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Development of shared information in communication despite hippocampal amnesia

Nature Neuroscience volume 9, pages 140–146 (2006)Cite this article

Abstract

This study investigated the ability of individuals with amnesia to acquire referential labels across a series of collaborative, dynamic interactions with a communication partner. Despite their inability to learn arbitrary relations in paired-associate learning, the amnesic patients showed remarkably robust collaborative learning across trials, at a rate equal to that of normal comparison subjects. The amnesic participants' learning resulted in their arriving at labels for a set of abstract shapes (tangrams), thus facilitating rapid and efficient communication. The labels generated and used by the amnesics during interactions with their partners became simpler across trials, with most labels stabilizing long before the end of training and then being used consistently throughout; moreover, they endured long after the task had ended. These findings have important implications for understanding the memory systems involved in semantic learning and in acquiring shared knowledge ('common ground') among communication partners, and the nature of hippocampal-dependent versus hippocampal-independent learning.

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Figure 2: Amnesic patients show intact rate of learning.
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References

  1. Clark, H. Arenas of Language Use. (University of Chicago Press, Chicago, 1992).

    Google Scholar 

  2. Cohen, N.J. Preserved learning capacity in amnesia: evidence for multiple memory systems. in The Neuropsychology of Memory (eds. Butters, N. & Squire, L.R.) 83–103 (Guilford Press, New York, 1984).

    Google Scholar 

  3. Cohen, N.J. Declarative memory. in Learning and Memory 2nd edn. (ed. Byrne, J.H.) (Macmillan Library Reference, New York, 2003).

    Google Scholar 

  4. Cohen, N.J. & Eichenbaum, H. Memory, Amnesia and the Hippocampal System. (MIT Press, Cambridge, Massachusetts, 1993).

    Google Scholar 

  5. Eichenbaum, H. & Cohen, N.J. From Conditioning to Conscious Recollection: Memory Systems of the Brain. (Oxford Univ. Press, New York, 2001).

    Google Scholar 

  6. Gabrieli, J.D. Cognitive neuroscience of human memory. Annu. Rev. Psychol. 49, 87–115 (1998).

    Article  CAS  Google Scholar 

  7. Squire, L.R. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol. Rev. 99, 195–231 (1992).

    Article  CAS  Google Scholar 

  8. MacKay, D.G., Burke, D.M. & Stewart, R.H. M's language production deficits: implications for relations between memory, semantic binding, and the hippocampal system. J. Mem. Lang. 38, 28–69 (1998).

    Article  Google Scholar 

  9. MacKay, D.G., Stewart, R. & Burke, D.M. H.M. revisited: relations between language, comprehension, memory and the hippocampal system. J. Cogn. Neurosci. 10, 377–394 (1998).

    Article  CAS  Google Scholar 

  10. MacKay, D.G. & James, L.E. The binding problem for syntax, semantics, and prosody: H.M.'s selective sentence reading deficits under the theoretical-syndrome approach. Lang. Cogn. Process. 16, 419–460 (2001).

    Article  Google Scholar 

  11. Clark, H. & Wilkes-Gibbs, D. Referring as a collaborative process. Cognition 22, 1–39 (1986).

    Article  Google Scholar 

  12. Hengst, J. Collaborative referencing between individuals with aphasia and routine communication partners. J. Speech Lang. Hear. Res. 46, 831–848 (2003).

    Article  Google Scholar 

  13. Cohen, N.J., Poldrack, R. & Eichenbaum, H. Memory for items and memory for relations in the procedural/declarative memory framework. in Theories of Organic Amnesia (eds. Mayes, A. & Downes, J.) 131–178 (Psychology Press, Hove, UK, 1997).

    Google Scholar 

  14. Cohen, N.J. et al. Hippocampal system and declarative (relational) memory: summarizing the data from functional neuroimaging studies. Hippocampus 9, 83–98 (1999).

    Article  CAS  Google Scholar 

  15. Ryan, J.D., Althoff, R.R., Whitlow, S. & Cohen, N.J. Amnesia is a deficit in relational memory. Psychol. Sci. 11, 454–461 (2000).

    Article  CAS  Google Scholar 

  16. Ryan, J. & Cohen, N.J. The nature of change detection and online representations of scenes. J. Exp. Psychol. Hum. Percept. Perform. 30, 988–1015 (2004).

    Article  Google Scholar 

  17. Gabrieli, J.D., Cohen, N.J. & Corkin, S. The impaired learning of semantic knowledge following bilateral medial temporal-lobe resection. Brain Cogn. 7, 157–177 (1988).

    Article  CAS  Google Scholar 

  18. O'Kane, G., Kensinger, E.A. & Corkin, S. Evidence for semantic learning in profound amnesia: an investigation with patient H.M. Hipppocampus 14, 417–425 (2004).

    Article  Google Scholar 

  19. Bayley, P.J. & Squire, L.R. Medial temporal lobe amnesia: gradual acquisition of factual information by nondeclarative memory. J. Neurosci. 22, 5741–5748 (2002).

    Article  CAS  Google Scholar 

  20. Wilson, B.A. & Wearing, D. Prisoner of consciousness: a state of just awakening following herpes simplex encephalitis. in Broken Memories: Case Studies in Memory Impairment (eds. Campbell, R. & Conway, M.A.) 14–30 (Blackwell, Cambridge, Massachusetts, 1995).

    Google Scholar 

  21. Kovner, R., Mattis, S. & Goldmeier, E. A technique for promoting robust free recall in chronic organic amnesia. J. Clin. Neuropsychol. 5, 65–71 (1983).

    Article  CAS  Google Scholar 

  22. Tulving, E., Hayman, C.A. & Macdonald, C. Long-lasting perceptual priming and semantic learning in amnesia: a case experiment. J. Exp. Psychol. Learn. Mem. Cogn. 17, 595–617 (1991).

    Article  CAS  Google Scholar 

  23. Eichenbaum, H. Hippocampus: cognitive processes and neural representations that underlie declarative memory. Neuron 44, 109–120 (2004).

    Article  CAS  Google Scholar 

  24. Squire, L.R., Cohen, N.J. & Nadel, L. The medial temporal region and memory consolidation: a new hypothesis. in Memory Consolidation (eds. Weingartner, H. & Parker, E.) 185–210 (Erlbaum, Hillsdale, New Jersey, 1984).

    Google Scholar 

  25. Teyler, T.J. & DiScenna, P. The role of hippocampus in memory: a hypothesis. Neurosci. Biobehav. Rev. 9, 377–389 (1985).

    Article  CAS  Google Scholar 

  26. Damasio, A.R. Time-locked multiregional retroactivation: a systems-level proposal for the neural substrates of recall and recognition. Cognition 33, 25–62 (1989).

    Article  CAS  Google Scholar 

  27. McClelland, J.L., McNaughton, B.L. & O'Reilly, R.C. Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. Psychol. Rev. 102, 419–457 (1995).

    Article  Google Scholar 

  28. O'Reilly, R.C. & Rudy, J.W. Computational principles of learning in the neocortex and hippocampus. Hippocampus 10, 389–397 (2000).

    Article  CAS  Google Scholar 

  29. Vargha-Khadem, F. et al. Differential effects of early hippocampal pathology on episodic and semantic memory. Science 277, 376–380 (1997).

    Article  CAS  Google Scholar 

  30. Skotko, B. et al. Puzzling thoughts for H.M.: can new semantic information be anchored to old semantic memories? Neuropsychology 18, 756–769 (2004).

    Article  Google Scholar 

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

  32. Wechsler, D. Wechsler Memory Scale 3rd edn. (Psychological Corporation, New York, 1997).

    Google Scholar 

  33. Wechsler, D. Wechsler Adult Intelligence Scale 3rd edn. (Psychological Corporation, New York, 1997).

    Google Scholar 

  34. Elffers, J. & Schuyt, M. Tangram: 1600 Ancient Chinese Puzzles. (Barnes & Nobel, Hong Kong, 1997).

    Google Scholar 

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Acknowledgements

We thank W. Viechtbauer for conducting the statistical analyses, and K. McEnery, S. McWalter, C. Slovin and E. Whitebread for transcribing the sessions. This work was supported by grants from the US National Institute of Mental Health and National Science Foundation (N.J.C.) and the National Institute of Neurological Disorders and Stroke (D.T.).

Author information

Authors and Affiliations

  1. Beckman Institute, University of Illinois at Urbana-Champaign, 405 North Mathews Avenue, Urbana, 61801, Illinois, USA

    Melissa C Duff & Neal J Cohen

  2. Department of Speech and Hearing Science, University of Illinois at Urbana-Champaign, 901 South Sixth Street, Champaign, 61820, Illinois, USA

    Melissa C Duff & Julie Hengst

  3. Department of Neurology, University of Iowa, 200 Hawkins Drive, 2100-RCP, Iowa City, 52242, Iowa, USA

    Daniel Tranel

Authors
  1. Melissa C Duff
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  2. Julie Hengst
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  3. Daniel Tranel
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  4. Neal J Cohen
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Corresponding author

Correspondence to Neal J Cohen.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

Total word counts per trial. (PDF 85 kb)

Supplementary Table 1

Demographic Information and Neuropsychological Assessment of Amnesic Participants (PDF 37 kb)

Supplementary Table 2

Card descriptions on trial 1 by an amnesic individual and partner (PDF 90 kb)

Supplementary Table 3 (PDF 40 kb)

Supplementary Methods (PDF 69 kb)

Supplementary Note (PDF 44 kb)

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Duff, M., Hengst, J., Tranel, D. et al. Development of shared information in communication despite hippocampal amnesia. Nat Neurosci 9, 140–146 (2006). https://doi.org/10.1038/nn1601

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