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Can Delay-Period Activity Explain Working Memory?

Department of Neurobiology and Anatomy, University of Rochester Medical Center, Rochester, New York

Submitted 17 October 2003; accepted in final form 7 August 2004

Working-memory tasks often lead to elevated delay-period discharge rates in cortical neurons. When this altered neuronal discharge rate, called delay activity, shows stimulus specificity, it is a good candidate for a neuronal mechanism of working memory. If the delay activity is indeed the carrier of memory, then experimental manipulation during the delay period that disrupts delay activity should also disrupt behavioral performance. We tested this hypothesis in two macaque monkeys with a delayed matching-to-sample task (delay time: 8 or 10 s) in which only two visual images were used. In each trial, one of the images was randomly chosen as the sample. In control trials (without disruptive stimulation), the monkeys performed at the level of 74.3% correct recognition. Three electrical stimulation levels (mild: a 0.25-s train of electrical pulses; medium: 1-s train; strong: 4 s), delivered to the hippocampal formation or to the orbito-frontal and inferotemporal cortices during delay period, decreased the performance to 71.4, 66.8, and 58.0% respectively (all are significantly less than control performance, P < 0.05 for mild stimulation and P < 0.0001 for other stimulation levels). Three hundred and thirty-four cells were recorded from inferotemporal (211 cells) and prefrontal (123 cells) cortices. Significant (P < 0.05) stimulus-specific delay activity was found in about one-third of recorded cells. For these cells in control trials, the mean difference in delay-period spike rates between preferred and nonpreferred images was 26%. The electrical stimulation reduced this difference to 20% (not a statistically significant reduction) in trials with mild stimulation, to 14% (P < 0.05) with medium stimulation, and just to 4% (P < 0.0005) with strong stimulation. These results, that increasing electrical stimulation reduced neuronal selectivity and at the same time reduced behavioral performance, directly support the hypothesis that delay activity is the carrier of memory through the delay period.

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