Successful choice behavior is associated with distinct and coherent network states in anterior cingulate cortex
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Successful decision making requires an ability to monitor contexts, actions, and outcomes. The anterior cingulate cortex (ACC) is thought to be critical for these functions, monitoring and guiding decisions especially in challenging situations involving conflict and errors. A number of different single-unit correlates have been observed in the ACC that reflect the diverse cognitive components involved. Yet how ACC neurons function as an integrated network is poorly understood. Here we show, using advanced population analysis of multiple single-unit recordings from the rat ACC during performance of an ecologically valid decision-making task, that ensembles of neurons move through different coherent and dissociable states as the cognitive requirements of the task change. This organization into distinct network patterns with respect to both firing-rate changes and correlations among units broke down during trials with numerous behavioral errors, especially at choice points of the task. These results point to an underlying functional organization into cell assemblies in the ACC that may monitor choices, outcomes, and task contexts, thus tracking the animal's progression through “task space.”
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The activity of neurons varied substantially in different trial epochs (99% of neurons, 675/681, ANOVA p<0.05).
“Consistent with previous studies23-25, we found that the activity of neurons varied substantially in different trial epochs (99% of neurons, 675/681, ANOVA p<0.05).”
From A reservoir of time constants for memory traces in cortical neurons (2011) · cites this paper as [23]
Cites
A Simple Sequentially Rejective Multiple Test Procedure
(1979) · Scandinavian Journal of Statistics · doi:10.2307/4615733 · Cited by 21,526 · see citing works
The attention system of the human brain
Posner, M. I., & Petersen, S. E. (1990) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.13.030190.000325 · Cited by 8,070 · cited 1× · see citing works
“This high degree of flexibility and context dependence supports the view of the ACC as a device for monitoring or attending to actions (16, 17).”
BackgroundConflict monitoring and cognitive control
Botvinick, M. M., Braver, T. S., Barch, D. M., Carter, C. S., & Cohen, J. D. (2001) · Psychological Review · doi:10.1037/0033-295x.108.3.624 · Cited by 7,351 · see citing works
Visual Feature Integration and the Temporal Correlation Hypothesis
Singer, W., & Gray, C. M. (1995) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.18.030195.003011 · Cited by 3,157 · see citing works
Squire, L. R., Stark, C. E. L., & Clark, R. E. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144130 · Cited by 2,680 · see citing works
Motor Areas of the Medial Wall: A Review of Their Location and Functional Activation
Picard, N., & Strick, P. L. (1996) · Cerebral Cortex · doi:10.1093/cercor/6.3.342 · Cited by 1,712 · see citing works
The Timing of Action-Monitoring Processes in the Anterior Cingulate Cortex
van Veen, V., & Carter, C. S. (2002) · Journal of Cognitive Neuroscience · doi:10.1162/08989290260045837 · Cited by 1,288 · 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
Spike Synchronization and Rate Modulation Differentially Involved in Motor Cortical Function
Riehle, A., Grün, S., Diesmann, M., & Aertsen, A. (1997) · Science · doi:10.1126/science.278.5345.1950 · Cited by 895 · see citing works
Organization of cell assemblies in the hippocampus
Harris, K. D., Csicsvari, J., Hirase, H., Dragoi, G., & Buzsáki, G. (2003) · Nature · doi:10.1038/nature01834 · Cited by 869 · see citing works
Principles of Multivariate Analysis
Ling, R. F., & Krzanowski, W. J. (1990) · Technometrics · doi:10.2307/1268873 · Cited by 809 · see citing works
Neurocomputational models of working memory
Durstewitz, D., Seamans, J. K., & B, T. J. S. A. (2000) · Nature Neuroscience · doi:10.1038/81460 · Cited by 710 · see citing works
Self-citationDevelopment and plasticity of cortical processing architectures
Singer, W. (1995) · Science · doi:10.1126/science.270.5237.758 · Cited by 669 · 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
Performance monitoring by the anterior cingulate cortex during saccade countermanding
Ito, S., Stuphorn, V., Brown, J. W., & Schall, J. D. (2003) · Science · doi:10.1126/science.1087847 · Cited by 581 · see citing works
Population coding of shape in area V4
Pasupathy, A., & Connor, C. E. (2002) · Nature Neuroscience · doi:10.1038/972 · Cited by 552 · see citing works
Fuster, J. M. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(97)01128-4 · Cited by 516 · see citing works
Prefrontal and cingulate unit activity during timing behavior in the monkey
Niki, H., & Watanabe, M. (1979) · Brain Research · doi:10.1016/0006-8993(79)90328-7 · Cited by 507 · see citing works
Mazor, O., & Laurent, G. (2005) · Neuron · doi:10.1016/j.neuron.2005.09.032 · Cited by 484 · see citing works
Principles of Multivariate Analysis
Krzanowski, W. J. (2000) · doi:10.1093/oso/9780198507086.001.0001 · Cited by 474 · see citing works
Biologically Based Computational Models of High-Level Cognition
O’Reilly, R. C. (2006) · Science · doi:10.1126/science.1127242 · Cited by 447 · see citing works
Neuronal correlates of goal-based motor selection in the prefrontal cortex.
Matsumoto, K., Suzuki, W., & Tanaka, K. (2003) · Science · doi:10.1126/science.1084204 · Cited by 384 · see citing works
Seamans, J. K., Floresco, S., & Phillips, A. G. (1995) · Behavioral Neuroscience · doi:10.1037//0735-7044.109.6.1063 · Cited by 370 · see citing works
Self-citationDynamics of Population Code for Working Memory in the Prefrontal Cortex
Baeg, E. H., Kim, Y. B., Huh, K., Mook-Jung, I., Kim, H. T., & Jung, M. W. (2003) · Neuron · doi:10.1016/s0896-6273(03)00597-x · Cited by 338 · see citing works
Seamans, J. K., Floresco, S., & Phillips, A. G. (1995) · Behavioral Neuroscience · doi:10.1037/0735-7044.109.6.1063 · Cited by 324 · see citing works
Self-citationTop-Down Control of Motor Cortex Ensembles by Dorsomedial Prefrontal Cortex
Narayanan, N. S., & Laubach, M. (2006) · Neuron · doi:10.1016/j.neuron.2006.10.021 · Cited by 311 · see citing works
Jung, M. W., Qin, Y. F., McNaughton, B. L., & Barnes, C. A. (1998) · Cerebral Cortex · doi:10.1093/cercor/8.5.437 · Cited by 307 · see citing works
Natural stimuli evoke dynamic sequences of states in sensory cortical ensembles
Jones, L. M., Fontanini, A., Sadacca, B. F., Miller, P. C., & Katz, D. B. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0705546104 · Cited by 287 · see citing works
Short-term memory in olfactory network dynamics
Stopfer, M., & Laurent, G. (1999) · Nature · doi:10.1038/45244 · Cited by 272 · see citing works
Passingham, R. E. (1996) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1996.0132 · Cited by 236 · see citing works
Chapin, J. K., & Nicolelis, M. A. L. (1999) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(99)00130-2 · Cited by 186 · see citing works
Pratt, W. E., & Mizumori, S. J. Y. (2001) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00204-2 · Cited by 179 · see citing works
Correlations of cortical Hebbian reverberations: theory versus experiment
Amit, D., Brunel, N., & Tsodyks, M. V. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-11-06435.1994 · Cited by 176 · see citing works
Seidemann, E., Meilijson, I., Abeles, M., Bergman, H., & Vaadia, E. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-02-00752.1996 · Cited by 165 · see citing works
Lin, L., Osan, R. M., & Tsien, J. Z. (2005) · Trends in Neurosciences · doi:10.1016/j.tins.2005.11.004 · Cited by 164 · see citing works
Coding of visual objects in the ventral stream
Reddy, L., & Kanwisher, N. (2006) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2006.06.004 · Cited by 159 · see citing works
How do cell assemblies encode information in the brain?
Sakurai, Y. (1999) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(99)00017-2 · Cited by 123 · see citing works
Isomura, Y., Ito, Y., Akazawa, T., Nambu, A., & Takada, M. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-22-08002.2003 · Cited by 107 · see citing works
Euston, D. R., & McNaughton, B. L. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3803-06.2006 · Cited by 101 · see citing works
Cowen, S. L., & McNaughton, B. L. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00150.2007 · Cited by 89 · see citing works
Dynamic Synchrony of Firing in the Monkey Prefrontal Cortex during Working-Memory Tasks
Sakurai, Y., & TAKAHASHI, S. Y. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2423-06.2006 · Cited by 83 · see citing works
Jy, C., Chen, L., Luo, F., L.-H., S., & Woodward, D. J. (2002) · Experimental Brain Research · doi:10.1007/s00221-001-0918-3 · Cited by 78 · see citing works
Hoshi, E., Sawamura, H., & Tanji, J. (2005) · Journal of Neurophysiology · doi:10.1152/jn.01201.2004 · Cited by 67 · see citing works
Neuronal assemblies: Single cortical neurons are obedient members of a huge orchestra
Grinvald, A., Arieli, A., Tsodyks, M. V., & Kenet, T. (2003) · Biopolymers · doi:10.1002/bip.10273 · Cited by 61 · see citing works
Niche-related learning in laboratory paradigms: the case of maze behavior in Norway rats
Timberlake, W. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00048-7 · Cited by 54 · see citing works
Kargo, W. J., Szatmáry, B., & Nitz, D. A. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3604-06.2007 · Cited by 51 · see citing works
Neural Mechanisms of Versatile Functions in Primate Anterior Cingulate Cortex
Isomura, Y., & Takada, M. (2004) · Reviews in the Neurosciences · doi:10.1515/revneuro.2004.15.4.279 · Cited by 46 · see citing works
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The multiple-demand (MD) system of the primate brain: mental programs for intelligent behaviour
Duncan, J. (2010) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2010.01.004 · Cited by 1,846 · see citing works
The role of medial prefrontal cortex in memory and decision making
Euston, D. R., Gruber, A. J., & McNaughton, B. L. (2012) · Neuron · doi:10.1016/j.neuron.2012.12.002 · Cited by 1,541 · see citing works
Floresco, S. B. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00062 · Cited by 336 · see citing works
A reservoir of time constants for memory traces in cortical neurons
Bernacchia, A., Seo, H., Lee, D., & Wang, X.-J. (2011) · Nature Neuroscience · doi:10.1038/nn.2752 · Cited by 292 · see citing works
Rigotti, M. (2010) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2010.00024 · Cited by 184 · see citing works
Hierarchical coding for sequential task events in the monkey prefrontal cortex
Sigala, N., Kusunoki, M., Nimmo-Smith, I., Gaffan, D., & Duncan, J. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0802569105 · Cited by 140 · see citing works
Kim, U., & Lee, T. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08030.x · Cited by 133 · see citing works
- Authors
- Lapish, C. C., Durstewitz, D., Chandler, L. J., & Seamans, J. K.
- Affiliations
- University of British Columbia (CA)
- University of Plymouth (GB)
- Medical University of South Carolina (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2008-08-19
- Volume
- 105
- Issue
- 33
- Pages
- 11963-11968
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2516968
- OpenAlex
- W2032434570
- Cited by
- 119
- References
- 47
- Citations by year
- 2025: 1 · 2024: 4 · 2023: 4 · 2022: 2 · 2021: 4 · 2020: 4 · 2019: 10 · 2018: 11 · 2017: 12 · 2016: 7 · 2015: 10 · 2014: 10 · 2013: 11 · 2012: 8
- FWCI
- 3.62
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- Canadian Institutes of Health Research (84319_1)
- National Institute on Alcohol Abuse and Alcoholism (R01AA010983, R29AA010983, AA 10983)
- National Institute of Mental Health (MH065924, R01MH065924, MH064569, R01MH064569)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- anterior cingulate cortex, decision-making, choice behavior, neuronal ensembles, cell assemblies, single-unit activity, behavioral errors, task space, rats
- MeSH terms
- Animals, Behavior, Animal, Brain, Choice Behavior, Decision Making, Electrophysiology, Male, Nerve Net, Neural Pathways, Neurons, Rats, Long-Evans, Rats
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