Acute stress affects free recall and recognition of pictures differently depending on age and sex

Behavioural Brain Research

Volumn 292, Issue , 2015, Pages 393-402

  Hidalgo, Vanesa ^a   Pulopulos, Matias M ^a   Puig Perez, Sara ^a   Espin, Laura ^b   Gomez Amor, Jesus ^b   Salvador, Alicia ^a  

^a UNIVERSITY OF VALENCIA   (Spain)

^b UNIVERSITY OF MURCIA   (Spain)

Author keywords

Age; Alpha amylase; Cortisol; Memory retrieval; Sex; Stress

Indexed keywords

AMYLASE; HYDROCORTISONE; ALPHA AMYLASE SALIVA ISOENZYME;

ACUTE STRESS; ADULT; AGE; AGED; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; EMOTIONALITY; FEMALE; GENDER; HUMAN; HUMAN EXPERIMENT; HYDROCORTISONE RELEASE; LEARNING; LONG TERM MEMORY; MALE; MENTAL STRESS; MENTAL TASK; NORMAL HUMAN; PRIORITY JOURNAL; RECALL; RECOGNITION; STIMULUS RESPONSE; ACUTE DISEASE; METABOLISM; MIDDLE AGED; SEX DIFFERENCE;

ACUTE DISEASE; AGE FACTORS; AGED; FEMALE; HUMANS; HYDROCORTISONE; MALE; MENTAL RECALL; MIDDLE AGED; RECOGNITION (PSYCHOLOGY); SALIVARY ALPHA-AMYLASES; SEX FACTORS; STRESS, PSYCHOLOGICAL;

EID: 84937000080     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2015.07.011     Document Type: Article

References (77)

1. Lupien S.J., Lepage M. Stress, memory, and the hippocampus: can't live with it, can't live without it. Behav. Brain Res. 2001, 127:137-158. 10.1016/S0166-4328(01)00361-8.
2. Lupien S.J., Maheu F., Tu M., Fiocco A., Schramek T.E. The effects of stress and stress hormones on human cognition: Implications for the field of brain and cognition. Brain Cogn. 2007, 65:209-237. 10.1016/j.bandc.2007.02.007.
3. Roozendaal B., McEwen B.S., Chattarji S. Stress, memory and the amygdala. Nat Rev Neurosci. 2009, 10:423-433. 10.1038/nrn2651.
4. McGaugh J.L. Memory - A century of consolidation. Science 2000, 287:248-251. 10.1126/science.287.5451.248.
5. Packard M.G., Williams C.L., Cahill L., McGaugh J.L. The anatomy of a memory modulatory system: from periphery to brain. Neurobehavioral Plasticity: Learning, Development, and Response to Brain Insults 1995, 149-184. Erlbaum, Hillsdale. N.E. Spear, L.P. Spear, M.L. Woodruf (Eds.).
6. de Quervain D.J., Roozendaal B., Nitsch R.M., McGaugh J.L., Hock C. Acute cortisone administration impairs retrieval of long-term declarative memory in humans. Nat. Neurosci. 2000, 3:313-314. 10.1038/73873.
7. de Quervain D.J., Henke K., Aerni A., Treyer V., McGaugh J.L., Berthold T., Nitsch R.M., Buck A., Roozendaal B., Hock C. Glucocorticoid-induced impairment of declarative memory retrieval is associated with reduced blood flow in the medial temporal lobe. Eur. J. Neurosci. 2003, 17:1296-1302. 10.1046/j.1460-9568.2003.02542.
8. Kuhlmann S., Wolf O.T. Cortisol and memory retrieval in women: influence of menstrual cycle and oral contraceptives. Psychopharmacol. (Berl) 2005, 183:65-71. 10.1007/s00213-005-0143-z.
9. Kuhlmann S., Kirschbaum C., Wolf O.T. Effects of oral cortisol treatment in healthy young women on memory retrieval of negative and neutral words. Neurobiol. Learn. Mem. 2005, 83:158-162. 10.1016/j.nlm.2004.09.001.
10. Buchanan T.W., Tranel D., Adolphs R. Impaired memory retrieval correlates with individual differences in cortisol response but not autonomic response. Learn. Mem. 2006, 13:382-387. 10.1101/lm.206306.
11. Buchanan T.W., Tranel D. Stress and emotional memory retrieval: effects of sex and cortisol response. Neurobiol. Learn. Mem. 2008, 89:134-141. 10.1016/j.nlm.2007.07.003.
12. Domes G., Heinrichs M., Rimmele U., Reichwald U., Hautzinger M. Acute stress impairs recognition for positive words-association with stress-induced cortisol secretion. Stress 2004, 7:173-181. 10.1080/10253890412331273213.
13. Kuhlmann S., Piel M., Wolf O.T. Impaired memory retrieval after psychosocial stress in healthy young men. J. Neurosci. 2005, 25:2977-2982. 5139-04, 2005. 10.1523/JNEUROSCI.
14. Oei N.Y., Everaerd W.T., Elzinga B.M., van Well S., Bermond B. Psychosocial stress impairs working memory at high loads: an association with cortisol levels and memory retrieval. Stress 2006, 9:133-141. 10.1080/10253890600965773.
15. Smeets T., Otgaar H., Candel I., Wolf O.T. True or false? Memory is differentially affected by stress-induced cortisol elevations and sympathetic activity at consolidation and retrieval. Psychoneuroendocrinology 2008, 33:1378-1386. 10.1016/j.psyneuen.2008.07.009.
16. Smeets T. Acute stress impairs memory retrieval independent of time of day. Psychoneuroendocrinology 2011, 36:495-501. 10.1016/j.psyneuen.2010.08.001.
17. Schoofs D., Wolf O.T. Stress and memory retrieval in women: no strong impairing effect during the luteal phase. Behav. Neurosci. 2009, 123:547-554. 10.1037/a0015625.
18. Beckner V.E., Tucker D.M., Delville Y., Mohr D.C. Stress facilitates consolidation of verbal memory for a film but does not affect retrieval. Behav. Neurosci. 2006, 120:518-527. 10.1037/0735-7044.120.3.518.
19. Wolf O.T., Schommer N.C., Hellhammer D.H., Reischies F.M., Kirschbaum C. Moderate psychosocial stress appears not to impair recall of words learned 4 weeks prior to stress exposure. Stress 2002, 5:59-64. 10.1080/102538902900012332.
20. Wolf O.T., Kuhlmann S., Buss C., Hellhammer D.H., Kirschbaum C. Cortisol and memory retrieval in humans: influence of emotional valence. Ann. N. Y. Acad. Sci. 2004, 1032:195-197. 10.1196/annals.1314.019.
21. Mather M., Carstenesen L.L. Aging and motivated cognition: the positivity effect in attention and memory. Trends Cogn. Sci. 2005, 9:496-502. 10.1016/j.tics.2005.08.005.
22. Mather M. Why memories may become more positive as people age. Memory and emotion: Interdisciplinary perspectives 2006, 135-157. Blackwell, Malden. B. Uttl, A.L. Ohta (Eds.).
23. Murty V.P., Sambataro F., Das S., Tan H.Y., Callicott J.H., Goldberg T.E., Meyer-Lindenberg A., Weinberger D.R., Mattay V.S. Age-related alterations in simple declarative memory and the effect of negative stimulus valence. J. Cogn. Neurosci. 2009, 21:1920-1933. 10.1162/jocn.2009.21130.
24. St Jacques P.L., Dolcos F., Cabeza R. Effects of aging on functional connectivity of the amygdala for subsequent memory of negative pictures: a network analysis of functional magnetic resonance imaging data. Psychol. Sci. 2009, 20:74-84. 10.1111/j.1467-9280.2008.02258.
25. Giordano R., Bo M., Pellegrino M., Vezzari M., Baldi M., Picu A., Balvo M., Bonelli L., Migliaretti G., Ghigo E., Arvat E. Hypothalamus-pituitary-adrenal hyperactivity in human aging is partially refractory to stimulation by mineralocorticoid receptor blockade. J. Clin. Endocrinol. Metab. 2004, 90:5656-5662. http://dx.doi.org/10.1210/jc.2005-0105.
26. Mizoguchi K., Ikeda R., Shoji H., Tanaka Y., Maruyama W., Tabira T. Aging attenuates glucocorticoid negative feedback in rat brain. Neuroscience 2009, 159:259-270. 10.1016/j.neuroscience.2008.12.020.
27. Perlman W.R., Webster M.J., Herman M.M., Kleinman J.E., Weickert C.S. Age-related differences in glucocorticoid receptor mRNA levels in the human brain. Neurobiol. Aging 2007, 28:447-458. 10.1016/j.neurobiolaging.2006.01.010.
28. Heffelfinger A.K., Newcomer J.W. Glucocorticoid effects on memory function over the human life span. Dev. Psychopathol. 2001, 13:491-513.
29. Newcomer J.W., Selke G., Kelly A.K., Paras L., Craft S. Age-related differences in glucocorticoid effect on memory in human subjects. Behav. Neurosci. 1995, 21:161. 10.1016/j.neurobiolaging.2006.01.010.
30. Almela M., Hidalgo V., Villada C., Espin L., Gomez-Amor J., Salvador A. The impact of cortisol reactivity to acute stress on memory: sex differences in middle-aged people. Stress 2011, 14:117-127. 10.3109/10253890.2010.514671.
31. Hidalgo V., Almela M., Villada C., Salvador A. Acute stress impairs recall after interference in older people, but not in young people. Horm. Behav. 2014, 65:264-272. 10.1016/j.yhbeh.2013.12.017.
32. Lupien S.J., Gaudreau S., Tchiteya B.M., Maheu F., Sharma S., Nair N.P., Hauger R.L., McEwen B.S., Meaney M.J. Stress-induced declarative memory impairment in healthy elderly subjects: relationship to cortisol reactivity. J. Clin. Endocrinol. Metab. 1997, 82:2070-2075. http://dx.doi.org/10.1210/jcem.82.7.4075.
33. Wolf O.T., Convit A., McHugh P.F., Kandil E., Thorn E.L., De Santi S., McEwen B.S., de Leon M.J. Cortisol differentially affects memory in young and elderly men. Behav. Neurosci. 2001, 115:1002-1011. http://dx.doi.org/10.1037/0735-7044.115.5.1002.
34. Domes G., Heinrichs M., Reichwald U., Hautzinger M. Hypothalamic-pituitary-adrenal axis reactivity to psychological stress and memory in middle-aged women: high responders exhibit enhanced declarative memory performance. Psychoneuroendocrinology 2002, 27:843-853. 10.1016/S0306-4530(01)00085-3.
35. Buechel H.M., Popovic J., Staggs K.H., Anderson K.L., Thibault O., Blalock E. Aged rats are hyporesponsive to acute restraint: implications for psychosocial stress in aging. Front Aging Neurosci. 2014, 6:13. 10.3389/fnagi.2014.00013.
36. Porter R.J., Barnett N.A., Idey A., McGuckin E.A., O'Brien J.T. Effects of hydrocortisone administration on cognitive function in the elderly. J. Psychopharmacol. 2002, 16:65-71. 10.1177/026988110201600106.
37. Yehuda R., Harvey P.D., Buchsbaum M., Tischler L., Schmeidler J. Enhanced effects of cortisol administration on episodic and working memory in aging veterans with PTSD. Neuropsychopharmacology 2007, 32:2581-2591. 10.1038/sj.npp.1301380.
38. Pulopulos M.M., Hidalgo V., Almela M., Puig-Perez S., Villada C., Salvador A. Acute stress and working memory in older people. Stress 2015, in press. 10.3109/10253890.2015.1004538.
39. Pulopulos M.M., Almela M., Hidalgo V., Villada C., Puig-Perez S., Salvador A. Acute stress does not impair long-term memory retrieval in older people. Neurobiol. Learn Mem. 2013, 104C:16-24. 10.1016/j.nlm.2013.04.010.
40. Andreano J.M., Cahill L. Glucocorticoid release and memory consolidation in men and women. Psychol. Sci. 2006, 17:466-470. 10.1111/j.1467-9280.2006.01729.
41. Espin L., Almela M., Hidalgo V., Villada C., Salvador A., Gomez-Amor J. Acute pre-learning stress and declarative memory: impact of sex, cortisol response and menstrual cycle phase. Horm. Behav. 2013, 63:759-765. 10.1016/j.yhbeh.2013.03.013.
42. Wolf O.T., Schommer N.C., Hellhammer D.H., McEwen B.S., Kirschbaum C. The relationship between stress induced cortisol levels and memory differs between men and women. Psychoneuroendocrinology 2001, 26:711-720. 10.1016/S0306-4530(01)00025-7.
43. Kirschbaum C., Kudielka B.M., Gaab J., Schommer N.C., Hellhammer D.H. Impact of gender, menstrual cycle phase, and oral contraceptives on the activity of the hypothalamus-pituitary-adrenal axis. Psychosom. Med. 1999, 61:154-162. doi: 0033-3174/99/6102-0154.
44. Kudielka B.M., Kirschbaum C. Sex differences in HPA axis responses to stress: a review. Biol. Psychol. 2005, 69:113-132. 10.1016/j.biopsycho.2004.11.009.
45. Kudielka B.M., Hellhammer D.H., Wust S. Why do we respond so differently? Reviewing determinants of human salivary cortisol responses to challenge. Psychoneuroendocrinology 2009, 34:2-18. 10.1016/j.psyneuen.2008.10.004.
46. Wolf O.T. Effects of stress hormones on the structure and function of the human brain. Expert Rev. Endocrinol. Metab. 2006, 1:623-632. 10.1586/17446651.1.5.623.
47. Peavy G.M., Salmon D.P., Jacobson M.W., Hervey A., Gamst A.C., Wolfson T., Patterson T.L., Goldman S., Mills P.J., Khandrika S., Galasko D. Effects of chronic stress on memory decline in cognitively normal and mildly impaired older adults. Am. J. Psychiatry 2009, 166:1384-1391. 10.1176/appi.ajp.2009.09040461.
48. Sapolsky R.M., Plotsky P.M. Hypercortisolism and its possible neural bases. Biol. Psychiatry 1990, 27:937-952. 10.1016/0006-3223(90)90032-W.
49. Sauro M.D., Jorgensen R.S., Pedlow C.T. Stress, glucocorticoids, and memory: a meta-analytic review. Stress 2003, 6:235-245. 10.1080/10253890310001616482.
50. Lobo A., Saz P., Marcos G., Dia J.L., de la Camara C., Ventura T., Morales Asin F., Fernando Pascual L., Montanes J.A., Aznar S. Revalidation and standardization of the cognition mini-exam (first Spanish version of the Mini-Mental Status Examination) in the general geriatric population. Med. Clin. (Barc). 1999, 112:767-774.
51. Portet F., Ousset P.J., Visser P.J., Frisoni G.B., Nobili F., Scheltens P., Vellas B., Touchon J. MCI Working Group of the European Consortium on Alzheimer's Disease (EADC). Mild cognitive impairment (MCI) in medical practice: a critical review of the concept and new diagnostic procedure. Report of the MCI Working Group of the European Consortium on Alzheimer's Disease. J. Neurol. Neurosurg. Psychiatry 2006, 77:714-718. 10.1136/jnnp.2005.085332.
52. Vila J., Sánchez M., Ramírez I., Fernández M.C., Cobos P., Rodríguez S., Muñoz M.A., Tormo M.P., Herrero M., Segarra P., Pastor M.C., Montañes S., Moltó J., Poy R. El sistema internacional de imágenes afectivas (IAPS): adaptación española. Segunda Parte. Rev de Psicol Gral y Aplic 2001, 54:635-657.
53. P.J. Lang, M.M. Bradley, B.N. Cuthbert, International Affective Picture System (IAPS): Affective ratings of pictures and instruction manual, University of Florida: Technical Report A-6. Gainesville; 2005.
54. Lang P.J. Behavioral treatment and bio-behavioral assessment: Computer applications. Technology in mental health care delivery systems 1980, 119-137. Ablex, Norwood. J.B. Sidowski, J.H. Johnson, T.A. Williams (Eds.).
55. Kirschbaum C., Pirke K.M., Hellhammer D.H. The 'Trier Social Stress Test'-a tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology 1993, 81:76. 10.1159/000119004.
56. Almela M., Hidalgo V., Villada C., van der Meij L., Espin L., Gomez-Amor J., Salvador A. Salivary alpha-amylase response to acute psychosocial stress: the impact of age. Biol. Psychol. 2011, 87:421-429. 10.1016/j.biopsycho.2011.05.008.
57. Dickerson S.S., Kemeny M.E. Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychol. Bull. 2004, 130:355-391. 10.1037/0033-2909.130.3.355.
58. Baggert H.L., Saab P.G., Carver C.S. Appraisal, coping, task performance, and cardiovascular responses during the evaluated speaking task. Pers. Soc. Psychol. Bull. 1996, 22:483-494. 10.1177/0146167296225006.
59. Gonzalez-Bono E., Moya-Albiol L., Salvador A., Carrillo E., Ricarte J., Gomez-Amor J. Anticipatory autonomic response to a public speaking task in women: the role of trait anxiety. Biol. Psychol. 2002, 60:37-49. 10.1016/S0301-0511(02)00008-X.
60. Sandín B., Chorot P., Lostao L., Joiner T.E., Santed M.A. Valiente RM. The PANAS scales of positive and negative affect: factor analytic validation and cross-cultural convergence. Psicothema 1999, 11:37-51.
61. Watson D., Clark L.A., Tellegen A. Development and validation of brief measures of positive and negative affect: The PANAS scales. J. Pers. Soc. Psychol. 1988, 1070:1063. 10.1037/0022-3514.54.6.1063.
62. Cornelisse S., van Stegeren A.H., Joëls M. Implications of psychosocial stress on memory formation in a typical male versus female student sample. Psychoneuroendocrinology 2011, 36:569-578. 10.1016/j.psyneuen.2010.09.002.
63. Seals D.R., Dinenno F.A. Collateral damage: cardiovascular consequences of chronic sympathetic activation with human aging. Am. J. Physiol. Heart Circ. Physiol. 2004, 287:H1895-H1905. 10.1152/ajpheart.00486.2004.
64. Kivlighan K.T., Granger D.A. Salivary alpha-amylase response to competition: relation to gender, previous experience, and attitudes. Psychoneuroendocrinology 2006, 31:703-714. 10.1016/j.psyneuen.2006.01.007.
65. Takai N., Yamaguchi M., Aragaki T., Eto K., Uchihashi K., Nishikawa Y. Gender-specific differences in salivary biomarker responses to acute psychological stress. Ann. N. Y. Acad. Sci. 2007, 1098:510-515. 10.1196/annals.1384.014.
66. Kudielka B.M., Schmidt-Reinwald A.K., Hellhammer D.H., Kirschbaum C. Psychological and endocrine responses to psychosocial stress and dexamethasone/corticotropin-releasing hormone in healthy postmenopausal women and young controls: the impact of age and a two-week estradiol treatment. Neuroendocrinology 1999, 70:422-430. 10.1159/000054504.
67. Kudielka B.M., Schmidt-Reinwald A.K., Hellhammer D.H., Schürmeyer T., Kirschbaum C. Psychosocial stress and HPA functioning: no evidence for a reduced resilience in healthy elderly men. Stress 2000, 3:229-240.
68. Nicolson N., Storms C., Ponds R., Sulon J. Salivary cortisol levels and stress reactivity in human aging. J. Gerontol. A Biol. Sci. Med. Sci. 1997, 52:M68-M75. 10.1093/gerona/52A.2.
69. Kudielka B.M., Buske-Kirschbaum A., Hellhammer D.H., Kirschbaum C. HPA axis responses to laboratory psychosocial stress in healthy elderly adults, younger adults, and children: impact of age and gender. Psychoneuro. Endocrinology 2004, 29:83-98. 10.1016/S0306-4530(02)00146-4.
70. Bhatnagari M., Cintra A., Chadi G., Lindberg J., Oitzl M., De Kloet E.R., Moller A., Agnati L.F., Fuxe K. Neurochemical changes in the hippocampus of the brown Norway rat during aging. Neurobiol. Aging 1997, 18:319-327. 10.1016/S0197-4580(97)80314-4.
71. Schwabe L., Romer S., Richter S., Dockendorf S., Bilak B., Schachinger H. Stress effects on declarative memory retrieval are blocked by a beta-adrenoceptor antagonist in humans. Psychoneuroendocrinology 2009, 34:446-454. 10.1016/j.psyneuen.2008.10.009.
72. Roozendaal B. Stress and memory: opposing effects of glucocorticoids on memory consolidation and memory retrieval. Neurobiol. Learn. Mem. 2002, 78:578-595. 10.1006/nlme.2002.4080.
73. Joëls M., Pu Z., Wiegert O., Oitzl M.S., Krugers H.J. Learning under stress: how does it work?. Trends Cog Sci 2006, 10:152-158. 10.1016/j.tics.2006.02.002.
74. Mandler G. Recognizing the judgment of previous occurrence. Psychol. Rev. 1980, 87:252-271. 10.1037/0033-295X.87.3.252.
75. Squire L.R., Wixted J.T., Clark R.E. Recognition memory and the medial temporal lobe: a new perspective. Nat. Rev. Neurosci. 2007, 8:872-883. 10.1038/nrn2154.
76. Brown M.W., Aggleton J.P. Recognition memory: what are the roles of the perirhinal cortex and hippocampus?. Nat. Rev. Neurosci. 2001, 2:51-61. 10.1038/35049064.
77. Park H.L., O'Connell J.E., Thomson R.G. A systematic review of cognitive decline in the general elderly population. Int. J. Geriatr. Psychiatry 2003, 18:1121-1134. 10.1002/gps.1023.