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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Wechsler, D. Wechsler Memory Scale-Revised (The Psychological Corporation, Harcourt Brace Jovanovich, San Antonio, 1987).
Meyer, V. & Yates, A. J. J. Neurol. Neurosurg. Psychiat. 18, 44–52 (1955).
Milner, B. Brain Mechanisms Underlying Speech and Language, 122–145 (Grune & Stratton, New York, 1967).
Jones, M. K. Neuropsychologia 12, 21–30 (1974).
Petrides, M. Neuropsychologia 23, 601–614 (1985).
Goldstein, L. H., Canavan, A. G. M. & Polkey, C. E. Cortex 24, 41–52 (1988).
Murray, E. A., Gaffan, D. & Mishkin, M. Soc. Neurosci. Abstr. 14, 2 (1988).
Miyashita, Y. & Chang, H. S. Nature 331, 68–70 (1988).
Miyashita, Y. Nature 335, 817–820 (1988).
Snedecor, G. W. & Cochran, W. G. Statistical Methods 8th edn, 97 (Iowa State University Press, Ames, 1989).
Perrett, D. I., Rolls, E. T. & Caan, W. Expl Brain Res. 47, 329–342 (1982).
Desimone, R., Albright, T. D., Gross, C. G. & Bruce, C. J. Neurosci. 4, 2051–2062 (1984).
Schwartz, E. L., Desimone, R., Albright, T. D. & Gross, C. G. Proc. natn. Acad. Sci. U.S.A. 80, 5776–5778 (1983).
Artola, A. & Singer, W. Nature 330, 649–652 (1987).
Frégnac, Y., Shulz, D., Thorpe, S. & Bienenstock, E. Nature 333, 367–370 (1988).
Bruce, C. J. & Goldberg, M. E. J. Neurophysiol. 53, 603–635 (1985).
Mauritz, K.-H. & Wise, S. P. Expl Brain Res. 61, 229–244 (1986).
Funahashi, S., Bruce, C. J. & Goldman-Rakic, P. S. J. Neurophysiol. 61, 331–349 (1989).
Milner, B. Clin. Neurosurg 19, 421–446 (1972).
Squire, L. R., Cohen, N. J. & Nadel, L. Memory Consolidation: Psychobiology of Cognition, 185–210 (Lawrence Erlbaum, Hillsdale, 1984).
Insausti, R., Amaral, D. G. & Cowan, W. M. J. comp. Neurol. 264, 356–395 (1987).
Webster, M. J., Ungerleider, L. G. & Bachevalier, J. J. Neurosci. 11, 1095–1116 (1991).
Zahn, C. T. & Roskies, R. Z. IEEE Trans. Comput. 21, 269–281 (1972).
Rolls, E. T. et al. J. Neurosci. 9, 1835–1845 (1989).
Gross, C. G., Rocha-Miranda, C. E. & Bender, D. B. J. Neurophysiol. 35, 96–111 (1972).
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Sakai, K., Miyashita, Y. Neural organization for the long-term memory of paired associates. Nature 354, 152–155 (1991). https://doi.org/10.1038/354152a0
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