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Science 10 March 1995:
Vol. 267. no. 5203, pp. 1512 - 1515
DOI: 10.1126/science.7878473

Articles

Science, Vol 267, Issue 5203, 1512-1515
Copyright © 1995 by American Association for the Advancement of Science


articles

Storage of 7 +/- 2 short-term memories in oscillatory subcycles

JE Lisman and MA Idiart

Department of Biology, Brandeis University, Waltham, MA 02254.

Psychophysical measurements indicate that human subjects can store approximately seven short-term memories. Physiological studies suggest that short-term memories are stored by patterns of neuronal activity. Here it is shown that activity patterns associated with multiple memories can be stored in a single neural network that exhibits nested oscillations similar to those recorded from the brain. Each memory is stored in a different high-frequency ("40 hertz") subcycle of a low-frequency oscillation. Memory patterns repeat on each low-frequency (5 to 12 hertz) oscillation, a repetition that relies on activity-dependent changes in membrane excitability rather than reverberatory circuits. This work suggests that brain oscillations are a timing mechanism for controlling the serial processing of short-term memories.


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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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