Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Amygdala damage impairs emotional memory for gist but not details of complex stimuli

Nature Neuroscience volume 8, pages 512–518 (2005)Cite this article

Abstract

Neurobiological studies demonstrate the amygdala's role in emotional memory, and psychological studies suggest a particular pattern: enhanced memory for the gist but not the details of complex stimuli. We hypothesized that these two findings are related. Whereas normal (n = 52) and brain-damaged (n = 22) controls showed the expected enhancement of gist memory when the encoding context was emotional, persons with unilateral damage to the medial temporal lobe including the amygdala (n = 16) did not show this pattern. Furthermore, amygdala volume showed a significant positive correlation with gist memory but not with overall memory. A further study in four subjects with selective medial temporal damage sparing the amygdala, and one with selective damage confined to the amygdala, confirmed the specificity of this effect to the amygdala. The data support a model whereby the amygdala focuses processing resources on gist, possibly accounting for features of traumatic memories and eyewitness testimony in real life.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Task design.
Figure 2: Differential modulation of memory for gist by emotion.
Figure 3: Differential modulation of memory for gist by emotion: replication with Experiment 2.
Figure 4: Within-subject gist memory.
Figure 5: Correlation between memory performance and neuroanatomy.
Figure 6: Neuroanatomy of subjects with selective hippocampal or amygdala damage.
Figure 7: Gist memory in subjects with bilateral hippocampal or bilateral amygdala damage.

References

  1. Christianson, S.-A. & Loftus, E.F. Remembering emotional events: the fate of detailed information. Cogn. Emotion 5, 81–108 (1991).

    Article  Google Scholar 

  2. Reisberg, D. & Heuer, F. in Affect and Accuracy in Recall: Studies of 'Flashbulb' Memories (eds. Winograd, E. & Neisser, U.) 163–190 (Harvard Univ. Press, Cambridge, Massachusetts, 1992).

    Google Scholar 

  3. Burke, A., Heuer, F. & Reisberg, D. Remembering emotional events. Mem. Cognit. 20, 277–290 (1992).

    Article  CAS  Google Scholar 

  4. Wessel, I. & Merckelbach, H. Memory for threat-relevant and threat-irrelevant cues in spider phobics. Cogn. Emotion 12, 93–104 (1998).

    Article  Google Scholar 

  5. Loftus, E.F. Eyewitness Testimony (Harvard Univ. Press, Cambridge, Massachusetts, 1979).

    Google Scholar 

  6. Maass, A. & Koehnken, G. Eyewitness identification. Law Hum. Behav. 13, 397–408 (1989).

    Article  Google Scholar 

  7. Cahill, L. & McGaugh, J.L. Mechanisms of emotional arousal and lasting declarative memory. Trends Neurosci. 21, 294–299 (1998).

    Article  CAS  Google Scholar 

  8. Canli, T., Zhao, Z., Brewer, J., Gabrieli, J.D.E. & Cahill, L. Event-related activation in the human amygdala associates with later memory for individual emotional experience. J. Neurosci. 20, RC99 (2000).

    Article  CAS  Google Scholar 

  9. Hamann, S.B., Ely, T.D., Grafton, S.T. & Kilts, C.D. Amygdala activity related to enhanced memory for pleasant and aversive stimuli. Nat. Neurosci. 2, 289–293 (1999).

    Article  CAS  Google Scholar 

  10. Phelps, E.A. et al. Specifying the contributions of the human amygdala to emotional memory: a case study. Neurocase 4, 527–540 (1998).

    Article  Google Scholar 

  11. Adolphs, R., Cahill, L., Schul, R. & Babinsky, R. Impaired declarative memory for emotional material following bilateral amygdala damage in humans. Learn. Mem. 4, 291–300 (1997).

    Article  CAS  Google Scholar 

  12. McGaugh, J.L. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu. Rev. Neurosci. 27, 1–28 (2004).

    Article  CAS  Google Scholar 

  13. Kensinger, E.A. & Corkin, S. Two routes to emotional memory: distinct neural processes for valence and arousal. Proc. Natl. Acad. Sci. USA 101, 3310–3315 (2004).

    Article  CAS  Google Scholar 

  14. Rauch, S.L. et al. A symptom provocation study of posttraumatic stress disorder using positron emission tomography and script-driven imagery. Arch. Gen. Psychiatry 53, 380–387 (1996).

    Article  CAS  Google Scholar 

  15. Mori, E. et al. Amygdalar volume and emotional memory in Alzheimer's disease. Am. J. Psychiatry 156, 216–222 (1999).

    CAS  PubMed  Google Scholar 

  16. Adolphs, R., Denburg, N. & Tranel, D. The amygdala's role in declarative memory for gist and detail. Behav. Neurosci. 115, 983–992 (2001).

    Article  CAS  Google Scholar 

  17. Smith, A.P., Dolan, R.J. & Rugg, M.D. Event-related potential correlates of the retrieval of emotional and nonemotional context. J. Cogn. Neurosci. 16, 760–775 (2004).

    Article  Google Scholar 

  18. Cahill, L. & McGaugh, J.L. A novel demonstration of enhanced memory associated with emotional arousal. Conscious. Cogn. 4, 410–421 (1995).

    Article  CAS  Google Scholar 

  19. Adolphs, R. & Tranel, D. in The Amygdala. A Functional Analysis (ed. Aggleton, J.P.) 587–630 (Oxford Univ. Press, New York, 2000).

    Google Scholar 

  20. Easterbrook, J.A. The effect of emotion on cue utilization and the organization of behavior. Psychol. Rev. 66, 183–201 (1959).

    Article  CAS  Google Scholar 

  21. LaBar, K.S. & Phelps, E.A. Arousal-mediated memory consolidation: role of the medial temporal lobe in humans. Psychol. Sci. 9, 490–494 (1998).

    Article  Google Scholar 

  22. Parker, A., Wilding, E. & Akerman, C. The von Restorff effect in visual object recognition memory in humans and monkeys: the role of frontal/perirhinal interaction. J. Cogn. Neurosci. 10, 691–703 (1998).

    Article  CAS  Google Scholar 

  23. Phelps, E.A., LaBar, K.S. & Spencer, D.D. Memory for emotional words following unilateral temporal lobectomy. Brain Cogn. 35, 85–109 (1997).

    Article  CAS  Google Scholar 

  24. Brierley, B., Medford, N., Shaw, P. & David, A.S. Emotional memory and perception in temporal lobectomy patients with amygdala damage. J. Neurol. Neurosurg. Psychiatry 75, 593–599 (2004).

    Article  CAS  Google Scholar 

  25. Hamann, S.B., Cahill, L. & Squire, L.R. Emotional perception and memory in amnesia. Neuropsychology 11, 104–113 (1997).

    Article  CAS  Google Scholar 

  26. Cahill, L. et al. Sex-related difference in amygdala activity during emotionally influenced memory storage. Neurobiol. Learn. Mem. 75, 1–9 (2001).

    Article  CAS  Google Scholar 

  27. Canli, T., Desmond, J.E., Zhao, Z. & Gabrieli, J.D.E. Sex differences in the neural basis of emotional memories. Proc. Natl. Acad. Sci. USA 99, 10789–10794 (2002).

    Article  CAS  Google Scholar 

  28. Cahill, L. & van Stegeren, A. Sex-related impairment of memory for emotional events with beta-adrenergic blockade. Neurobiol. Learn. Mem. 79, 81–88 (2003).

    Article  CAS  Google Scholar 

  29. Dolan, R.J., Lane, R., Chua, P. & Fletcher, P.C. Dissociable temporal lobe activations during emotional episodic memory retrieval. Neuroimage 11, 203–209 (2000).

    Article  CAS  Google Scholar 

  30. Packard, M.G. & Chen, S.A. The basolateral amygdala is a cofactor in memory enhancement produced by intrahippocampal glutamate injections. Psychobiology 27, 377–385 (1999).

    Google Scholar 

  31. Gale, G.D. et al. Role of the basolateral amygdala in the storage of fear memories across the adult lifetime of rats. J. Neurosci. 24, 3810–3815 (2004).

    Article  CAS  Google Scholar 

  32. Dolcos, F., LaBar, K.S. & Cabeza, R. Interaction between the amygdala and the medial temporal lobe memory system predicts better memory for emotional events. Neuron 42, 855–863 (2004).

    Article  CAS  Google Scholar 

  33. Bechara, A. et al. Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. Science 269, 1115–1118 (1995).

    Article  CAS  Google Scholar 

  34. Richardson, M.P., Strange, B.A. & Dolan, R.J. Encoding of emotional memories depends on amygdala and hippocampus and their interaction. Nat. Neurosci. 7, 278–285 (2004).

    Article  CAS  Google Scholar 

  35. Ikegaya, Y., Saito, H. & Abe, K. The basomedial and basolateral amygdaloid nuclei contribute to the induction of long-term potentiation in the dentate gyrus in vivo. Eur. J. Neurosci. 8, 1833–1839 (1996).

    Article  CAS  Google Scholar 

  36. Akirav, I. & Richter-Levin, G. Biphasic modulation of hippocampal plasticity by behavioral stress and basolateral amygdala stimulation in the rat. J. Neurosci. 19, 10530–10535 (1999).

    Article  CAS  Google Scholar 

  37. Frank, R.J., Damasio, H. & Grabowski, T.J. Brainvox: an interactive, multi-modal visualization and analysis system for neuroanatomical imaging. Neuroimage 5, 13–30 (1997).

    Article  CAS  Google Scholar 

  38. Lang, P.J., Oehman, A. & Vaitl, D. The International Affective Picture System (Univ. of Florida, Gainesville, Florida, 1988).

    Google Scholar 

  39. Allen, J.S., Tranel, D., Bruss, J. & Damasio, H. Correlations between regional brain volumes and memory performance in anoxia. J. Clin. Neuropsychol. (in press).

Download references

Acknowledgements

We thank J. Nath, S. Lemker and M. Karafin for assistance in testing subjects, and D. Krutzfeldt and R. Henson for help in scheduling their visits. This study was supported by grant R01 MH67681 from the National Institute of Mental Health and by grant P01 19632 from the National Institute of Neurological Disorders and Stroke.

Author information

Authors and Affiliations

  1. Division of Humanities and Social Sciences, California Institute of Technology, Pasadena, 91125, California, USA

    Ralph Adolphs

  2. Department of Neurology, Division of Cognitive Neuroscience, University of Iowa College of Medicine, Iowa City, 52242, Iowa, USA

    Ralph Adolphs, Daniel Tranel & Tony W Buchanan

Authors
  1. Ralph Adolphs
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daniel Tranel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tony W Buchanan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ralph Adolphs.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Figure 1

Raw memory scores for gist and for detail. (PDF 45 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Adolphs, R., Tranel, D. & Buchanan, T. Amygdala damage impairs emotional memory for gist but not details of complex stimuli. Nat Neurosci 8, 512–518 (2005). https://doi.org/10.1038/nn1413

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn1413

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing