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The Journal of Neuroscience, February 28, 2007, 27(9):2204-2211; doi:10.1523/JNEUROSCI.4483-06.2007

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Behavioral/Systems/Cognitive
Prefrontal Neural Correlates of Memory for Sequences

Bruno B. Averbeck^1,2 and Daeyeol Lee^1,3

¹Department of Brain and Cognitive Sciences, Center for Visual Science, University of Rochester, Rochester, New York 14627, ²Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, University College London, London WC1N 3BG, United Kingdom, and ³Department of Neurobiology, Yale University School of Medicine, New Haven, Connecticut 06510

Correspondence should be addressed to Dr. Bruno B. Averbeck, University College London Institute of Neurology, Sobell Department, Box 28, Queen Square, London WC1N 3BG, UK. E-mail: Email: b.averbeck{at}ion.ucl.ac.uk

The sequence of actions appropriate to solve a problem often needs to be discovered by trial and error and recalled in the future when faced with the same problem. Here, we show that when monkeys had to discover and then remember a sequence of decisions across trials, ensembles of prefrontal cortex neurons reflected the sequence of decisions the animal would make throughout the interval between trials. This signal could reflect either an explicit memory process or a sequence-planning process that begins far in advance of the actual sequence execution. This finding extended to error trials such that, when the neural activity during the intertrial interval specified the wrong sequence, the animal also attempted to execute an incorrect sequence. More specifically, we used a decoding analysis to predict the sequence the monkey was planning to execute at the end of the fore-period, just before sequence execution. When this analysis was applied to error trials, we were able to predict where in the sequence the error would occur, up to three movements into the future. This suggests that prefrontal neural activity can retain information about sequences between trials, and that regardless of whether information is remembered correctly or incorrectly, the prefrontal activity veridically reflects the animal's action plan.

Key words: sequence; ensemble; monkey; executive control; neurophysiology; prefrontal cortex

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Received Oct. 13, 2006; revised Dec. 20, 2006; accepted Jan. 16, 2007.

Correspondence should be addressed to Dr. Bruno B. Averbeck, University College London Institute of Neurology, Sobell Department, Box 28, Queen Square, London WC1N 3BG, UK. E-mail: Email: b.averbeck{at}ion.ucl.ac.uk

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