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Volume 16, Number 16, Issue of August 15, 1996 pp. 5154-5167
Copyright ©1996 Society for Neuroscience

Neural Mechanisms of Visual Working Memory in Prefrontal Cortex of the Macaque

Received March 8, 1996; revised May 23, 1996; accepted May 30, 1996.

Earl K. Miller1, 2, Cynthia A. Erickson1, and Robert Desimone1

1 Laboratory of Neuropsychology, National Institute of Mental Health, Bethesda, Maryland 20892-4415, and 2 Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139

Prefrontal (PF) cells were studied in monkeys performing a delayed matching to sample task, which requires working memory. The stimuli were complex visual patterns and to solve the task, the monkeys had to discriminate among the stimuli, maintain a memory of the sample stimulus during the delay periods, and evaluate whether a test stimulus matched the sample presented earlier in the trial. PF cells have properties consistent with a role in all three of these operations. Approximately 25% of the cells responded selectively to different visual stimuli. Half of the cells showed heightened activity during the delay after the sample and, for many of these cells, the magnitude of delay activity was selective for different samples. Finally, more than half of the cells responded differently to the test stimuli depending on whether they matched the sample. Because inferior temporal (IT) cortex also is important for working memory, we compared PF cells with IT cells studied in the same task. Compared with IT cortex, PF responses were less often stimulus-selective but conveyed more information about whether a given test stimulus was a match to the sample. Furthermore, sample-selective delay activity in PF cortex was maintained throughout the trial even when other test stimuli intervened during the delay, whereas delay activity in IT cortex was disrupted by intervening stimuli. The results suggest that PF cortex plays a primary role in working memory tasks and may be a source of feedback inputs to IT cortex, biasing activity in favor of behaviorally relevant stimuli.

Key words: inferior temporal cortex; memory; macaque; vision; neurophysiology; attention




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Cereb CortexHome page
Z. Kourtzi, M. Erb, W. Grodd, and H. H. Bulthoff
Representation of the Perceived 3-D Object Shape in the Human Lateral Occipital Complex
Cereb Cortex, September 1, 2003; 13(9): 911 - 920.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
J. D. Wallis and E. K. Miller
From Rule to Response: Neuronal Processes in the Premotor and Prefrontal Cortex
J Neurophysiol, September 1, 2003; 90(3): 1790 - 1806.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
K.-I. Tsutsui, M. Jiang, H. Sakata, and M. Taira
Short-Term Memory and Perceptual Decision for Three-Dimensional Visual Features in the Caudal Intraparietal Sulcus (Area CIP)
J. Neurosci., July 2, 2003; 23(13): 5486 - 5495.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
G. d'Avossa, G. L. Shulman, and M. Corbetta
Identification of Cerebral Networks by Classification of the Shape of BOLD Responses
J Neurophysiol, July 1, 2003; 90(1): 360 - 371.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
D. J. Freedman, M. Riesenhuber, T. Poggio, and E. K. Miller
A Comparison of Primate Prefrontal and Inferior Temporal Cortices during Visual Categorization
J. Neurosci., June 15, 2003; 23(12): 5235 - 5246.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
Y. Ninokura, H. Mushiake, and J. Tanji
Representation of the Temporal Order of Visual Objects in the Primate Lateral Prefrontal Cortex
J Neurophysiol, May 1, 2003; 89(5): 2868 - 2873.
[Abstract] [Full Text] [PDF]


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Cereb CortexHome page
D.J. Amit, A. Bernacchia, and V. Yakovlev
Multiple-object Working Memory--A Model for Behavioral Performance
Cereb Cortex, May 1, 2003; 13(5): 435 - 443.
[Abstract] [Full Text] [PDF]


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Cereb CortexHome page
R. J. Kyd and D. K. Bilkey
Prefrontal Cortex Lesions Modify the Spatial Properties of Hippocampal Place Cells
Cereb Cortex, May 1, 2003; 13(5): 444 - 451.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
H. C. Cromwell and W. Schultz
Effects of Expectations for Different Reward Magnitudes on Neuronal Activity in Primate Striatum
J Neurophysiol, May 1, 2003; 89(5): 2823 - 2838.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
P. R. Roelfsema, P. S. Khayat, and H. Spekreijse
Subtask sequencing in the primary visual cortex
PNAS, April 29, 2003; 100(9): 5467 - 5472.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
D. J. Freedman, M. Riesenhuber, T. Poggio, and E. K. Miller
Visual Categorization and the Primate Prefrontal Cortex: Neurophysiology and Behavior
J Neurophysiol, August 1, 2002; 88(2): 929 - 941.
[Abstract] [Full Text] [PDF]


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Cereb CortexHome page
M. H.J. Munk, D. E.J. Linden, L. Muckli, H. Lanfermann, F. E. Zanella, W. Singer, and R. Goebel
Distributed Cortical Systems in Visual Short-term Memory Revealed by Event-related Functional Magnetic Resonance Imaging
Cereb Cortex, August 1, 2002; 12(8): 866 - 876.
[Abstract] [Full Text] [PDF]


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Behav Cogn Neurosci RevHome page
M. A. Lebedev and S. P. Wise
Insights into seeing and grasping: distinguishing the neural correlates of perception and action.
Behav Cogn Neurosci Rev, June 1, 2002; 1(2): 108 - 129.
[Abstract] [PDF]


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J. Neurosci.Home page
M. Watanabe, K. Hikosaka, M. Sakagami, and S.-i. Shirakawa
Coding and Monitoring of Motivational Context in the Primate Prefrontal Cortex
J. Neurosci., March 15, 2002; 22(6): 2391 - 2400.
[Abstract] [Full Text] [PDF]



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