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The human orbitofrontal cortex: linking reward to hedonic experience

Key Points

  • The prefrontal cortex seems to be essential for the control and organization of behaviour. In particular, it has been linked to the relative cognitive sophistication that has been reached by higher primates, especially humans. However, the functions of one of its constituent regions, the orbitofrontal cortex, have remained enigmatic.

  • In terms of neuroanatomical connectivity, the primate orbitofrontal cortex is uniquely placed to integrate sensory and autonomic information to modulate behaviour through both visceral and motor systems.

  • Recent neuroimaging studies in humans have confirmed the role of the human orbitofrontal cortex as a nexus for sensory integration, modulation of visceral reactions, and participation in learning, prediction and decision making for emotional and reward-related behaviours. But these studies have also shown that the human orbitofrontal cortex is a highly heterogeneous brain region that encompasses many different functions.

  • In particular, the human orbitofrontal cortex has been found to represent not only the reward value and expected reward value of foods and other reinforcers, but also their subjective pleasantness. This link to subjective hedonic processing could provide a basis for further exploration of the brain systems involved in the conscious experience of pleasure and reward, and, as such, offer a unique method for studying the hedonic quality of human experience.

  • Based on the available evidence from neuroimaging and neuropsychology, a tentative new model of the functional neuroanatomy of the orbitofrontal cortex is offered with medial–lateral and posterior–anterior distinctions, in which the implicit reward value is assigned early on in the hierarchy for each type of reinforcer, with a further progression up the processing hierarchy (reflecting the effects of combinations of stimuli) towards areas that are connected to brain regions necessary for conscious hedonic processing.

  • At present, little is known about the functional and structural development of the human orbitofrontal cortex in children and adolescents. However, further investigation of the link to hedonic processing could potentially lead to a better understanding of and novel treatments for disorders linked to anhedonia, such as depression, obesity and eating disorders.

Abstract

Hedonic experience is arguably at the heart of what makes us human. In recent neuroimaging studies of the cortical networks that mediate hedonic experience in the human brain, the orbitofrontal cortex has emerged as the strongest candidate for linking food and other types of reward to hedonic experience. The orbitofrontal cortex is among the least understood regions of the human brain, but has been proposed to be involved in sensory integration, in representing the affective value of reinforcers, and in decision making and expectation. Here, the functional neuroanatomy of the human orbitofrontal cortex is described and a new integrated model of its functions proposed, including a possible role in the mediation of hedonic experience.

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Figure 1: Cytoarchitectonic maps of human and monkey orbitofrontal cortices.
Figure 2: Anatomy, variability and development of the human orbitofrontal cortex.
Figure 3: Meta-analysis of the functions of the orbitofrontal cortex.
Figure 5: Hedonic processing.
Figure 4: Co-activation of the lateral orbitofrontal and anterior cingulate cortices.
Figure 6: A model of orbitofrontal cortex function.

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Acknowledgements

This research is supported by the Wellcome Trust and the Medical Research Council (to the Oxford Centre for Functional Magnetic Resonance Imaging of the Brain (FMRIB)).

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FURTHER INFORMATION

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Glossary

REINFORCERS

Positive reinforcers (rewards) increase the frequency of behaviour that leads to their acquisition. Negative reinforcers (punishers) decrease the frequency of behaviour that leads to their encounter and increase the frequency of behaviour that leads to their avoidance.

BRODMANN'S AREAS

(BA). Korbinian Brodmann (1868–1918) was an anatomist who divided the cerebral cortex into numbered subdivisions on the basis of cell arrangements, types and staining properties (for example, the dorsolateral prefrontal cortex contains several subdivisions, including BA 46 and BA 9). Modern derivatives of Brodmann's maps are commonly used as the reference system for the discussion of brain-imaging findings.

GOAL-DIRECTED BEHAVIOUR

Behaviour directed towards the attainment of a future state (for example, obtaining the next meal).

VENTROMEDIAL PREFRONTAL CORTEX

An anatomical term that refers to most of the medial orbitofrontal cortex and areas on the medial wall, but not to more central and lateral regions of the orbitofrontal cortex.

RESPONSE INHIBITION

Lack of control and general perseveration are symptoms that commonly follow damage to the frontal lobes, and have often been ascribed to a lack of inhibitory control over the appropriate responses.

REVERSAL LEARNING

Describes a task in which participants are trained to respond differentially to two stimuli under conditions of reward and punishment (or non-reward), and subsequently have to learn to change their behaviour when the reward values are reversed (that is, when the previously rewarded stimulus is no longer rewarded, and vice versa).

JAMES–LANGE THEORY

Two nineteenth-century scholars, William James and Carl Lange, independently proposed that emotions arise as a result of bodily physiological events, such as increases in heart rate, rather than being the cause of them

SELECTIVE SATIETY

A form of reinforcer devaluation in which participants that have been fed to satiety on one food still find other foods rewarding, and will eat some of these other foods. Selective satiety is particularly useful for studying affective representation in the brain, because it provides a means of altering the affective value of a stimulus without modifying its physical attributes, allowing a change in reward value to be detected.

CO-ACTIVATION

The presence, in a neuroimaging experiment, of significant activity in two brain structures in the same subtraction.

TRUE TASTE SYNERGISM

The combined effect of two taste stimuli, when greater than the sum of the effects of each one present alone.

MULTIMODAL INTEGRATION

The process of combining information from different sensory modalities.

MAGNETOENCEPHALOGRAPHY

(MEG). A non-invasive technique that allows the detection of the changing magnetic fields that are associated with brain activity on the timescale of milliseconds.

GRANGER CAUSALITY

A technique for determining whether one time series is useful in predicting another.

ANHEDONIA

Loss of interest or pleasure in almost all activities.

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Kringelbach, M. The human orbitofrontal cortex: linking reward to hedonic experience. Nat Rev Neurosci 6, 691–702 (2005). https://doi.org/10.1038/nrn1747

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