The cingulate cortex and limbic systems for emotion, action, and memory

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Abstract

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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Neurons in the orbitofrontal cortex encode economic value.

Camillo Padoa-Schioppa, John Assad (2006)

Economic choice is the behaviour observed when individuals select one among many available options. There is no intrinsically 'correct' answer: economic choice depends on subjective preferences. This behaviour is traditionally the object of economic analysis and is also of primary interest in psychology. However, the underlying mental processes and neuronal mechanisms are not well understood. Theories of human and animal choice have a cornerstone in the concept of 'value'. Consider, for example, a monkey offered one raisin versus one piece of apple: behavioural evidence suggests that the animal chooses by assigning values to the two options. But where and how values are represented in the brain is unclear. Here we show that, during economic choice, neurons in the orbitofrontal cortex (OFC) encode the value of offered and chosen goods. Notably, OFC neurons encode value independently of visuospatial factors and motor responses. If a monkey chooses between A and B, neurons in the OFC encode the value of the two goods independently of whether A is presented on the right and B on the left, or vice versa. This trait distinguishes the OFC from other brain areas in which value modulates activity related to sensory or motor processes. Our results have broad implications for possible psychological models, suggesting that economic choice is essentially choice between goods rather than choice between actions. In this framework, neurons in the OFC seem to be a good candidate network for value assignment underlying economic choice.

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Abstract reward and punishment representations in the human orbitofrontal cortex.

J. O'Doherty, M Kringelbach, E Rolls … (2001)

The orbitofrontal cortex (OFC) is implicated in emotion and emotion-related learning. Using event-related functional magnetic resonance imaging (fMRI), we measured brain activation in human subjects doing an emotion-related visual reversal-learning task in which choice of the correct stimulus led to a probabilistically determined 'monetary' reward and choice of the incorrect stimulus led to a monetary loss. Distinct areas of the OFC were activated by monetary rewards and punishments. Moreover, in these areas, we found a correlation between the magnitude of the brain activation and the magnitude of the rewards and punishments received. These findings indicate that one emotional involvement of the human orbitofrontal cortex is its representation of the magnitudes of abstract rewards and punishments, such as receiving or losing money.

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Neural correlates of decision variables in parietal cortex.

M Platt, P W Glimcher (1999)

Decision theory proposes that humans and animals decide what to do in a given situation by assessing the relative value of each possible response. This assessment can be computed, in part, from the probability that each action will result in a gain and the magnitude of the gain expected. Here we show that the gain (or reward) a monkey can expect to realize from an eye-movement response modulates the activity of neurons in the lateral intraparietal area, an area of primate cortex that is thought to transform visual signals into eye-movement commands. We also show that the activity of these neurons is sensitive to the probability that a particular response will result in a gain. When animals can choose freely between two alternative responses, the choices subjects make and neuronal activation in this area are both correlated with the relative amount of gain that the animal can expect from each response. Our data indicate that a decision-theoretic model may provide a powerful new framework for studying the neural processes that intervene between sensation and action.

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Contributors

Edmund T. Rolls:

ORCID: http://orcid.org/0000-0003-3025-1292

Edmund.Rolls@oxcns.org , http://www.oxcns.org

Journal

Journal ID (nlm-ta): Brain Struct Funct

Journal ID (iso-abbrev): Brain Struct Funct

Title: Brain Structure & Function

Publisher: Springer Berlin Heidelberg (Berlin/Heidelberg )

ISSN (Print): 1863-2653

ISSN (Electronic): 1863-2661

Publication date (Electronic): 26 August 2019

Publication date PMC-release: 26 August 2019

Publication date (Print): 2019

Volume: 224

Issue: 9

Pages: 3001-3018

Affiliations

[1 ]GRID grid.419956.6, Oxford Centre for Computational Neuroscience, ; Oxford, UK

[2 ]GRID grid.7372.1, ISNI 0000 0000 8809 1613, Department of Computer Science, , University of Warwick, ; Coventry, CV4 7AL UK

Author information

Edmund T. Rolls http://orcid.org/0000-0003-3025-1292

Article

Publisher ID: 1945

DOI: 10.1007/s00429-019-01945-2

PMC ID: 6875144

PubMed ID: 31451898

SO-VID: a26a6e5e-8fd5-4611-9464-ce158590b972

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Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

History

Date received : 19 April 2019

Date accepted : 19 August 2019

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ScienceOpen disciplines: Neurology

Keywords: cingulate cortex,limbic systems,hippocampus,orbitofrontal cortex,emotion,memory,depression

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ScienceOpen disciplines: Neurology

Keywords: cingulate cortex, limbic systems, hippocampus, orbitofrontal cortex, emotion, memory, depression

The cingulate cortex and limbic systems for emotion, action, and memory

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Most cited references 129

Neurons in the orbitofrontal cortex encode economic value.

Abstract reward and punishment representations in the human orbitofrontal cortex.

Neural correlates of decision variables in parietal cortex.

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