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The cingulate cortex and limbic systems for emotion, action, and memory
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Evidence is provided for a new conceptualization of the connectivity and functions of the cingulate cortex in emotion, action, and memory. The anterior cingulate cortex receives information from the orbitofrontal cortex about reward and non-reward outcomes. The posterior cingulate cortex receives spatial and action-related information from parietal cortical areas. It is argued that these inputs allow the cingulate cortex to perform action-outcome learning, with outputs from the midcingulate motor area to premotor areas. In addition, because the anterior cingulate cortex connects rewards to actions, it is involved in emotion; and because the posterior cingulate cortex has outputs to the hippocampal system, it is involved in memory. These apparently multiple different functions of the cingulate cortex are related to the place of this proisocortical limbic region in brain connectivity.
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“Underactivated MCC in ADHD individuals may be construed as connected with the core symptom of inattention”
From Overlapping and differential neuropharmacological mechanisms of stimulants and nonstimulants for attention-deficit/hyperactivity disorder: A comparative neuroimaging analysis (2024) · cites this paper as Rolls, 2019
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“the MCC is considered a key area of emotion and cognition processing and subserves bottom-up attention diversion”
From Overlapping and differential neuropharmacological mechanisms of stimulants and nonstimulants for attention-deficit/hyperactivity disorder: A comparative neuroimaging analysis (2024) · cites this paper as Rolls, 2019
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Self-citationThe effect of cingulate lesions on social behaviour and emotion
Hadland, K. A., Rushworth, M. F. S., Gaffan, D., & Passingham, R. E. (2003) · Neuropsychologia · doi:10.1016/s0028-3932(02)00325-1 · Cited by 225
Neuronal Encoding of Subjective Value in Dorsal and Ventral Anterior Cingulate Cortex
Cai, X., & Padoa‐Schioppa, C. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.3864-11.2012 · Cited by 220
Pain and Stroop interference tasks activate separate processing modules in anterior cingulate cortex
Derbyshire, S. W. G., Vogt, B. A., & Jones, A. K. P. (1998) · Experimental Brain Research · doi:10.1007/s002210050254 · Cited by 218
The medial pain system, cingulate cortex, and parallel processing of nociceptive information
Vogt, B. A., & Sikes, R. W. (2000) · Progress in brain research · doi:10.1016/s0079-6123(08)62141-x · Cited by 218
Neural Activation during Covert Processing of Positive Emotional Facial Expressions
Dolan, R. J., Fletcher, P. C., Morris, J., Kapur, N., Deakin, J. F. W., & Frith, C. (1996) · NeuroImage · doi:10.1006/nimg.1996.0070 · Cited by 217
Selective attention to affective value alters how the brain processes taste stimuli
Fabian Grabenhorst, B., & Rolls, E. T. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06033.x · Cited by 216
Self-citationRolls, E. (2008) · Acta Physiologica Hungarica · doi:10.1556/aphysiol.95.2008.2.1 · Cited by 214
Self-citationKennerley, S. W., & Wallis, J. D. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06743.x · Cited by 211
How the Brain Represents the Reward Value of Fat in the Mouth
Fabian Grabenhorst, B., Rolls, E. T., Parris, B. A., & D’Souza, A. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp169 · Cited by 210
Self-citationThe neural correlates of intentional and incidental self processing
Kircher, T. T. J., Brammer, M. J., Bullmore, E. T., Simmons, A., Bartels, M., & David, A. S. (2002) · Neuropsychologia · doi:10.1016/s0028-3932(01)00138-5 · Cited by 200
Posterior Cingulate Cortex Mediates Outcome-Contingent Allocation of Behavior
Hayden, B. Y., Nair, A. C., McCoy, A. N., & Platt, M. L. (2008) · Neuron · doi:10.1016/j.neuron.2008.09.012 · Cited by 200
Brain mechanisms for perceptual and reward-related decision-making
Deco, G., Rolls, E. T., Albantakis, L., & Romo, R. (2013) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2012.01.010 · Cited by 196
Self-citationThe storage and recall of memories in the hippocampo-cortical system
Rolls, E. T. (2017) · Cell and Tissue Research · doi:10.1007/s00441-017-2744-3 · Cited by 195
Self-citationCamille, N., Tsuchida, A., & Fellows, L. K. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.3164-11.2011 · Cited by 195
Saccade Reward Signals in Posterior Cingulate Cortex
McCoy, A. N., Crowley, J. C., Haghighian, G., Dean, H. L., & Platt, M. L. (2003) · Neuron · doi:10.1016/s0896-6273(03)00719-0 · Cited by 193
The role of incentive learning in instrumental outcome revaluation by sensory-specific satiety
Balleine, B. W., & Dickinson, A. (1998) · Animal Learning & Behavior · doi:10.3758/bf03199161 · Cited by 187
Cerebral cortex : principles of operation
Rolls, E. T. (2016) · doi:10.82444/warw.33712699 · Cited by 187
Self-citationA non-reward attractor theory of depression
Rolls, E. T. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.05.007 · Cited by 180
Self-citationInformation About Spatial View in an Ensemble of Primate Hippocampal Cells
Rolls, E. T., Treves, A., Robertson, R. G., Georges‐François, P., & Panzeri, S. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.79.4.1797 · Cited by 179
Self-citationSpatial representations in the primate hippocampus, and their functions in memory and navigation
Rolls, E. T., & Wirth, S. (2018) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2018.09.004 · Cited by 173
Self-citationGabbott, P. L. A., Warner, T. A., Jays, P. R. L., & Bacon, S. J. (2003) · Brain Research · doi:10.1016/j.brainres.2003.08.056 · Cited by 157
Spatial View Cells in the Primate Hippocampus: Effects of Removal of View Details
Robertson, R. G., Rolls, E. T., & Georges‐François, P. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.79.3.1145 · Cited by 153
Self-citationDistinct Roles of Three Frontal Cortical Areas in Reward-Guided Behavior
Noonan, M. P., Mars, R. B., & Rushworth, M. F. S. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.6456-10.2011 · Cited by 151
Choice, difficulty, and confidence in the brain
Rolls, E. T., Grabenhorst, F., & Deco, G. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.06.073 · Cited by 148
Self-citationObject, Space, and Object-Space Representations in the Primate Hippocampus
Rolls, E. T., Xiang, J.-Z., & Franco, L. (2005) · Journal of Neurophysiology · doi:10.1152/jn.01063.2004 · Cited by 146
Self-citationFunctional Connectivity of the Anterior Cingulate Cortex in Depression and in Health
Rolls, E. T., Cheng, W., Gong, W., Qiu, J., Zhou, C., Zhang, J., Lv, W., Ruan, H., Wei, D., Cheng, K., et al. (2018) · Cerebral Cortex · doi:10.1093/cercor/bhy236 · Cited by 138
Self-citationThe effect of cingulate cortex lesions on task switching and working memory
Rushworth, M. F. S., Hadland, K. A., Gaffan, D., & Passingham, R. E. (2003) · Journal of Cognitive Neuroscience · doi:10.1162/089892903321593072 · Cited by 138
Palomero‐Gallagher, N., Eickhoff, S. B., Hoffstaedter, F., Schleicher, A., Mohlberg, H., Vogt, B. A., Amunts, K., & Zilles, K. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.04.053 · Cited by 136
Midcingulate Motor Map and Feedback Detection: Converging Data from Humans and Monkeys
Procyk, E., Wilson, C. R. E., Stoll, F. M., Faraut, M. C. M., Petrides, M., & Amiez, C. (2014) · Cerebral Cortex · doi:10.1093/cercor/bhu213 · Cited by 136
Reward-Spatial View Representations and Learning in the Primate Hippocampus
Rolls, E. T., & Xiang, J.-Z. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1481-05.2005 · Cited by 133
Self-citationFunctional connectivity of the right inferior frontal gyrus and orbitofrontal cortex in depression
Rolls, E. T., Cheng, W., Du, J., Wei, D., Qiu, J., Dai, D., Zhou, Q., Xie, P., & Feng, J. (2020) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsaa014 · Cited by 132
Self-citationFrom affective value to decision‐making in the prefrontal cortex
Fabian Grabenhorst, B., Rolls, E. T., & Parris, B. A. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06489.x · Cited by 130
Self-citationDecision-Making, Errors, and Confidence in the Brain
Rolls, E. T., Fabian Grabenhorst, B., & Deco, G. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00571.2010 · Cited by 123
Self-citationCheng, W., Rolls, E. T., Qiu, J., Xie, X., Wei, D., Huang, C., Yang, A. C., Tsai, S., Li, Q., Meng, J., et al. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0139-1 · Cited by 123
Self-citationPrice, J. L. (2006) · doi:10.1093/acprof:oso/9780198565741.003.0003 · Cited by 121
Selective Attention to Affective Value Alters How the Brain Processes Olfactory Stimuli
Rolls, E. T., Fabian Grabenhorst, B., Margot, C., da Silva, M. A. A. P., & Velazco, M. I. (2008) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2008.20128 · Cited by 116
Self-citationRolls, E. T. (2016) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198784852.001.0001 · Cited by 116
Self-citationPandya, D. Ν., Seltzer, B., Petrides, M., & Cipolloni, P. B. (2015) · Oxford University Press eBooks · doi:10.1093/med/9780195385151.001.0001 · Cited by 114
Emotion and decision-making explained: A précis
Rolls, E. T. (2014) · Cortex · doi:10.1016/j.cortex.2014.01.020 · Cited by 109
Self-citationSpatial View Cells in the Primate Hippocampus and Memory Recall
Rolls, E. T., & Xiang, J.-Z. (2006) · Reviews in the Neurosciences · doi:10.1515/revneuro.2006.17.1-2.175 · Cited by 108
Self-citationFunctional Connectivity of the Precuneus in Unmedicated Patients With Depression
Cheng, W., Rolls, E. T., Qiu, J., Yang, D., Ruan, H., Wei, D., Zhao, L., Meng, J., Xie, P., & Feng, J. (2018) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2018.07.008 · Cited by 106
Self-citationCerebral Cortex: Architecture, Connections, and the Dual Origin Concept
Pandya, D. Ν., Seltzer, B., Petrides, M., & Cipolloni, P. B. (2015) · Cited by 106
Assessing the mechanism of response in the retrosplenial cortex of good and poor navigators
Auger, S. D., & Maguire, E. A. (2013) · Cortex · doi:10.1016/j.cortex.2013.08.002 · Cited by 98
Cingulofrontal Interactions And The Cingulate Motor Areas
Morecraft, R. J., & Tanji, J. (2009) · doi:10.1093/oso/9780198566960.003.0005 · Cited by 98
(1921) · The Antiquaries Journal · doi:10.1017/s0003581500089393 · Cited by 97
Choice Coding in Frontal Cortex during Stimulus-Guided or Action-Guided Decision-Making
Luk, C.-H., & Wallis, J. D. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.4920-12.2013 · Cited by 96
Role of long‐term synaptic modification in short‐term memory
Kesner, R. P., & Rolls, E. T. (2001) · Hippocampus · doi:10.1002/hipo.1040 · Cited by 95
Self-citationDynamic Encoding of Responses and Outcomes by Neurons in Medial Prefrontal Cortex
Luk, C.-H., & Wallis, J. D. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0386-09.2009 · Cited by 88
A common neural scale for the subjective pleasantness of different primary rewards
Fabian Grabenhorst, B., D’Souza, A., Parris, B. A., Rolls, E. T., & Passingham, R. E. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.03.043 · Cited by 72
Self-citationRolls, E. T. (2019) · Oxford University Press eBooks · doi:10.1093/oso/9780198845997.001.0001 · Cited by 66
Self-citationFrom Paul Broca's great limbic lobe to the limbic system
Pessoa, L., & Hof, P. R. (2015) · The Journal of Comparative Neurology · doi:10.1002/cne.23840 · Cited by 63
Neuronal coding of implicit emotion categories in the subcallosal cortex in patients with depression
Laxton, A. W., Neimat, J. S., Davis, K. D., Womelsdorf, T., Hutchison, W. D., Dostrovsky, J. O., Hamani, C., Mayberg, H. S., & Lozano, A. M. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.03.029 · Cited by 62
The Anterior and Midcingulate Cortices and Reward
Rolls, E. T. (2009) · doi:10.1093/oso/9780198566960.003.0008 · Cited by 47
Self-citationNeuronal evidence for good-based economic decisions under variable action costs
Cai, X., & Padoa‐Schioppa, C. (2019) · Nature Communications · doi:10.1038/s41467-018-08209-3 · Cited by 37
Absence of Spatial Tuning in the Orbitofrontal Cortex
Grattan, L. E., & Glimcher, P. W. (2014) · PLoS ONE · doi:10.1371/journal.pone.0112750 · Cited by 35
Architectonic structure of the orbital and medial prefrontal cortex
Price, J. L. (2006) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198565741.003.0001 · Cited by 28
Vogt, B. A., & Laureys, S. (2009) · doi:10.1093/oso/9780198566960.003.0013 · Cited by 16
The orbitofrontal cortex, depression, and other mental disorders
Rolls, E. T. (2019) · Oxford University Press eBooks · doi:10.1093/oso/9780198845997.003.0007 · Cited by 2
Self-citationConnectional networks within the orbital and medial prefrontal cortex of macaque monkeys
Carmichael, S. T., & Price, J. L. (1996) · Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960722)371:2
Rempel-Clower, N. L., & Barbas, H. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19980831)398:3
Flagged first, then by citations
Research works printed but not linked: 2
- Rolls ET (2018a) The brain, emotion, and depression. Oxford University Press, Oxford
- Vogt BA (ed) (2019) Handbook of clinical neurology: cingulate cortex. handbook of clinical neurology, 3rd edn. Elsevier, New York
Cited by
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Automated anatomical labelling atlas 3
Rolls, E. T., Huang, C., Lin, C., Feng, J., & Joliot, M. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.116189 · Cited by 2,035
Self-citationThe orbitofrontal cortex: reward, emotion and depression
Rolls, E. T., Cheng, W., & Feng, J. (2020) · Brain Communications · doi:10.1093/braincomms/fcaa196 · Cited by 474
Self-citationRolls, E. T. (2023) · Brain Structure and Function · doi:10.1007/s00429-023-02644-9 · Cited by 356
Self-citationCommon genetic variation influencing human white matter microstructure
Zhao, B., Li, T., Yang, Y., Wang, X., Luo, T., Shan, Y., Zhu, Z., Xiong, D., Hauberg, M. E., Bendl, J. M., et al. (2021) · Science · doi:10.1126/science.abf3736 · Cited by 222
Long COVID: cognitive complaints (brain fog) and dysfunction of the cingulate cortex
Hugon, J., Msika, E.-F., Queneau, M., Farid, K., & Paquet, C. (2021) · Journal of Neurology · doi:10.1007/s00415-021-10655-x · Cited by 216
Metadata
- Authors
- Rolls, E. T.
- Affiliations
- University of Warwick (GB)
- Corresponding author
- Rolls, Edmund T.
- ORCID
- Rolls, Edmund T.
- Venue
- Brain Structure and Function
- Published
- 2019-08-26
- Volume
- 224
- Issue
- 9
- Pages
- 3001-3018
- ISSN
- 1863-2653 (ISSN-L)
- 1863-2661
- PMC
- PMC6875144
- OpenAlex
- W2970957161
- Cited by
- 859
- References
- 171
- Citations by year
- 2026: 110 · 2025: 175 · 2024: 173 · 2023: 114 · 2022: 148 · 2021: 94 · 2020: 39 · 2019: 6
- FWCI
- 9.11
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Brain Structure and Function (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Warwick Research Archive Portal (University of Warwick) (submittedVersion, cc-by)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- cingulate cortex, anterior cingulate cortex, posterior cingulate cortex, orbitofrontal cortex, reward processing, action-outcome learning, premotor cortex, parietal cortex, hippocampal system, emotions, memory, limbic system, brain connectivity
- MeSH terms
- Animals, Emotions, Gyrus Cinguli, Humans, Limbic System, Memory, Motor Activity, Neural Pathways, Reward
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