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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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J. W. Bisley, D. Zaksas, J. A. Droll, and T. Pasternak
Activity of Neurons in Cortical Area MT During a Memory for Motion Task
J Neurophysiol,
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P. F. Balan and V. P. Ferrera
Effects of Spontaneous Eye Movements on Spatial Memory in Macaque Periarcuate Cortex
J. Neurosci.,
December 10, 2003;
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A. Compte,, C. Constantinidis, J. Tegner, S. Raghavachari, M. V. Chafee, P. S. Goldman-Rakic, and X.-J. Wang
Temporally Irregular Mnemonic Persistent Activity in Prefrontal Neurons of Monkeys During a Delayed Response Task
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November 1, 2003;
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G. N. Elston
Cortex, Cognition and the Cell: New Insights into the Pyramidal Neuron and Prefrontal Function
Cereb Cortex,
November 1, 2003;
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[Abstract]
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D. J. Amit and G. Mongillo
Selective Delay Activity in the Cortex: Phenomena and Interpretation
Cereb Cortex,
November 1, 2003;
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N. Brunel
Dynamics and Plasticity of Stimulus-selective Persistent Activity in Cortical Network Models
Cereb Cortex,
November 1, 2003;
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[Abstract]
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C. D. Brody, A. Hernandez, A. Zainos, and R. Romo
Timing and Neural Encoding of Somatosensory Parametric Working Memory in Macaque Prefrontal Cortex
Cereb Cortex,
November 1, 2003;
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[Abstract]
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D. A. McCormick, Y. Shu, A. Hasenstaub, M. Sanchez-Vives, M. Badoual, and T. Bal
Persistent Cortical Activity: Mechanisms of Generation and Effects on Neuronal Excitability
Cereb Cortex,
November 1, 2003;
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[Abstract]
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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;
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[Abstract]
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J. D. Wallis and E. K. Miller
From Rule to Response: Neuronal Processes in the Premotor and Prefrontal Cortex
J Neurophysiol,
September 1, 2003;
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[Abstract]
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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;
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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;
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[Abstract]
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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;
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[Abstract]
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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;
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[Abstract]
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D.J. Amit, A. Bernacchia, and V. Yakovlev
Multiple-object Working Memory--A Model for Behavioral Performance
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May 1, 2003;
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R. J. Kyd and D. K. Bilkey
Prefrontal Cortex Lesions Modify the Spatial Properties of Hippocampal Place Cells
Cereb Cortex,
May 1, 2003;
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[Abstract]
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H. C. Cromwell and W. Schultz
Effects of Expectations for Different Reward Magnitudes on Neuronal Activity in Primate Striatum
J Neurophysiol,
May 1, 2003;
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P. R. Roelfsema, P. S. Khayat, and H. Spekreijse
Subtask sequencing in the primary visual cortex
PNAS,
April 29, 2003;
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[Abstract]
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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;
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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
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August 1, 2002;
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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;
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[Abstract]
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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;
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