Cognitive, Affective, & Behavioral Neuroscience

, Volume 4, Issue 3, pp 294–306 | Cite as

How arousal modulates memory: Disentangling the effects of attention and retention

Article

Abstract

Emotion may influence memory both by altering attention and perception during encoding and by affecting memory retention. To date, studies have focused on the enhancement of memory consolidation by arousal. However, they have failed to rule out a role for attention. To specifically link memory enhancement of arousing material to modulation of memory retention, we examined recognition of neutral and arousing words at two time points and under conditions that manipulate attention during encoding. Participants were briefly presented with an arousing or neutral word at the periphery, while fixating on a central word. Recognition of peripheral words was assessed either immediately or after 24 h. Whereas recognition of neutral words became worse over time, recognition of arousing words remained the same and was better than neutral word recognition at delay. The results indicate that arousal supports slower forgetting even when the difference in attentional resources allocated to stimuli is minimized.

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References

  1. Adolphs, R., Denburg, N. L., & Tranel, D. (2001). The amygdala’s role in long-term declarative memory for gist and detail. Behavioral Neuroscience, 115, 983–992.PubMedCrossRefGoogle Scholar
  2. Adolphs, R., Tranel, D., & Denburg, N. L. (2000). Impaired emotional declarative memory following unilateral amygdala damage. Learning & Memory, 7, 180–186.CrossRefGoogle Scholar
  3. Anderson, A. K., & Phelps, E. A. (2001). Lesions of the human amygdala impair enhanced perception of emotionally salient events. Nature, 411, 305–309.PubMedCrossRefGoogle Scholar
  4. Baddeley, A. D. (1982). Implications of neuropsychological evidence for theories of normal memory. Philosophical Transactions of the Royal Society of London: Series B, 298, 59–72.CrossRefGoogle Scholar
  5. Balch, W. R., Myers, D. M., & Papotto, C. (1999). Dimensions of mood in mood-dependent memory. Journal of Experimental Psychology: Learning, Memory, & Cognition, 25, 70–83.CrossRefGoogle Scholar
  6. Balota, D. A., Pilotti, M., & Cortese, M. J. (2001). Subjective frequency estimates for 2,938 monosyllabic words. Memory & Cognition, 29, 639–647.CrossRefGoogle Scholar
  7. Bargh, J. A., Chaiken, S., Govender, R., & Pratto, F. (1992). The generality of the automatic attitude activation effect. Journal of Personality & Social Psychology, 62, 893–912.CrossRefGoogle Scholar
  8. Bohannon, J. N., III (1988). Flashbulb memories for the space shuttle disaster: A tale of two theories. Cognition, 29, 179–196.PubMedCrossRefGoogle Scholar
  9. Bradley, M. M., Greenwald, M. K., Petry, M. C., & Lang, P. J. (1992). Remembering pictures: Pleasure and arousal in memory. Journal of Experimental Psychology: Learning, Memory, & Cognition, 18, 379–390.CrossRefGoogle Scholar
  10. Buchanan, T. W., & Lovallo, W. R. (2001). Enhanced memory for emotional material following stress-level cortisol treatment in humans. Psychoneuroendocrinology, 26, 307–317.PubMedCrossRefGoogle Scholar
  11. Burke, A., Heuer, F., & Reisberg, D. (1992). Remembering emotional events. Memory & Cognition, 20, 277–290.CrossRefGoogle Scholar
  12. Cahill, L. (1997). The neurobiology of emotionally influenced memory: Implications for understanding traumatic memory. In R. Yehuda & A. C. McFarlane (Eds.). Psychobiology of posttraumatic stress disorder (Annals of the New York Academy of Sciences, Vol. 821, pp. 238–246). New York: New York Academy of Sciences.Google Scholar
  13. Cahill, L., & Alkire, M. T. (2003). Epinephrine enhancement of human memory consolidation: Interaction with arousal at encoding. Neurobiology of Learning & Memory, 79, 2194–2198.Google Scholar
  14. Cahill, L., Babinsky, R., Markowitsch, H. J., & McGaugh, J. L. (1995). The amygdala and emotional memory. Nature, 377, 295–296.PubMedCrossRefGoogle Scholar
  15. Cahill, L., Gorski, L., & Le, K. (2003). Enhanced human memory consolidation with post-learning stress: Interaction with the degree of arousal at encoding. Learning & Memory, 10, 4270–4274.CrossRefGoogle Scholar
  16. Cahill, L., Haier, R. J., Fallon, J., Alkire, M. T., Tang, C., Keator, D., Wu, J., & McGaugh, J. L.(1996). Amygdala activity at encoding correlated with long-term, free recall of emotional information. Proceedings of the National Academy of Sciences, 93, 8016–8021.CrossRefGoogle Scholar
  17. Cahill, L., Prins, B., Weber, M., & McGaugh, J. L. (1994). Beta-adrenergic activation and memory for emotional events. Nature, 20, 702–704.CrossRefGoogle Scholar
  18. Canli, T., Desmond, J. E., Zhao, Z., & Gabrieli, J. D. (2002). Sex differences in the neural basis of emotional memories. Proceedings of the National Academy of Science, 99, 10789–10794.CrossRefGoogle Scholar
  19. Carpenter, R. H. S. (1988). Movements of the eyes. London: Pion Press.Google Scholar
  20. Christianson, S. A. (1984). The relationship between induced emotional arousal and amnesia. Scandinavian Journal of Psychology, 25, 147–160.PubMedCrossRefGoogle Scholar
  21. Christianson, S. A. (1992). Remembering emotional events: Potential mechanisms. In S. Christianson (Ed.), The handbook of emotion and memory: Research and theory (pp. 307–340). Hillsdale, NJ: Erlbaum.Google Scholar
  22. Christianson, S. A., & Fallman, L. (1990). The role of age on reactivity and memory for emotional pictures. Scandinavian Journal of Psychology, 31, 291–301.PubMedCrossRefGoogle Scholar
  23. Christianson, S. A., & Loftus, E. F. (1991). Remembering emotional events: The fate of detailed information. Cognition & Emotion, 5, 81–108.CrossRefGoogle Scholar
  24. Christianson, S. A., Loftus, E. F., Hoffman, H., & Loftus, G. R. (1991). Eye fixations and memory for emotional events. Journal of Experimental Psychology: Learning, Memory, & Cognition, 17, 693–701.CrossRefGoogle Scholar
  25. Clifford, B., & Hollins, C. (1981). Effects of the type of incident and the number of perpetrators on eyewitness memory. Journal of Applied Psychology, 66, 364–370.CrossRefGoogle Scholar
  26. Craik, F. I. M., & Lockhart, R. S. (1972). Levels of processing: A framework for memory research. Journal of Verbal Learning & Verbal Behavior, 11, 671–684.CrossRefGoogle Scholar
  27. Doerksen, S., & Shimamura, A. P. (2001). Source memory enhancement for emotional words. Emotion, 1, 5–11.PubMedCrossRefGoogle Scholar
  28. Dolan, R. J., Lane, R., Chua, P., & Fletcher, P. (2000). Dissociable temporal lobe activations during emotional episodic memory retrieval. NeuroImage, 11, 203–209.PubMedCrossRefGoogle Scholar
  29. Easterbrook, J. A. (1959). The effect of emotion on cue utilization and the organization of behavior. Psychology Review, 66, 183–201.CrossRefGoogle Scholar
  30. Fox, E., Russo, R., Bowles, R., & Dutton, K. (2001). Do threatening stimuli draw or hold visual attention in subclinical anxiety? Journal of Experimental Psychology: General, 130, 681–700.CrossRefGoogle Scholar
  31. Gallagher, M., & Kapp, B. S. (1981). Effect of phentolamine administration into the amygdala complex of rats on time-dependent memory processes. Behavioral & Neural Biology, 31, 90–95.CrossRefGoogle Scholar
  32. Gernsbacher, M. A. (1984). Resolving twenty years of inconsistent interactions between lexical familiarity and orthography, concreteness, and polysemy. Journal of Experimental Psychology: General, 113, 256–281.CrossRefGoogle Scholar
  33. Gilhooly, K. J., & Logie, R. H. (1980). Age-of-acquisition, imagery, concreteness, familiarity, and ambiguity measures for 1,944 words. Behavior Research Methods & Instrumentation, 12, 395–427.CrossRefGoogle Scholar
  34. Hamann, S. B., Ely, T. D., Grafton, S. T., & Kilts, C. D. (1999). Amygdala activity related to enhanced memory for pleasant and aversive stimuli. Nature Neuroscience, 2, 289–293.PubMedCrossRefGoogle Scholar
  35. Hansen, C. H., & Hansen, R. D. (1988). Finding the face in the crowd: An anger superiority effect. Journal of Personality & Social Psychology, 54, 917–924.CrossRefGoogle Scholar
  36. Heuer, F., & Reisberg, D. (1990). Vivid memories of emotional events: The accuracy of remembered minutiae. Memory & Cognition, 18, 496–506.CrossRefGoogle Scholar
  37. Hochberg, J. (1978). Perception (2nd ed.). Englewood Cliffs, NJ: Prentice-Hall.Google Scholar
  38. Keppel, G. (1991). Design and analysis: A researcher’s handbook (3rd ed.). Englewood Cliffs, NJ: Prentice-Hall.Google Scholar
  39. Kleinsmith, L. J., & Kaplan, S. (1963). Paired-associate learning as a function of arousal and interpolated interval. Journal of Experimental Psychology, 65, 190–193.PubMedCrossRefGoogle Scholar
  40. LaBar, K. S., LeDoux, J. E., Spencer, D. D., & Phelps, E. A. (1995). Impaired fear conditioning following unilateral temporal lobectomy in humans. Journal of Neuroscience, 15, 6846–6855.PubMedGoogle Scholar
  41. LaBar, K. S., & Phelps, E. A. (1998). Arousal-mediated memory consolidation: Role of the medial temporal lobe in humans. Psychological Science, 9, 490–493.CrossRefGoogle Scholar
  42. Levonian, E. (1966). Evoked potential in relation to subsequent alpha frequency. Science, 152, 1280–1282.PubMedCrossRefGoogle Scholar
  43. Liang, K. C., Juler, R. G., & McGaugh, J. L. (1986). Modulating effects of posttraining epinephrine on memory: Involvement of the amygdala noradrenergic system. Brain Research, 12, 125–133.CrossRefGoogle Scholar
  44. Libkuman, T. M., Nichols-Whitehead, P., Griffith, J., & Thomas, R. (1999). Source of arousal and memory for detail. Memory & Cognition, 27, 166–190.CrossRefGoogle Scholar
  45. Loftus, E. F., Loftus, G. R., & Messo, J. (1987). Some facts about weapon focus. Law & Human Behavior, 11, 55–62.CrossRefGoogle Scholar
  46. Mayfrank, L., Kimmig, H., & Fischer, B. (1987). The role of attention in the preparation of visually guided saccadic eye movements in man. In J. K. O’Regan & A. Levy-Schoen (Eds.), Eye movements: From physiology to cognition (pp. 37–45). New York: Elsevier, North-Holland.Google Scholar
  47. McGaugh, J. L. (1992). Affect, neuromodulatory systems and memory storage. In S. Christianson (Ed.), The handbook of emotion and memory: Research and theory (pp. 269–288). Hillsdale, NJ: Erlbaum.Google Scholar
  48. McGaugh, J. L. (2000). Memory: A century of consolidation. Science, 14, 248–251.CrossRefGoogle Scholar
  49. Neisser, U. (1976). Cognition and reality. New York: Freeman.Google Scholar
  50. Ochsner, K. N. (2000). Are affective events richly recollected or simply familiar? The experience and process of recognizing feelings past. Journal of Experimental Psychology. General, 129, 242–261.PubMedCrossRefGoogle Scholar
  51. Öhman, A., Estevens, F., & Soares, F. (1995). Preparedness and preattentive associative learning: Electrodermal conditioning masked stimuli. Journal of Psychophysiology, 9, 99–108.Google Scholar
  52. Packard, M. G., & Teather, L. A. (1998). Amygdala modulation of multiple memory systems: Hippocampus and caudate-putamen. Neurobiology of Learning & Memory, 69, 163–203.CrossRefGoogle Scholar
  53. Reisberg, D., & Heuer, F. (1992). Remembering the details of emotional events. In E. Winograd & U. Neisser (Eds.), Affect and accuracy in recall: Studies of “flashbulb” memories (pp. 163–190). Cambridge, MA: Harvard University Press.Google Scholar
  54. Revelle, W. (1989). Personality, motivation, and cognitive performance. In P. Ackerman, R. Kanfer, & R. Cudeck (Eds.), Learning and individual differences: Abilities, motivations, and methodology (pp. 297–341). Hillsdale, NJ: Erlbaum.Google Scholar
  55. Revelle, W., & Loftus, D. A. (1990). Individual differences and arousal: Implications for the study of mood and memory. Cognition & Emotion, 4, 209–237.CrossRefGoogle Scholar
  56. Richardson, M. P., Strange, B. A., & Dolan, R. J. (2004). Encoding of emotional memories depends on amygdala and hippocampus and their interactions. Nature Neuroscience, 7, 278–285.PubMedCrossRefGoogle Scholar
  57. Strange, B. A., Henson, R. N., Friston, K. J., & Dolan, R. J. (2000). Brain mechanisms for detecting perceptual, semantic, and emotional deviance. NeuroImage, 12, 425–433.PubMedCrossRefGoogle Scholar
  58. Strange, B. A., Hurlemann, R., & Dolan, R. J. (2003). An emotioninduced retrograde amnesia in humans is amygdala- and betaadrenergic-dependent. Proceedings of the National Academy of Sciences, 100, 13626–13631.CrossRefGoogle Scholar
  59. Vazdarjanova, A., & McGaugh, J. L. (1999). Basolateral amygdala is involved in modulating consolidation of memory for classical fear conditioning. Journal of Neuroscience, 1, 6615–6622.Google Scholar
  60. Venables, P. H., & Christie, M. J. (1973). Mechanisms, instrumentation, recording techniques, and quantification of responses. In W. F. Prokasy & D. C. Raskin (Eds.), Electrodermal activity in psychological research (pp. 125–155). New York: Academic Press.Google Scholar
  61. Vuilleumier, P., Armony, J. L., Driver, J., & Dolan, R. J. (2001). Effects of attention and emotion on face processing in the human brain: An event-related fMRI study. Neuron, 30, 829–841.PubMedCrossRefGoogle Scholar
  62. Vuilleumier, P., & Schwartz, S. (2001). Emotional facial expressions capture attention. Neurology, 23, 153–158.Google Scholar
  63. Walker, E. L. (1958). Action decrement and its relation to learning. Psychological Review, 65, 129–142.CrossRefGoogle Scholar
  64. Walker, E. L., & Tarte, R. D. (1963). Memory storage as a function of arousal and time with homogeneous and heterogeneous lists. Journal of Verbal Learning & Verbal Behavior, 2, 113–119.CrossRefGoogle Scholar
  65. Wessel, I., van der Kooy, P., & Merckelbach, H. (2000). Differential recall of central and peripheral details of emotional slides is not a stable phenomenon. Memory, 8, 95–109.PubMedCrossRefGoogle Scholar

Copyright information

© Psychonomic Society, Inc. 2004

Authors and Affiliations

  1. 1.Department of PsychologyNew York UniversityNew York

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