Neural organization for the long-term memory of paired associates


MOST of our long-term memories of episodes or objects are organized so that we can retrieve them by association. Clinical neuropsychologists assess human memory by the paired-associate learning test, in which a series of paired words or figures is presented and the subject is then asked to retrieve the other pair member associated with each cue1. Patients with lesions of the temporal lobe show marked impairment in this test2–6. In our study, we trained monkeys in a pair-association task7 using a set of computer-generated paired patterns. We found two types of task-related neurons in the anterior temporal cortex. One type selectively responded to both pictures of the paired associates. The other type, which had the strongest response to one picture during the cue presentation, exhibited increasing activity during the delay period when the associate of that picture was used as a cue. These results provide new evidence that single neurons acquire selectivity for visual patterns through associative learning. They also indicate neural mechanisms for storage and retrieval in the long-term memory of paired associates.

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  1. 1

    Wechsler, D. Wechsler Memory Scale-Revised (The Psychological Corporation, Harcourt Brace Jovanovich, San Antonio, 1987).

    Google Scholar 

  2. 2

    Meyer, V. & Yates, A. J. J. Neurol. Neurosurg. Psychiat. 18, 44–52 (1955).

    Article  Google Scholar 

  3. 3

    Milner, B. Brain Mechanisms Underlying Speech and Language, 122–145 (Grune & Stratton, New York, 1967).

    Google Scholar 

  4. 4

    Jones, M. K. Neuropsychologia 12, 21–30 (1974).

    CAS  Article  Google Scholar 

  5. 5

    Petrides, M. Neuropsychologia 23, 601–614 (1985).

    CAS  Article  Google Scholar 

  6. 6

    Goldstein, L. H., Canavan, A. G. M. & Polkey, C. E. Cortex 24, 41–52 (1988).

    CAS  Article  Google Scholar 

  7. 7

    Murray, E. A., Gaffan, D. & Mishkin, M. Soc. Neurosci. Abstr. 14, 2 (1988).

    Google Scholar 

  8. 8

    Miyashita, Y. & Chang, H. S. Nature 331, 68–70 (1988).

    ADS  CAS  Article  Google Scholar 

  9. 9

    Miyashita, Y. Nature 335, 817–820 (1988).

    ADS  CAS  Article  Google Scholar 

  10. 10

    Snedecor, G. W. & Cochran, W. G. Statistical Methods 8th edn, 97 (Iowa State University Press, Ames, 1989).

    Google Scholar 

  11. 11

    Perrett, D. I., Rolls, E. T. & Caan, W. Expl Brain Res. 47, 329–342 (1982).

    CAS  Article  Google Scholar 

  12. 12

    Desimone, R., Albright, T. D., Gross, C. G. & Bruce, C. J. Neurosci. 4, 2051–2062 (1984).

    CAS  Article  Google Scholar 

  13. 13

    Schwartz, E. L., Desimone, R., Albright, T. D. & Gross, C. G. Proc. natn. Acad. Sci. U.S.A. 80, 5776–5778 (1983).

    ADS  CAS  Article  Google Scholar 

  14. 14

    Artola, A. & Singer, W. Nature 330, 649–652 (1987).

    ADS  CAS  Article  Google Scholar 

  15. 15

    Frégnac, Y., Shulz, D., Thorpe, S. & Bienenstock, E. Nature 333, 367–370 (1988).

    ADS  Article  Google Scholar 

  16. 16

    Bruce, C. J. & Goldberg, M. E. J. Neurophysiol. 53, 603–635 (1985).

    CAS  Article  Google Scholar 

  17. 17

    Mauritz, K.-H. & Wise, S. P. Expl Brain Res. 61, 229–244 (1986).

    CAS  Article  Google Scholar 

  18. 18

    Funahashi, S., Bruce, C. J. & Goldman-Rakic, P. S. J. Neurophysiol. 61, 331–349 (1989).

    CAS  Article  Google Scholar 

  19. 19

    Milner, B. Clin. Neurosurg 19, 421–446 (1972).

    CAS  Article  Google Scholar 

  20. 20

    Squire, L. R., Cohen, N. J. & Nadel, L. Memory Consolidation: Psychobiology of Cognition, 185–210 (Lawrence Erlbaum, Hillsdale, 1984).

    Google Scholar 

  21. 21

    Insausti, R., Amaral, D. G. & Cowan, W. M. J. comp. Neurol. 264, 356–395 (1987).

    CAS  Article  Google Scholar 

  22. 22

    Webster, M. J., Ungerleider, L. G. & Bachevalier, J. J. Neurosci. 11, 1095–1116 (1991).

    CAS  Article  Google Scholar 

  23. 23

    Zahn, C. T. & Roskies, R. Z. IEEE Trans. Comput. 21, 269–281 (1972).

    Article  Google Scholar 

  24. 24

    Rolls, E. T. et al. J. Neurosci. 9, 1835–1845 (1989).

    CAS  Article  Google Scholar 

  25. 25

    Gross, C. G., Rocha-Miranda, C. E. & Bender, D. B. J. Neurophysiol. 35, 96–111 (1972).

    CAS  Article  Google Scholar 

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Sakai, K., Miyashita, Y. Neural organization for the long-term memory of paired associates. Nature 354, 152–155 (1991).

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