The prefrontal cortex and working memory: physiology and brain imaging

Passingham, Dick; Sakai, Katsuyuki

doi:10.1016/j.conb.2004.03.003

Cited by 207Neural and Behavioral Psychology StudiesCognitive Abilities and TestingNeural dynamics and brain function

The prefrontal cortex and working memory: physiology and brain imaging

Passingham, Dick, Sakai, Katsuyuki·2004·Current Opinion in Neurobiology

DOI 10.1016/j.conb.2004.03.003

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Abstract

Sustained activity has been recorded in the prefrontal cortex during working memory tasks. First, we compare the anatomical distribution of this activity in humans and monkeys. Then, we show that it reflects many factors, maintenance of the items presented, preparation for the response, transformation of the items during the delay, task rules and task goals. Finally, we point out that sustained activity has also been recorded in other areas, such as the parietal cortex. We suggest that the key to prefrontal cortex lies not in the maintenance of sensory information but in the prospective use of that information for behaviour.

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Memory traces in neural signals are mixed with other task-dependent factors.
“Memory traces in the neural signals are mixed with other task-dependent factors44,45, and it has been debated whether other processes involved in goal-directed behavior could be mistakenly identified as memory, such as spatial attention46, motor planning47, anticipation of future events48, or timing49.”
From A reservoir of time constants for memory traces in cortical neurons (2011) · cites this paper as [45]

An Integrative Theory of Prefrontal Cortex Function
Miller, E. K., & Cohen, J. D. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.167 · Cited by 12,803 · see citing works
Working memory: Looking back and looking forward
Baddeley, A. (2003) · Nature Reviews Neuroscience · doi:10.1038/nrn1201 · Cited by 5,200 · see citing works
Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex
Funahashi, S., Bruce, C. J., & Goldman-Rakic, P. S. (1989) · Journal of Neurophysiology · doi:10.1152/jn.1989.61.2.331 · Cited by 2,685 · see citing works
Persistent activity in the prefrontal cortex during working memory
Curtis, C. E., & D'Esposito, M. (2003) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(03)00197-9 · Cited by 2,001 · see citing works
Circuitry of Primate Prefrontal Cortex and Regulation of Behavior by Representational Memory
Goldman‐Rakic, P. S. (1987) · Comprehensive Physiology · doi:10.1002/cphy.cp010509 · Cited by 1,960 · see citing works
Principles of Frontal Lobe Function
Stuss, D. T. (2002) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195134971.001.0001 · Cited by 1,708 · see citing works
Neural responses during anticipation of a primary taste reward
O'Doherty, J. P., Deichmann, R., Critchley, H. D., & Dolan, R. J. (2002) · Neuron · doi:10.1016/s0896-6273(02)00603-7 · Cited by 1,076 · see citing works
Single neurons in prefrontal cortex encode abstract rules
Wallis, J. D., Anderson, K. C., & Miller, E. K. (2001) · Nature · doi:10.1038/35082081 · Cited by 1,075 · see citing works
Dorsolateral prefrontal cortex: comparative cytoarchitectonic analysis in the human and the macaque brain and corticocortical connection patterns
Petrides, M., & Pandya, D. N. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00518.x · Cited by 1,068 · see citing works
The anatomical basis of functional localization in the cortex
Passingham, R. E., Stephan, K. E., & Kötter, R. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn893 · Cited by 1,024 · see citing works
An area specialized for spatial working memory in human frontal cortex.
Courtney, S., Petit, L., Maisog, J., Ungerleider, L. G., & Haxby, J. (1998) · Science · doi:10.1126/science.279.5355.1347 · Cited by 1,010 · see citing works
Reward processing in primate orbitofrontal cortex and basal ganglia
Schultz, W. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.3.272 · Cited by 942 · see citing works
Common cortical and subcortical targets of the dorsolateral prefrontal and posterior parietal cortices in the rhesus monkey: evidence for a distributed neural network subserving spatially guided behavior
Selemon, L. D., & Goldman-Rakic, P. S. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-11-04049.1988 · Cited by 908 · see citing works
Connections underlying the synthesis of cognition, memory, and emotion in primate prefrontal cortices
Barbas, H. (2000) · Brain Research Bulletin · doi:10.1016/s0361-9230(99)00245-2 · Cited by 664 · see citing works
Matching Patterns of Activity in Primate Prefrontal Area 8a and Parietal Area 7ip Neurons During a Spatial Working MemoryTask
Chafee, M. V., & Goldman, P. S. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.79.6.2919 · Cited by 655 · see citing works
Dissociating valence of outcome from behavioral control in human orbital and ventral prefrontal cortices
O'Doherty, J., Critchley, H., Deichmann, R., & Dolan, R. J. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-21-07931.2003 · Cited by 611 · see citing works
Executive frontal functions
Fuster, J. M. (2000) · Experimental Brain Research · doi:10.1007/s002210000401 · Cited by 558 · see citing works
Effect of Expected Reward Magnitude on the Response of Neurons in the Dorsolateral Prefrontal Cortex of the Macaque
Leon, M. I., & Shadlen, M. N. (1999) · Neuron · doi:10.1016/s0896-6273(00)80854-5 · Cited by 449 · see citing works
Neural Correlates of Visual Working Memory
Pessoa, L., Gutiérrez, E., Bandettini, P. A., & Ungerleider, L. G. (2002) · Neuron · doi:10.1016/s0896-6273(02)00817-6 · Cited by 444 · see citing works
Prospective coding for objects in primate prefrontal cortex
Rainer, G., Rao, S. C., & Miller, E. K. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-13-05493.1999 · Cited by 432 · cited 1× · see citing works
“of object X [25].”
The neural system that bridges reward and cognition in humans: An fMRI study
Pochon, J.-B., Lévy, R., Fossati, P., Lehéricy, S., Poline, J.-B., Pillon, B., Bihan, D. L., & Dubois, B. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.082111099 · Cited by 431 · see citing works
Inactivation of Parietal and Prefrontal Cortex Reveals Interdependence of Neural Activity During Memory-Guided Saccades
Chafee, M. V., & Goldman, P. S. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.83.3.1550 · Cited by 406 · see citing works
Active maintenance in prefrontal area 46 creates distractor-resistant memory
Sakai, K., Rowe, J. B., & Passingham, R. E. (2002) · Nature Neuroscience · doi:10.1038/nn846 · Cited by 390 · see citing works
Self-citation
Prefrontal interactions reflect future task operations
Sakai, K., & Passingham, R. E. (2002) · Nature Neuroscience · doi:10.1038/nn987 · Cited by 382 · see citing works
Self-citation
Encoding Strategies Dissociate Prefrontal Activity from Working Memory Demand
Bor, D., Duncan, J., Wiseman, R. J., & Owen, A. M. (2003) · Neuron · doi:10.1016/s0896-6273(02)01171-6 · Cited by 373 · see citing works
Neural Circuits Subserving the Retrieval and Maintenance of Abstract Rules
Bunge, S. A., Kahn, I., Wallis, J. D., Miller, E. K., & Wagner, A. D. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00910.2002 · Cited by 361 · see citing works
From Rule to Response: Neuronal Processes in the Premotor and Prefrontal Cortex
Wallis, J. D., & Miller, E. K. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00086.2003 · Cited by 352 · see citing works
The dependence of span and delayed-response performance on prefrontal cortex.
D’Esposito, M., & Postle, B. R. (1999) · Neuropsychologia · doi:10.1016/s0028-3932(99)00021-4 · Cited by 350 · see citing works
Functional neuroanatomical double dissociation of mnemonic and executive control processes contributing to working memory performance
Postle, B. R., Berger, J. S., & D’Esposito, M. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.22.12959 · Cited by 341 · see citing works
Sustained Mnemonic Response in the Human Middle Frontal Gyrus during On-Line Storage of Spatial Memoranda
Leung, H.-C., Gore, J. C., & Goldman-Rakic, P. S. (2002) · Journal of Cognitive Neuroscience · doi:10.1162/08989290260045882 · Cited by 314 · see citing works
The Role of Dorsolateral Prefrontal Cortex in the Preparation of Forthcoming Actions: an fMRI Study
Pochon, J.-B. (2001) · Cerebral Cortex · doi:10.1093/cercor/11.3.260 · Cited by 296 · see citing works
Redefining the functional organization of working memory processes within human lateral prefrontal cortex
Owen, A. M., Herrod, N. J., Menon, D. K., Clark, J. C., Downey, S. P. M. J., Carpenter, T. A., Minhas, P. S., Turkheimer, F., Williams, E., Robbins, T. W., et al. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00449.x · Cited by 281 · see citing works
Attention to Action: Specific Modulation of Corticocortical Interactions in Humans
Rowe, J. B., Friston, K. J., Frackowiak, R. S. J., & Passingham, R. E. (2002) · NeuroImage · doi:10.1006/nimg.2002.1156 · Cited by 219 · see citing works
Dissecting Contributions of Prefrontal Cortex and Fusiform Face Area to Face Working Memory
Druzgal, T. J., & D’Esposito, M. (2003) · Journal of Cognitive Neuroscience · doi:10.1162/089892903322370708 · Cited by 213 · see citing works
Influence of Reward Expectation on Visuospatial Processing in Macaque Lateral Prefrontal Cortex
Kobayashi, S., Lauwereyns, J., Koizumi, M., Sakagami, M., & Hikosaka, O. (2002) · Journal of Neurophysiology · doi:10.1152/jn.00472.2001 · Cited by 206 · see citing works
Neuronal Activity in the Primate Prefrontal Cortex in the Process of Motor Selection Based on Two Behavioral Rules
Hoshi, E., Shima, K., & Tanji, J. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.83.4.2355 · Cited by 204 · see citing works
Prefrontal Task-Related Activity Representing Visual Cue Location or Saccade Direction in Spatial Working Memory Tasks
Takeda, K., & Funahashi, S. (2002) · Journal of Neurophysiology · doi:10.1152/jn.00249.2001 · Cited by 201 · see citing works
Working Memory for Location and Time: Activity in Prefrontal Area 46 Relates to Selection Rather than Maintenance in Memory
Rowe, J. B., & Passingham, R. E. (2001) · NeuroImage · doi:10.1006/nimg.2001.0784 · Cited by 199 · see citing works
Functional topography of a distributed neural system for spatial and nonspatial information maintenance in working memory
Sala, J. B., Pia Rämä, A., & Courtney, S. M. (2002) · Neuropsychologia · doi:10.1016/s0028-3932(02)00166-5 · Cited by 191 · see citing works
Coding and Monitoring of Motivational Context in the Primate Prefrontal Cortex
Watanabe, M., Hikosaka, K., Sakagami, M., & Shirakawa, S. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-06-02391.2002 · Cited by 159 · see citing works
The Influence of Memory Load Upon Delay-Interval Activity in a Working-Memory Task: An Event-Related Functional MRI Study
Jha, A. P., & McCarthy, G. (2000) · Journal of Cognitive Neuroscience · doi:10.1162/089892900564091 · Cited by 158 · see citing works
Activity in Human Frontal Cortex Associated with Spatial Working Memory and Saccadic Behavior
Postle, B. R., Berger, J. S., Taich, A. M., & D’Esposito, M. (2000) · Journal of Cognitive Neuroscience · doi:10.1162/089892900564028 · Cited by 147 · see citing works
Temporal isolation of the neural correlates of spatial mnemonic processing with fMRI
Zarahn, E., Aguirre, G. K., & D’Esposito, M. (1999) · Cognitive Brain Research · doi:10.1016/s0926-6410(98)00029-9 · Cited by 135 · see citing works
Functional Architecture of the Dorsolateral Prefrontal Cortex in Monkeys and Humans
Goldman, P. S., & Leung, H. (2002) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195134971.003.0005 · Cited by 93 · see citing works
Instructed Delay Activity in the Human Prefrontal Cortex is Modulated by Monetary Reward Expectation
Ramnani, N. (2003) · Cerebral Cortex · doi:10.1093/cercor/13.3.318 · Cited by 91 · see citing works
Properties of Delay-Period Neuronal Activity in the Monkey Dorsolateral Prefrontal Cortex During a Spatial Delayed Matching-to-Sample Task
Sawaguchi, T., & Yamane, I. (1999) · Journal of Neurophysiology · doi:10.1152/jn.1999.82.5.2070 · Cited by 90 · see citing works
Models of Functional Organization of the Lateral Prefrontal Cortex in Verbal Working Memory: Evidence in Favor of the Process Model
Barde, L. H. F., & Thompson‐Schill, S. L. (2002) · Journal of Cognitive Neuroscience · doi:10.1162/089892902320474508 · Cited by 90 · see citing works
Functional analysis of spatially discriminative neurons in prefrontal cortex of rhesus monkey
Kojima, S., & Goldman‐Rakic, P. S. (1984) · Brain Research · doi:10.1016/0006-8993(84)91255-1 · Cited by 87 · see citing works
Information Processes in the Primate Prefrontal Cortex in Relation to Working Memory Processes
Funahashi, S., & Takeda, K. (2002) · Reviews in the Neurosciences · doi:10.1515/revneuro.2002.13.4.313 · Cited by 68 · see citing works
The role of spatial configuration in tests of working memory explored with functional neuroimaging
Bor, D., Duncan, J., & Owen, A. M. (2001) · Scandinavian Journal of Psychology · doi:10.1111/1467-9450.00232 · Cited by 43 · see citing works
Dorsal Prefrontal Cortex: Maintenance in Memory or Attentional Selection?
Passingham, R. E., & Rowe, J. B. (2002) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195134971.003.0014 · Cited by 36 · see citing works
Prefrontal cortex and attention to action
Passingham, R. E., Rowe, J. B., & Sakai, K. (2010) · Taylor & Francis eBooks · doi:10.4324/9780203449226_chapter_11 · Cited by 4 · see citing works
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Cieslik, E. C., Zilles, K., Caspers, S., Roski, C., Kellermann, T. S., Jakobs, O., Langner, R., Laird, A. R., Fox, P. T., & Eickhoff, S. B. (2013) · Cerebral Cortex · doi:10.1093/cercor/bhs256 · Cited by 391 · see citing works
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Testa, R., & Pantelis, C. (2009) · The Neuropsychology of Mental Illness · doi:10.1017/cbo9780511642197.012 · Cited by 25 · see citing works

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Authors: Passingham, D., & Sakai, K.
Affiliations: University of Oxford (GB)
University College London (GB)
Corresponding author: Passingham, Dick
Sakai, Katsuyuki
Venue: Current Opinion in Neurobiology
Publisher: Elsevier BV
Published: 2004-04
Volume: 14
Issue: 2
Pages: 163-168
ISSN: 0959-4388 (ISSN-L)
DOI: 10.1016/j.conb.2004.03.003
OpenAlex: W1973267026
Cited by: 207
References: 52
Citations by year: 2025: 2 · 2024: 7 · 2023: 6 · 2022: 4 · 2021: 4 · 2020: 3 · 2019: 5 · 2018: 3 · 2017: 7 · 2016: 7 · 2015: 10 · 2014: 5 · 2013: 6 · 2012: 13
FWCI: 1.72
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Current Opinion in Neurobiology (publishedVersion)
PubMed (publishedVersion)
Funders: Wellcome Trust
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Social Sciences › Psychology › Experimental and Cognitive Psychology › Cognitive Abilities and Testing
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Keywords: prefrontal cortex, working memory, sustained neural activity, human-monkey comparison, parietal cortex, response preparation, task rules, task goals, memory maintenance
MeSH terms: Animals, Cues, Discrimination Learning, Goals, Humans, Magnetic Resonance Imaging, Memory, Short-Term, Neural Pathways, Neuropsychological Tests, Species Specificity, Prefrontal Cortex

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The prefrontal cortex and working memory: physiology and brain imaging

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