Psychiatry Research: Neuroimaging
Volume 155, Issue 1 , Pages 1-10 , 15 May 2007

The associations among hippocampal volume, cortisol reactivity, and memory performance in healthy young men

  • Marita Pruessner

      Affiliations

    • Prevention and Early Intervention Program for Psychoses, Douglas Hospital Research Center, 6875 Boulevard LaSalle, Verdun, Montreal, Quebec, Canada H4H 1R3
    • Center for Studies on Human Stress, Douglas Hospital Research Center, McGill University, 6875 Boulevard LaSalle, Verdun, Montreal, Quebec, Canada H4H 1R3
    • Corresponding Author InformationCorresponding author. Prevention and Early Intervention Program for Psychoses, Douglas Hospital Research Center, Wilson Pavilion, 6875 Boulevard LaSalle, Montreal, Quebec, Canada H4H 1R3. Tel.: +1 514 761 6131x3381; fax: +1 514 888 4458.
    • ,
  • Jens C. Pruessner

      Affiliations

    • Center for Studies on Human Stress, Douglas Hospital Research Center, McGill University, 6875 Boulevard LaSalle, Verdun, Montreal, Quebec, Canada H4H 1R3
    • ,
  • Dirk H. Hellhammer

      Affiliations

    • Center for Psychobiological and Psychosomatic Research, University of Trier, Johanniterufer 15, 54290 Trier, Germany
    • ,
  • G. Bruce Pike

      Affiliations

    • McConnell Brain Imaging Centre, Montréal Neurological Institute, McGill University, 3801 University Street, Montreal, Quebec, Canada H3A 2B4
    • ,
  • Sonia J. Lupien

      Affiliations

    • Center for Studies on Human Stress, Douglas Hospital Research Center, McGill University, 6875 Boulevard LaSalle, Verdun, Montreal, Quebec, Canada H4H 1R3

Received 22 April 2006 ,Revised 20 October 2006 ,Accepted 23 December 2006.

References 

  1. Andreano JM, Cahill L. Glucocorticoid release and memory consolidation in men and women. Psychological Science. 2006;17:466–470
  2. Basso M, Yang J, Warren L, MacAvoy MG, Varma P, Bronen RA, et al. Volumetry of amygdala and hippocampus and memory performance in Alzheimer's disease. Psychiatry Research. Neuroimaging. 2006;146:251–261
  3. Bohbot VD, Kalina M, Stepankova K, Spackova N, Petrides M, Nadel L. Spatial memory deficits in patients with lesions to the right hippocampus and to the right parahippocampal cortex. Neuropsychologia. 1998;36:1217–1238
  4. Buchanan TW, Lovallo WR. Enhanced memory for emotional material following stress-level cortisol treatment in humans. Psychoneuroendocrinology. 2001;26(3):307–317
  5. Buchanan TW, Kern S, Allen JS, Tranel D, Kirschbaum C. Circadian regulation of cortisol after hippocampal damage in humans. Biological Psychiatry. 2004;56:651–656
  6. Buchanan TW, Tranel D, Adolphs R. Impaired memory retrieval correlates with individual differences in cortisol response but not autonomic response. Learning and Memory. 2006;13(3):382–387
  7. Cahill L, Gorski L, Le K. Enhanced human memory consolidation with post-learning stress: interaction with the degree of arousal at encoding. Learning and Memory. 2003;10:270–274
  8. Chantome M, Perruchet P, Hasboun D, Dormont D, Sahel M, Sourour N, et al. Is there a negative correlation between explicit memory and hippocampal volume?. NeuroImage. 1999;10:589–595
  9. Cho K. Chronic ‘jet lag’ produces temporal lobe atrophy and spatial cognitive deficits. Nature Neuroscience. 2001;4:567–568
  10. Collins DL, Neelin P, Peters TM, Evans AC. Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. Journal of Computer Assisted Tomography. 1994;18:192–205
  11. Corcoran C, Walker E, Huot R, Mittal V, Tessner K, Kestler L, et al. The stress cascade and schizophrenia: etiology and onset. Schizophrenia Bulletin. 2003;29:671–692
  12. De Bellis MD, Hall J, Boring AM, Frustaci K, Moritz G. A pilot longitudinal study of hippocampal volumes in pediatric maltreatment-related posttraumatic stress disorder. Biological Psychiatry. 2001;50:305–309
  13. De Kloet ER, Vreugdenhil E, Oitzl MS, Joels M. Brain corticosteroid receptor balance in health and disease. Endocrine Reviews. 1998;19:269–301
  14. De Kloet ER, Oitzl MS, Joels M. Stress and cognition: are corticosteroids good or bad guys?. Trends in Neurosciences. 1999;22:422–426
  15. De Quervain DJ, Roozendaal B, McGaugh JL. Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature. 1998;394(6695):787–790
  16. De Quervain DJ, Roozendaal B, Nitsch RM, McGaugh JL, Hock C. Acute cortisone administration impairs retrieval of long-term declarative memory in humans. Nature Neuroscience. 2000;3(4):313–314
  17. De Quervain DJ, Henke K, Aerni A, Treyer V, McGaugh JL, Berthold T, et al. Glucocorticoid-induced impairment of declarative memory retrieval is associated with reduced blood flow in the medial temporal lobe. European Journal of Neuroscience. 2003;17(6):1296–1302
  18. Dickerson SS, Kemeny ME. Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychological Bulletin. 2004;130:355–391
  19. Dressendorfer RA, Kirschbaum C, Rohde W, Stahl F, Strasburger CJ. Synthesis of a cortisol-biotin conjugate and evaluation as a tracer in an immunoassay for salivary cortisol measurement. Journal of Steroid Biochemistry and Molecular Biology. 1992;43:683–692
  20. Eichenbaum H. The hippocampus and mechanisms of declarative memory. Behavioural Brain Research. 1999;103:123–133
  21. Foster JK, Meikle A, Goodson G, Mayes AR, Howard M, Sunram SI, et al. The hippocampus and delayed recall: bigger is not necessarily better?. Memory. 1999;7:715–732
  22. Gilbertson MW, Shenton ME, Ciszewski A, Kasai K, Lasko NB, Orr SP, et al. Smaller hippocampal volume predicts pathologic vulnerability to psychological trauma. Nature Neuroscience. 2002;5:1242–1247
  23. Goldstein JM, Seidman LJ, Horton NJ, Makris N, Kennedy DN, Caviness VS, et al. Normal sexual dimorphism of the adult human brain assessed by in vivo magnetic resonance imaging. Cerebral Cortex. 2001;11:490–497
  24. Good CD, Johnsrude IS, Ashburner J, Henson RN, Friston KJ, Frackowiak RS. A voxel-based morphometric study of ageing in 465 normal adult human brains. NeuroImage. 2001;14:21–36
  25. Gould E, Tanapat P. Stress and hippocampal neurogenesis. Biological Psychiatry. 1999;46:1472–1479
  26. Gur RC, Mozley PD, Resnick SM, Gottlieb GL, Kohn M, Zimmerman R, et al Gender differences in age effect on brain atrophy measured by magnetic resonance imaging. Proceedings of the National Academy of Sciences of the United States of America. 1991;88:2845–2849
  27. Handelmann GE, Olton DS. Spatial memory following damage to hippocampal CA3 pyramidal cells with kainic acid: impairment and recovery with preoperative training. Brain Research. 1981;217:41–58
  28. Het S, Ramlow G, Wolf OT. A meta-analytic review of the effects of acute cortisol administration on human memory. Psychoneuroendocrinology. 2005;30:771–784
  29. Jacobson L, Sapolsky R. The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endocrine Reviews. 1991;12:118–134
  30. Kamber M, Shinghal R, Collins DL, Francis GS, Evans AC. Model-based 3-D segmentation of multiple sclerosis lesions in magnetic resonance brain images. IEEE Transactions on Medical Imaging. 1995;14:442–453
  31. Kirschbaum C, Wolf OT, May M, Wippich W, Hellhammer DH. Stress- and treatment-induced elevations of cortisol levels associated with impaired declarative memory in healthy adults. Life Sciences. 1996;58:1475–1483
  32. Kirschbaum C, Kudielka BM, Gaab J, Schommer NC, Hellhammer DH. Impact of gender, menstrual cycle phase, and oral contraceptives on the activity of the hypothalamus–pituitary–adrenal axis. Psychosomatic Medicine. 1999;61:154–162
  33. Leverenz JB, Wilkinson CW, Wamble M, Corbin S, Grabber JE, Raskind MA, et al. Effect of chronic high-dose exogenous cortisol on hippocampal neuronal number in aged nonhuman primates. Journal of Neuroscience. 1999;19:2356–2361
  34. Lupien SJ, Lepage M. Stress, memory, and the hippocampus: can't live with it, can't live without it. Behavioral Brain Research. 2001;127:137–158
  35. Lupien SJ, McEwen BS. The acute effects of corticosteroids on cognition: integration of animal and human model studies. Brain Research Brain Research Reviews. 1997;24:1–27
  36. Lupien S, Lecours AR, Lussier I, Schwartz G, Nair NP, Meaney MJ. Basal cortisol levels and cognitive deficits in human aging. Journal of Neuroscience. 1994;14:2893–2903
  37. Lupien SJ, Gaudreau S, Tchiteya BM, Maheu F, Sharma S, Nair NP, et al. Stress-induced declarative memory impairment in healthy elderly subjects: relationship to cortisol reactivity. Journal of Clinical Endocrinology and Metabolism. 1997;82:2070–2075
  38. Lupien SJ, de Leon M, de Santi S, Convit A, Tarshish C, Nair NP, et al. Cortisol levels during human aging predict hippocampal atrophy and memory deficits. Nature Neuroscience. 1998;1:69–73
  39. Lupien SJ, Gillin CJ, Hauger RL. Working memory is more sensitive than declarative memory to the acute effects of corticosteroids: a dose-response study in humans. Behavioral Neuroscience. 1999;113:420–430
  40. Lupien SJ, Wilkinson CW, Briere S, Menard C, Ng Ying Kin NM, Nair NP. The modulatory effects of corticosteroids on cognition: studies in young human populations. Psychoneuroendocrinology. 2002;27:401–416
  41. Lupien SJ, Wilkinson CW, Briere S, Ng Ying Kin NM, Meaney MJ, Nair NP. Acute modulation of aged human memory by pharmacological manipulation of glucocorticoids. Journal of Clinical Endocrinology and Metabolism. 2002;87:3798–3807
  42. Maheu FS, Joober R, Beaulieu S, Lupien SJ. Differential effects of adrenergic and corticosteroid hormonal systems on human short- and long-term declarative memory for emotionally arousing material. Behavioral Neuroscience. 2004;118:420–428
  43. Maheu FS, Collicutt P, Kornik R, Moszkowski R, Lupien SJ. The perfect time to be stressed: a differential modulation of human memory by stress applied in the morning or in the afternoon. Progress in Neuro-Psychopharmacology & Biological Psychiatry. 2005;29:1281–1288
  44. Mason JW. A review of psychoendocrine research on the pituitary–adrenal cortical system. Psychosomatic Medicine. 1968;30:576–607(Suppl)
  45. Milner B. Disorders of learning and memory after temporal lobe lesions in man. Clinical Neurosurgery. 1972;19:421–446
  46. O'Brien JT, Ames D, Schweitzer I, Colman P, Desmond P, Tress B. Clinical and magnetic resonance imaging correlates of hypothalamic–pituitary–adrenal axis function in depression and Alzheimer's disease. British Journal of Psychiatry. 1996;168:679–687
  47. Petersen RC, Jack CR, Xu YC, Waring SC, O'Brien PC, Smith GE, et al. Memory and MRI-based hippocampal volumes in aging and AD. Neurology. 2000;54:581–587
  48. Pruessner JC, Hellhammer DH, Kirschbaum C. Burnout, perceived stress, and cortisol responses to awakening. Psychosomatic Medicine. 1999;61:197–204
  49. Pruessner JC, Li LM, Serles W, Pruessner M, Collins DL, Kabani N, et al. Volumetry of hippocampus and amygdala with high-resolution MRI and three-dimensional analysis software: minimizing the discrepancies between laboratories. Cerebral Cortex. 2000;10:433–442
  50. Pruessner JC, Collins DL, Pruessner M, Evans AC. Age and gender predict volume decline in the anterior and posterior hippocampus in early adulthood. Journal of Neuroscience. 2001;21:194–200
  51. Pruessner M, Hellhammer DH, Pruessner JC, Lupien SJ. Self-reported depressive symptoms and stress levels in healthy young men: associations with the cortisol response to awakening. Psychosomatic Medicine. 2003;65:92–99
  52. Pruessner JC, Kirschbaum C, Meinlschmidt G, Hellhammer DH. Two formulas for the computation of the area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroendocrinology. 2003;28:916–931
  53. Pruessner JC, Baldwin MW, Dedovic K, Renwick R, Mahani NK, Lord C, et al. Self-esteem, locus of control, hippocampal volume, and cortisol regulation in young and old adulthood. NeuroImage. 2005;28(4):815–826
  54. Reagan LP, McEwen BS. Controversies surrounding glucocorticoid-mediated cell death in the hippocampus. Journal of Chemical Neuroanatomy. 1997;13:149–167
  55. Reul JM, de Kloet ER. Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology. 1985;117:2505–2511
  56. Roozendaal B. Stress and memory: opposing effects of glucocorticoids on memory consolidation and memory retrieval. Neurobiology of Learning and Memory. 2002;78:578–595
  57. Sanchez MM, Young LJ, Plotsky PM, Insel TR. Distribution of corticosteroid receptors in the rhesus brain: relative absence of glucocorticoid receptors in the hippocampal formation. Journal of Neuroscience. 2000;20:4657–4668
  58. Sapolsky RM. Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders. Archives of General Psychiatry. 2000;57:925–935
  59. Sapolsky RM. Stress hormones: good and bad. Neurobiology of Disease. 2000;7:540–542
  60. Sapolsky RM, Krey LC, McEwen BS. The neuroendocrinology of stress and aging: the glucocorticoid cascade hypothesis. Endocrine Reviews. 1986;7:284–301
  61. Sapolsky RM, Romero LM, Munck AU. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews. 2000;21:55–89
  62. Schulz P, Kirschbaum C, Pruessner J, Hellhammer D. Increased free cortisol secretion after awakening in chronically stressed individuals due to work overload. Stress Medicine. 1998;14:91–97
  63. Scoville WB, Milner B. Loss of recent memory after bilateral hippocampal lesions. Journal of Neuropsychiatry and Clinical Neurosciences. 1957;12:103–113
  64. Selye H. A syndrome produced by diverse noxious agents. In: Nature. 1936;p. 138
  65. Sheline YI, Wang PW, Gado MH, Csernansky JG, Vannier MW. Hippocampal atrophy in recurrent major depression. Proceedings of the National Academy of Sciences. 1996;93:3908–3913
  66. Sled JG, Zijdenbos AP, Evans AC. A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Transactions on Medical Imaging. 1998;17:87–97
  67. Squire LR. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychological Review. 1992;99:195–231
  68. Starkman MN, Gebarski SS, Berent S, Schteingart DE. Hippocampal formation volume, memory dysfunction, and cortisol levels in patients with Cushing's syndrome. Biological Psychiatry. 1992;32:756–765
  69. Talairach J, Tournoux P. Co-planar stereotaxic atlas of the human brain. 3-Dimensional Proportional System: an Approach to Cerebral Imaging. New York: Thieme; 1988;
  70. Thomas L. Labor and Diagnose: Indikation und Bewertung von Laborbefunden für die medizinische Diagnostik. Marburg: Medizinische Verlags Gesellschaft; 1992;
  71. Tuvnes FA, Steffenach HA, Murison R, Moser MB, Moser EI. Selective hippocampal lesions do not increase adrenocortical activity. Journal of Neuroscience. 2003;23:4345–4354
  72. Van Petten C. Relationship between hippocampal volume and memory ability in healthy individuals across the lifespan: review and meta-analysis. Neuropsychologia. 2004;42:1394–1413
  73. Walker EF, Diforio D. Schizophrenia: a neural diathesis-stress model. Psychological Review. 1997;104:667–685
  74. Wiedenmayer CP, Bansal R, Anderson GM, Zhu H, Amat J, Whiteman R, et al. Cortisol levels and hippocampus volumes in healthy preadolescent children. Biological Psychiatry. 2006;60(8):856–861
  75. Wolf OT, Convit A, de Leon MJ, Caraos C, Qadri SF. Basal hypothalamo–pituitary–adrenal axis activity and corticotropin feedback in young and older men: relationships to magnetic resonance imaging-derived hippocampus and cingulate gyrus volumes. Neuroendocrinology. 2002;75:241–249
  76. Wolf OT, Fujiwara E, Luwinski G, Kirschbaum C, Markowitsch HJ. No morning cortisol response in patients with severe global amnesia. Psychoneuroendocrinology. 2005;30:101–105
  77. Wolkowitz OM, Reus VI, Weingartner H, Thompson K, Breier A, Doran A, et al. Cognitive effects of corticosteroids. American Journal of Psychiatry. 1990;147:1297–1303
  78. Wust S, Federenko I, Hellhammer DH, Kirschbaum C. Genetic factors, perceived chronic stress, and the free cortisol response to awakening. Psychoneuroendocrinology. 2000;25:707–720
  79. Zijdenbos AP, Forghani R, Evans AC. Automatic ‘pipeline’ analysis of 3D MRI data for clinical trials: application to multiple sclerosis. IEEE Transactions on Medical Imaging. 2002;21:1280–1291

PII: S0925-4927(07)00004-2

doi: 10.1016/j.pscychresns.2006.12.007

Psychiatry Research: Neuroimaging
Volume 155, Issue 1 , Pages 1-10 , 15 May 2007

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