Psychoneuroendocrinology
Volume 34, Issue 9 , Pages 1263-1271 , October 2009

Endogenous noradrenergic activation and memory for emotional material in men and women

Received 29 July 2008 ,Revised 15 April 2009 ,Accepted 30 April 2009.

References 

  1. Andreano J, Cahill L. Glucocorticoid release and memory consolidation in men and women. Psychological Science. 2006;17(6):466–470
  2. Andreano JM, Arjomandi H, Cahill L. Menstrual cycle modulation of the relationship between cortisol and long-term memory. Psychoneuroendocrinology. 2008;33:874–882
  3. Bradley M, Greenwald M, Petry M, Lang P. Remembering pictures: pleasure and arousal in memory. Journal of Experimental Psychology: Learning, Memory, and, Cognition. 1992;18(2):379–390
  4. Buchanan T, Lovallo W. Enhanced memory for emotional material following stress-level cortisol treatment in humans. Psychoneuroendocrinology. 2001;26:307–317
  5. Cahill L. Sex- and hemisphere-related influences on the neurobiology of emotionally influenced memory. Progress in neuropsychopharmacology and biological psychology. 2003;27(8):1235–1241
  6. Cahill L. Sex-related influences on the neurobiology of emotionally influenced memory. Annals of New York Academy of Science. 2003;985:163–173
  7. Cahill L, Alkire M. Epinephrine enhancement of human memory consolidation: interaction with arousal at encoding. Neurobiology of Learning and Memory. 2003;79:194–198
  8. Cahill L, vanStegeren A. Sex-related impairment of memory for emotional events with β-adrenergic blockade. Neurobiology of Learning and Memory. 2003;81–88
  9. Cahill L, Prins B, Weber M, McGaugh J. Beta-adrenergic activation and memory for emotional events. Nature. 1994;371(20):702–704
  10. Cahill L, Pham CA, Setlow B. Impaired memory consolidation in rats produced with β-adrenergic blockade. Neurobiology of Learning and Memory. 2000;74:259–266
  11. Canli T, Desmond J, Zhao Z, Gabrieli J. Sex differences in the neural basis of emotional memories. Proceedings of the National Academy of Sciences United States of America. 2002;99(16):10789–10794
  12. Cahill L, Uncapher M, Kilpatrick L, Alkire MT. Sex-related hemispheric lateralization of amygdala function in emotionally influence memory: an fMRI investigation. Learning and Memory. 2004;11(3):261–266
  13. Castle D, Castle A. Intracellular transport and secretion of salivary proteins. Critical Reviews in Oral Biology & Medicine. 1998;9(1):4–22
  14. Chatterton RTJ, Vogelsong KM, Lu YC, Ellman AB, Hudgens GA. Salivary alpha-amylase as a measure of endogenous adrenergic activity. Clinical Physiology. 1996;16:433–448
  15. Clayton E, Williams C. Adrenergic activation of the nucleus tractus solitaries potentiates amygdale norepinephrine release and enhances retention performance in emotionally arousing and spatial memory tasks. Behavioral Brain Research. 2000;112:151–158
  16. Dolcos F, LaBar K, Cabeza R. Remembering one year later: role of the amygdala and the medial temporal lobe memory system in retrieving emotional memories. PNAS. 2004;102(7):2626–2631
  17. Ehlert U, Erni K, Hebisch G, Nater U. Salivary α-amylase levels after yohimbine challenge in healthy men. The Journal of Clinical Endocrinology and Metabolism. 2006;91(12):5130–5133
  18. Ferry B, Roozendaal B, McGaugh JL. Role of norepinephrine in mediating stress hormone regulation of long-term memory storage: a critical involvement of the amgygdala. Biological Psychiatry. 1999;46:1140–1152
  19. Gallacher DV, Peterson OH. Stimulus-secretion coupling in mammalian salivary glands. International Review of Physiology. 1983;28:1–52
  20. Gallagher M, Kapp BS, Musty RE, Driscoll PA. Memory formation: evidence for a specific neurochemical system in the amygdala. Science. 1977;198:423–425
  21. Gallagher M, Knapp BS. Effect of phentolamine administration into the amygdala complex of rats on time-dependent memory processes. Behavioral Neural Biology. 1981;1:90–95
  22. Galvez R, Mesches M, McGaugh JL. Norepinephrine release in the amygdala response to footshock stimulation. Neurobiology of Learning and Memory. 1996;66:253–257
  23. Hatfield T, McGaugh JL. Norepinephrine infused into the basolateral amygdala posttraining enhances retention in a spatial water maze task. Neurobiology of Learning and Memory. 1999;71(2):232–239
  24. Hubert W, de Jong-Meyer R. Emotional stress and saliva cortisol response. Journal of Clinical Chemistry and Clinical Biochemistry. 1991;27(4):235–237
  25. Introini-Collison IB, Miyazaki B, McGaugh JL. Involvement of the amygdala in the memory enhancing effects of clenbuterol. Pharmacology. 1991;104:541–544
  26. Introini-Collison IB, Castellano C, McGaugh JL. Interaction of GABAergic and beta-noradrenergic drugs in the regulation of memory storage. Behavioral Brain Research. 1994;61(2):150–155
  27. Kensinger E, Corkin S. Two routes to emotional memory: distinct neural processes for valence and arousal. PNAS. 2003;101(9):3310–3315
  28. Kuhlman S, Wolf OT. Arousal and cortisol interact in modulating memory consolidation in healthy young men. Behavioral Neuroscience. 2006;120:217–223
  29. Lalumiere R, Buen T, McGaugh JL. Post-training intra-basolateral amygdala infusions of norepinephrine enhance consolidation of memory for contextual fear conditioning. The Journal of Neuroscience. 2003;23(17):6754–6758
  30. Liang KC. Peripheral epinephrine modulates the effects of post-training amygdala stimulation on memory. Behavioral Brain Research. 1985;15(2):93–100
  31. Liang KC, Juler R, McGaugh JL. Modulating effects of postraining epinephrine on memory: Involvement of the amygdale noradrenergic system. Brain Research. 1986;368:125–133
  32. Liang KC, McGaugh JL, Yao HY. Involvement of amygdala pathways in the influence of post-training intra-amygdala norepinephrine, and peripheral epinephrine on memory storage. Brain Research. 1990;508(2):225–233
  33. Liang KC, Chen LL, Huang TE. The role of the amygdala norepinephrine in memory formtation: Involvement of memory enhancing effect of peripheral epinephrine. Chinese Journal of Physiology. 1995;38:81–91
  34. Mackiewicz KL, Sarinopoulos I, Cleven KL, Nitschke JB. The effect of anticipation and the specificity of sex differences for amygdala and hippocampus function in emotional memory. Proceedings of the National Academy of Sciences United States of America. 2006;103(38):14200–14205
  35. McGaugh JL, Liang KC, Bennet C, Sternberg D. Involvement of the amygdala in memory storage: interaction of peripheral and central systems. In:  Lynch G,  McGaugh JL,  Weinberger NM editor. Neurobiology of Learning and Memory. New York: Guilford; 1984;
  36. McGaugh JL, Cahill L, Roozendaal B. Involvement of the amygdala in memory storage: interaction with other brain regions. Proceedings of the National Academy of Sciences United States of America. 1996;93:13508–13514
  37. McIntyre C, Hatfield T, McGaugh JL. Amygdala norepinephrine levels after training predict inhibitory avoidance retention performance in rats. The European Journal of Neuroscience. 2002;16:1223–1226
  38. Nater UM, La Marca R, Florin L, Moses A, Langhans W, Koller MM, et al. Stress-induced changes in human salivary alpha-amylase activity–associations with adrenergic activity. Psychoneuroendocrinology. 2006;31(1):49–58
  39. Nederfors T, Dahlof C. Effects of the beta-adrenoceptor antagonist atenolol and propranolol on human whole saliva flow rate and composition. Archives of Oral Biology. 1992;37(7):579–584
  40. Nederfors T, Dahlof C, Twetman S. Effects of the beta-adrenoceptor antagonists atenolol and propranolol on human unstimulated whole saliva flow rate and protein composition. Scandinavian Journal of Dental Research. 1994;102(4):235–237
  41. O’Carroll RE, Drysdale E, Cahill L, Shajahan P, Ebmeier KP. Stimulation of the noradrenergic system enhances and blockade reduces memory for emotional material. Psychological Medicine. 1999;29:1083–1088
  42. Okuda S, Roozendaal B, McGaugh J. Glucocorticoids effect on object recognition memory require training-associated emotional arousal. PNAS. 2003;101(3):853–858
  43. Power AE, Thai LJ, McGaugh JL. Lesions of the nucleus basalis magnocellularis induced by 192 IgG-saporin block memory enhancement with posttraining norepinephrine in the basolateral amygdala. PNAS. 2001;99(4):2315–2319
  44. Pruessner J, Kirschbaum C, Meinlschmid G, Hellhammer D. Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroendocrinology. 2003;28:916–931
  45. Quirate GL, Galvez R, Roozendaal B, McGaugh JL. Norepinephrine release in the amygdala in response to footshock and opiod peptidergic drugs. Brain Research. 1998;808:134–140
  46. Richter-Levin G, Akirav I. Emotional tagging for memory formation—in the search for neural mechanisms. Brain Research Reviews. 2003;41(3):247–256
  47. Rimelle U, Domes G, Mathiak K, Hautzinger M. Cortisol has different effects on human memory for emotional and neutral stimuli. Cognitive Neuroscience and Neuropsychology. 2003;14(18):2485–2488
  48. Rohleder N, Nater U, Wolf J, Ehlert U, Kirschbaum C. Psychosocial stress-induced activation of salivary alpha-amylase: an indicator or sympathetic activity?. Annals of the New York Academy of Science. 2004;1032:258–263
  49. Roozendaal B, Okuda S, Van der Zee E, McGaugh J. Glucocorticoid Enhancement of memory requires arousal-induced noradrenergic activation in the basolateral amygdala. PNAS. 2006;103:6741–6746
  50. Shirtcliff EA, Granger DA, Schwartz E, Curran MJ. Use of biomarkers in biobehavioral research: cotton-based sample collection methods can interfere with salivary immunoassay results. Psychoneuroendocrinology. 2001;26(2):165–173
  51. Skov O, Kirekegaard P, Rasmussen T, Magid E, Poulsen S, Nexo E. Adrenergic effects on secretion of amylase from the rat salivary glands. Digestion. 1998;41(1):34–38
  52. Soetens E, Casaer S, D’Hooge R, Hueting JE. Effect of amphetamine on long-term retention of verbal material. Psychopharmacology. 1995;119:5–62
  53. Southwick S, Davis M, Horner B, Cahill LF, Morgan CA, Gold PE, et al. Relationship of enhanced norepinephrine activity during memory consolidation to enhanced long-term memory in humans. American Journal of Psychiatry. 2002;159:1420–1422
  54. Speirs RL, Herring J, Cooper WD, Hardy CC, Hind CR. The influence of Sympathetic activity and isoprenaline on the secretion of amylase from the human parotid gland. Archives of Oral Biology. 1974;19(9):747–752
  55. Strange B, Dolan R. (Beta)-adrenergic modulation of emotional memory-evoked human amygdala and hippocampal responses. PNAS. 2004;101(31):11454–11458
  56. van Stegeren AH, Cahill Everaerd W, Cahill L, McGaugh JL, Gooren LJ. Memory for emotional events: differential effects of centrally versus peripherally acting beta-blocking agents. Psychopharmacology. 1998;138(3–4):305–310
  57. van Stegeren A, Goekoop R, Everaerd W, Scheltens P, Barkhof F, Kuijer J, et al. Noradrenaline mediates amygdala activation in men and women during encoding of emotional material. Neuroimage. 2005;24:898–909
  58. Whelton H. Introduction: the anatomy and physiology of the salivary glands. In:  Edgar WM,  O’Mullane DM editor. Saliva and Oral Health. second ed.. London: British Dental Association; 1996;p. 1–8
  59. Wolf OT, Schommer NC, Hellhammer DH, McEwen BS, Kirschbaum C. The relationship between men and women. Psychoneuroendocrinology. 2001;26(7):711–720
  60. Yoshimura K, Fujita-Yoshigaki J, Murakami M, Segawa A. Cyclic AMP has distinct effects from Ca2+ in evoking priming and fushion/ exocytosis in parotid amylase secretion. European Journal of Physiology. 2002;444:586–596

PII: S0306-4530(09)00150-4

doi: 10.1016/j.psyneuen.2009.04.020

Psychoneuroendocrinology
Volume 34, Issue 9 , Pages 1263-1271 , October 2009