johnson, A.E., Westerlund, A., Pollak, S.D., Nelson, C.A., Gunnar, M.R., The effect of early deprivation on executive attention in middle childhood. J. Child Psychol. Psychiatry 54 (2013), 37–45.
57. Lupien, S.J., McEwen, B.S., Gunnar, M.R., Heim, C., Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat. Rev. Neurosci. 10 (2009), 434–445.
58. Maercker, A., Michael, T., Fehm, L., Becker, E.S., Margraf, J., Age of traumatisation as a predictor of post-traumatic stress disorder or major depression in young women. Br. J. Psychiatry 184 (2004), 482–487.
59. Mandelli, L., Petrelli, C., Serretti, A., The role of specific early trauma in adult depression: a meta-analysis of published literature. Childhood trauma and adult depression. Eur Psychiatry 30 (2015), 665–680.
60. McEwen, B.S., Stress, adaptation, and disease. Allostasis and allostatic load. Ann. N. Y. Acad. Sci. 840 (1998), 33–44.
61. McLaughlin, K.A., Conron, K.J., Koenen, K.C., Gilman, S.E., Childhood adversity, adult stressful life events, and risk of past-year psychiatric disorder: a test of the stress sensitization hypothesis in a population-based sample of adults. Psychol. Med. 40 (2010), 1647–1658.
62. McTeague, L.M., Goodkind, M.S., Etkin, A., Transdiagnostic impairment of cognitive control in mental illness. J. Psychiatr. Res. 83 (2016), 37–46.
63. Meinlschmidt, G., Heim, C., Decreased cortisol awakening response after early loss experience. Psychoneuroendocrinology 30 (2005), 568–576.
64. Mittal, C., Griskevicius, V., Simpson, J.A., Sung, S., Young, E.S., Cognitive adaptations to stressful environments: when childhood adversity enhances adult executive function. J. Pers. Soc. Psychol. 109 (2015), 604–621.
65. Monahan, K.C., King, K.M., Shulman, E.P., Cauffman, E., Chassin, L., The effects of violence exposure on the development of impulse control and future orientation across adolescence and early adulthood: time-specific and generalized effects in a sample of juvenile offenders. Dev. Psychopathol. 27 (2015), 1267–1283.
66. Moriarty, A.S., Bradley, A.J., Anderson, K.N., Watson, S., Gallagher, P., McAllister-Williams, R.H., Cortisol awakening response and spatial working memory in man: a U-shaped relationship. Hum Psychopharmacol 29 (2014), 295–298.
67. Pechtel, P., Pizzagalli, D.A., Effects of early life stress on cognitive and affective function: an integrated review of human literature. Psychopharmacology 214 (2011), 55–70.
68. Pechtel, P., Lyons-Ruth, K., Anderson, C.M., Teicher, M.H., Sensitive periods of amygdala development: the role of maltreatment in preadolescence. NeuroImage 97 (2014), 236–244.
69. Peng, H., Long, Y., Li, J., Guo, Y., Wu, H., Yang, Y., Ding, Y., He, J., Ning, Y., Hypothalamic-pituitary-adrenal axis functioning and dysfunctional attitude in depressed patients with and without childhood neglect. BMC Psychiatry, 14, 2014, 45.
70. Pennebaker, J.W., Susman, J.R., Disclosure of traumas and psychosomatic processes. Soc. Sci. Med. 26 (1988), 327–332.
71. Pruessner, J.C., Wolf, O.T., Hellhammer, D.H., Buske-Kirschbaum, A., von Auer, K., Jobst, S., Kaspers, F., Kirschbaum, C., Free cortisol levels after awakening: a reliable biological marker for the assessment of adrenocortical activity. Life Sci. 61 (1997), 2539–2549.
72. Read, J., Perry, B.D., Moskowitz, A., Connolly, J., The contribution of early traumatic events to schizophrenia in some patients: a traumagenic neurodevelopmental model. Psychiatry 64 (2001), 319–345.
73. Romens, S.E., McDonald, J., Svaren, J., Pollak, S.D., Associations between early life stress and gene methylation in children. Child Dev. 86 (2015), 303–309.
74. Roskar, S., Zorko, M., Bucik, V., Marusic, A., Problem solving for depressed suicide attempters and depressed individuals without suicide attempt. Psychiatr. Danub. 19 (2007), 296–302.
75. Sheikh, M.A., Abelsen, B., Olsen, J.A., Clarifying associations between childhood adversity, social support, behavioral factors, and mental health, health, and well-being in adulthood: a population-based study. Front. Psychol., 7, 2016, 727.
76. Stalder, T., Kirschbaum, C., Kudielka, B.M., Adam, E.K., Pruessner, J.C., Wust, S., Dockray, S., Smyth, N., Evans, P., Hellhammer, D.H., Miller, R., Wetherell, M.A., Lupien, S.J., Clow, A., Assessment of the cortisol awakening response: expert consensus guidelines. Psychoneuroendocrinology 63 (2016), 414–432.
77. Teicher, M.H., Andersen, S.L., Polcari, A., Anderson, C.M., Navalta, C.P., Kim, D.M., The neurobiological consequences of early stress and childhood maltreatment. Neurosci. Biobehav. Rev. 27 (2003), 33–44.
78. Teicher, M.H., Dumont, N.L., Ito, Y., Vaituzis, C., Giedd, J.N., Andersen, S.L., Childhood neglect is associated with reduced corpus callosum area. Biol. Psychiatry 56 (2004), 80–85.
79. Tiemeier, H., Lenroot, R.K., Greenstein, D.K., Tran, L., Pierson, R., Giedd, J.N., Cerebellum development during childhood and adolescence: a longitudinal morphometric MRI study. NeuroImage 49 (2010), 63–70.
80. Veen, G., van Vliet, I.M., DeRijk, R.H., Giltay, E.J., van Pelt, J., Zitman, F.G., Basal cortisol levels in relation to dimensions and DSM-IV categories of depression and anxiety. Psychiatry Res. 185 (2011), 121–128.
81. Vreeburg, S.A., Kruijtzer, B.P., van Pelt, J., van Dyck, R., DeRijk, R.H., Hoogendijk, W.J., Smit, J.H., Zitman, F.G., Penninx, B.W., Associations between sociodemographic, sampling and health factors and various salivary cortisol indicators in a large sample without psychopathology. Psychoneuroendocrinology 34 (2009), 1109–1120.
82. Williams, L.M., Debattista, C., Duchemin, A.M., Schatzberg, A.F., Nemeroff, C.B., Childhood trauma predicts antidepressant response in adults with major depression: data from the randomized international study to predict optimized treatment for depression. Transl. Psychiatry, 6, 2016, e799.
83. Wust, S., Wolf, J., Hellhammer, D.H., Federenko, I., Schommer, N., Kirschbaum, C., The cortisol awakening response - normal values and confounds. Noise Health 2 (2000), 79–88.
84. Zhang, L., Duan, H., Qin, S., Yuan, Y., Buchanan, T.W., Zhang, K., Wu, J., High cortisol awakening response is associated with impaired error monitoring and decreased post-error adjustment. Stress 18 (2015), 561–568.
85. Zigmond, A.S., Snaith, R.P., The hospital anxiety and depression scale. Acta Psychiatr. Scand. 67 (1983), 361–370.