Neurodynamics of cognitive set shifting in monkey frontal cortex and its causal impact on behavioral flexibility
Abstract
Flexible behavior depends on the ability to shift an internal cognitive set as soon as external demand changes. According to neuropsychological studies in human and nonhuman primates, selective lesion to the PFC impairs flexible behavioral shifting. Our previous fMRI study demonstrated that the prefrontal regions showed transient activation related to set shifting in humans and monkeys. To investigate the underlying neural processing, we recorded single-unit activities while monkeys performed a cognitive-set-shifting task, which required shifting between shape-matching and color-matching behaviors. We identified a group of neurons in the inferior arcuate region that exhibited selective activity when the monkeys were required to shift their cognitive set. These shift-related neurons were localized in the focal area along the posterior bank of the inferior arcuate sulcus. Reversible inactivation of this area ipsilateral to the response hand with a small volume of muscimol (even with 0.5 μl) selectively impaired the performance of behavioral shifting. Moreover, this selective behavioral impairment strongly correlated with the dose of muscimol. These results demonstrated localized neural processing for cognitive set shifting and its causal role for behavioral flexibility in primates.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Goal-related information used in cognitive flexibility tasks is primarily represented in the PFC in monkeys and humans.
“Goal-related information used in cognitive flexibility tasks is primarily represented in the PFC in monkeys (e.g. [56]) and humans [57].”
From Linking ADHD to the Neural Circuitry of Attention (2017) · cites this paper as [56]
Cites
Monsell, S. (2003) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(03)00028-7 · Cited by 2,984 · see citing works
Effects of Different Brain Lesions on Card Sorting: The Role of the Frontal Lobes
MILNER, B. (1963) · Archives of Neurology · doi:10.1001/archneur.1963.00460070100010 · Cited by 2,217 · see citing works
A Core System for the Implementation of Task Sets
Dosenbach, N. U. F., Visscher, K. M., Palmer, E. D., Miezin, F. M., Wenger, K. K., Kang, H. C., Burgund, E. D., Grimes, A. L., Schlaggar, B. L., & Petersen, S. E. (2006) · Neuron · doi:10.1016/j.neuron.2006.04.031 · Cited by 1,772 · see citing works
Dissociation in prefrontal cortex of affective and attentional shifts
Dias, R., Robbins, T. W., & Roberts, A. C. (1996) · Nature · doi:10.1038/380069a0 · Cited by 1,527 · see citing works
Rizzolatti, G., & Luppino, G. (2001) · Neuron · doi:10.1016/s0896-6273(01)00423-8 · Cited by 1,356 · see citing works
Shifting Intentional Set: Exploring the Dynamic Control of Tasks
(1994) · The MIT Press eBooks · doi:10.7551/mitpress/1478.003.0025 · Cited by 1,317 · see citing works
Reconfiguration of processing mode prior to task performance.
Meiran, N. (1996) · Journal of Experimental Psychology Learning Memory and Cognition · doi:10.1037/0278-7393.22.6.1423 · Cited by 1,155 · 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
Action sets and decisions in the medial frontal cortex
RUSHWORTH, M., WALTON, M., KENNERLEY, S., & BANNERMAN, D. (2004) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2004.07.009 · Cited by 1,004 · see citing works
Monchi, O., Petrides, M., Petre, V., Worsley, K., & Dagher, A. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-19-07733.2001 · Cited by 961 · see citing works
Petrides, M., & Pandya, D. N. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2001.02090.x · Cited by 882 · see citing works
Neural mechanisms of transient and sustained cognitive control during task switching.
Braver, T. S., Reynolds, J. R., & Donaldson, D. I. (2003) · Neuron · doi:10.1016/s0896-6273(03)00466-5 · Cited by 826 · see citing works
(1994) · The MIT Press eBooks · doi:10.7551/mitpress/1478.001.0001 · Cited by 749 · see citing works
Role for Cingulate Motor Area Cells in Voluntary Movement Selection Based on Reward
Shima, K., & Tanji, J. (1998) · Science · doi:10.1126/science.282.5392.1335 · Cited by 653 · see citing works
Motor areas in the frontal lobe of the primate
DUM, R., & STRICK, P. (2002) · Physiology & Behavior · doi:10.1016/s0031-9384(02)00929-0 · Cited by 653 · see citing works
The role of prefrontal cortex and posterior parietal cortex in task switching
Sohn, M.-H., Ursu, S., Anderson, J. R., Stenger, V. A., & Carter, C. S. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.240460497 · Cited by 552 · see citing works
Switching from automatic to controlled action by monkey medial frontal cortex
Isoda, M., & Hikosaka, O. (2007) · Nature Neuroscience · doi:10.1038/nn1830 · Cited by 430 · see citing works
Fogassi, L. (2001) · Brain · doi:10.1093/brain/124.3.571 · Cited by 429 · see citing works
Prefrontal interactions reflect future task operations
Sakai, K., & Passingham, R. E. (2002) · Nature Neuroscience · doi:10.1038/nn987 · Cited by 382 · see citing works
Direction of action is represented in the ventral premotor cortex
Kakei, S., Hoffman, D. S., & Strick, P. L. (2001) · Nature Neuroscience · doi:10.1038/nn726 · Cited by 373 · see citing works
Cortical mechanisms of space-based and object-based attentional control
Yantis, S., & Serences, J. T. (2003) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(03)00033-3 · Cited by 342 · see citing works
Neuronal Correlates of a Perceptual Decision in Ventral Premotor Cortex
Romo, R., Hernández, A., & Zainos, A. (2004) · Neuron · doi:10.1016/s0896-6273(03)00817-1 · Cited by 340 · see citing works
Orofacial somatomotor responses in the macaque monkey homologue of Broca's area
Petrides, M., Cadoret, G., & Mackey, S. (2005) · Nature · doi:10.1038/nature03628 · Cited by 337 · see citing works
Dissociable components of rule-guided behavior depend on distinct medial and prefrontal regions
Buckley, M. J., Mansouri, F. A., Hoda, H., Mahboubi, M., Browning, P. G. F., Kwok, S. C., Phillips, A., & Tanaka, K. (2009) · Science · doi:10.1126/science.1172377 · Cited by 319 · see citing works
Johnston, K., Levin, H., Koval, M. J., & Everling, S. (2007) · Neuron · doi:10.1016/j.neuron.2006.12.023 · Cited by 305 · see citing works
Functional MRI of macaque monkeys performing a cognitive set-shifting task
Nakahara, K., Hayashi, T., Konishi, S., & Miyashita, Y. (2002) · Science · doi:10.1126/science.1067653 · Cited by 286 · see citing works
Self-citationBichot, N. P., & Schall, J. D. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-11-04675.2002 · Cited by 251 · see citing works
Premotor cortex neurons in macaques: activity before distal and proximal forelimb movements
Kurata, K., & Tanji, J. (1986) · Journal of Neuroscience · doi:10.1523/jneurosci.06-02-00403.1986 · Cited by 232 · see citing works
Modulation of task-related neural activity in task-switching: An fMRI study.
Kimberg, D. Y., Aguirre, G. K., & D’Esposito, M. (2000) · Cognitive Brain Research · doi:10.1016/s0926-6410(00)00016-1 · Cited by 219 · see citing works
Muhammad, R., Wallis, J. D., & Miller, E. K. (2006) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2006.18.6.974 · Cited by 216 · see citing works
Kurata, K., & Hoffman, D. S. (1994) · Journal of Neurophysiology · doi:10.1152/jn.1994.71.3.1151 · Cited by 216 · see citing works
Prefrontal Cortex Activity Related to Abstract Response Strategies
Genovesio, A., Brasted, P. J., Mitz, A. R., & Wise, S. P. (2005) · Neuron · doi:10.1016/j.neuron.2005.06.006 · Cited by 205 · see citing works
Computational and neurobiological mechanisms underlying cognitive flexibility
Badre, D., & Wagner, A. D. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0509550103 · Cited by 199 · see citing works
Mansouri, F. A., Matsumoto, K., & Tanaka, K. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.5238-05.2006 · Cited by 196 · see citing works
Neural predictors of moment-to-moment fluctuations in cognitive flexibility
Leber, A. B., Turk‐Browne, N. B., & Chun, M. M. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0805423105 · Cited by 181 · see citing works
Chen, L. L., & Wise, S. P. (1995) · Journal of Neurophysiology · doi:10.1152/jn.1995.73.3.1122 · Cited by 161 · see citing works
Differential Representation of Perception and Action in the Frontal Cortex
Schwartz, A. B., Moran, D. W., & Reina, G. A. (2004) · Science · doi:10.1126/science.1087788 · Cited by 141 · see citing works
Non-reversal shifts after selective prefrontal ablations in monkeys (Macaca mulatta)
Passingham, R. E. (1972) · Neuropsychologia · doi:10.1016/0028-3932(72)90041-3 · Cited by 90 · see citing works
Neural correlates of executive control functions in the monkey
Stoet, G., & Snyder, L. H. (2009) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2009.02.002 · Cited by 81 · see citing works
Neural mechanism in anterior prefrontal cortex for inhibition of prolonged set interference
Konishi, S., Chikazoe, J., Jimura, K., Asari, T., & Miyashita, Y. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0500585102 · Cited by 62 · see citing works
Self-citationUnitized representation of paired objects in area 35 of the macaque perirhinal cortex
Fujimichi, R., Naya, Y., Koyano, K. W., et al. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07320.x · Cited by 51 · see citing works
Kurata, K., & Hoshi, E. (2002) · Journal of Neurophysiology · doi:10.1152/jn.00070.2002 · Cited by 50 · see citing works
Cognitive Set Reconfiguration Signaled by Macaque Posterior Parietal Neurons
Kamigaki, T., Fukushima, T., & Miyashita, Y. (2009) · Neuron · doi:10.1016/j.neuron.2009.01.028 · Cited by 46 · see citing works
Self-citationZhou, H., & Thompson, K. G. (2008) · Vision Research · doi:10.1016/j.visres.2008.03.024 · Cited by 31 · see citing works
Kurata, K. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00149.2007 · Cited by 23 · see citing works
In vivo visualization of single-unit recording sites using MRI-detectable elgiloy deposit marking
Koyano, K. W., Machino, A., Takeda, M., Matsui, T., Fujimichi, R., Ohashi, Y., & Miyashita, Y. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00358.2010 · Cited by 19 · see citing works
Self-citationKamigaki, T., Fukushima, T., & Miyashita, Y. (2011) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2011.21613 · Cited by 15 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Linking ADHD to the Neural Circuitry of Attention
Mueller, A., Hong, D. S., Shepard, S., & Moore, T. (2017) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2017.03.009 · Cited by 158 · see citing works
Khoury, J. E., & Milligan, K. (2019) · Journal of Attention Disorders · doi:10.1177/1087054715622016 · Cited by 30 · see citing works
- Authors
- Kamigaki, T., Fukushima, T., Tamura, K., & Miyashita, Y.
- Affiliations
- The University of Tokyo (JP)
- Japan Science and Technology Agency (JP)
- Venue
- Journal of Cognitive Neuroscience
- Publisher
- MIT Press
- Published
- 2012-11-01
- Volume
- 24
- Issue
- 11
- Pages
- 2171-2185
- ISSN
- 0898-929X (ISSN-L)
- 1530-8898
- OpenAlex
- W2046035408
- Cited by
- 25
- References
- 47
- Citations by year
- 2025: 2 · 2024: 2 · 2022: 1 · 2020: 2 · 2018: 4 · 2017: 3 · 2016: 4 · 2015: 1 · 2014: 2 · 2013: 3
- FWCI
- 0.98
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Cognitive Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- University of Tokyo
- Japan Society for the Promotion of Science (24220008)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- behavioral flexibility, prefrontal cortex, single-unit activity, muscimol inactivation, non-human primates, frontal lobe lesions
- MeSH terms
- Animals, Haplorhini, Choice Behavior, Cognition, Frontal Lobe, Macaca, Male, Photic Stimulation, Psychomotor Performance, Reaction Time
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review