Prefrontal Neural Correlates of Memory for Sequences

Overview

Journal J Neurosci

Specialty Neurology

Date 2007 Mar 3

PMID 17329417

Citations 44

Authors

Bruno B Averbeck

Daeyeol Lee

Affiliations

Soon will be listed here.

Abstract

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.

Citing Articles

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References

Kim J, Shadlen M . Neural correlates of a decision in the dorsolateral prefrontal cortex of the macaque. Nat Neurosci. 1999; 2(2):176-85. DOI: 10.1038/5739. View

Procyk E, Tanaka Y, Joseph J . Anterior cingulate activity during routine and non-routine sequential behaviors in macaques. Nat Neurosci. 2000; 3(5):502-8. DOI: 10.1038/74880. View

Asaad W, Rainer G, Miller E . Task-specific neural activity in the primate prefrontal cortex. J Neurophysiol. 2000; 84(1):451-9. DOI: 10.1152/jn.2000.84.1.451. View

Compte A, Brunel N, Goldman-Rakic P, Wang X . Synaptic mechanisms and network dynamics underlying spatial working memory in a cortical network model. Cereb Cortex. 2000; 10(9):910-23. DOI: 10.1093/cercor/10.9.910. View

Shima K, Tanji J . Neuronal activity in the supplementary and presupplementary motor areas for temporal organization of multiple movements. J Neurophysiol. 2000; 84(4):2148-60. DOI: 10.1152/jn.2000.84.4.2148. View

Lu X, Matsuzawa M, Hikosaka O . A neural correlate of oculomotor sequences in supplementary eye field. Neuron. 2002; 34(2):317-25. DOI: 10.1016/s0896-6273(02)00657-8. View

Averbeck B, Chafee M, Crowe D, Georgopoulos A . Parallel processing of serial movements in prefrontal cortex. Proc Natl Acad Sci U S A. 2002; 99(20):13172-7. PMC: 130605. DOI: 10.1073/pnas.162485599. View

Wang X . Probabilistic decision making by slow reverberation in cortical circuits. Neuron. 2002; 36(5):955-68. DOI: 10.1016/s0896-6273(02)01092-9. View

Averbeck B, Chafee M, Crowe D, Georgopoulos A . Neural activity in prefrontal cortex during copying geometrical shapes. I. Single cells encode shape, sequence, and metric parameters. Exp Brain Res. 2003; 150(2):127-41. DOI: 10.1007/s00221-003-1416-6. View

10.

Averbeck B, Crowe D, Chafee M, Georgopoulos A . Neural activity in prefrontal cortex during copying geometrical shapes. II. Decoding shape segments from neural ensembles. Exp Brain Res. 2003; 150(2):142-53. DOI: 10.1007/s00221-003-1417-5. View

11.

Britten K, Shadlen M, Newsome W, Movshon J . The analysis of visual motion: a comparison of neuronal and psychophysical performance. J Neurosci. 1992; 12(12):4745-65. PMC: 6575768. View

12.

Chafee M, Crowe D, Averbeck B, Georgopoulos A . Neural correlates of spatial judgement during object construction in parietal cortex. Cereb Cortex. 2005; 15(9):1393-413. DOI: 10.1093/cercor/bhi021. View

13.

Pasupathy A, Miller E . Different time courses of learning-related activity in the prefrontal cortex and striatum. Nature. 2005; 433(7028):873-6. DOI: 10.1038/nature03287. View

14.

Osborne L, Lisberger S, Bialek W . A sensory source for motor variation. Nature. 2005; 437(7057):412-6. PMC: 2551316. DOI: 10.1038/nature03961. View

15.

Messinger A, Squire L, Zola S, Albright T . Neural correlates of knowledge: stable representation of stimulus associations across variations in behavioral performance. Neuron. 2005; 48(2):359-71. PMC: 1480361. DOI: 10.1016/j.neuron.2005.08.035. View

16.

de Lafuente V, Romo R . Neuronal correlates of subjective sensory experience. Nat Neurosci. 2005; 8(12):1698-703. DOI: 10.1038/nn1587. View

17.

Averbeck B, Sohn J, Lee D . Activity in prefrontal cortex during dynamic selection of action sequences. Nat Neurosci. 2006; 9(2):276-82. DOI: 10.1038/nn1634. View

18.

Mansouri F, Matsumoto K, Tanaka K . Prefrontal cell activities related to monkeys' success and failure in adapting to rule changes in a Wisconsin Card Sorting Test analog. J Neurosci. 2006; 26(10):2745-56. PMC: 6675148. DOI: 10.1523/JNEUROSCI.5238-05.2006. View

19.

Averbeck B, Lee D . Effects of noise correlations on information encoding and decoding. J Neurophysiol. 2006; 95(6):3633-44. DOI: 10.1152/jn.00919.2005. View

20.

Mushiake H, Saito N, Sakamoto K, Itoyama Y, Tanji J . Activity in the lateral prefrontal cortex reflects multiple steps of future events in action plans. Neuron. 2006; 50(4):631-41. DOI: 10.1016/j.neuron.2006.03.045. View