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Specializations for reward-guided decision-making in the primate ventral prefrontal cortex

Abstract

The estimated values of choices, and therefore decision-making based on those values, are influenced by both the chance that the chosen items or goods can be obtained (availability) and their current worth (desirability) as well as by the ability to link the estimated values to choices (a process sometimes called credit assignment). In primates, the prefrontal cortex (PFC) has been thought to contribute to each of these processes; however, causal relationships between particular subdivisions of the PFC and specific functions have been difficult to establish. Recent lesion-based research studies have defined the roles of two different parts of the primate PFC — the orbitofrontal cortex (OFC) and the ventral lateral frontal cortex (VLFC) — and their subdivisions in evaluating each of these factors and in mediating credit assignment during reward-based decision-making.

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Fig. 1: The anatomy of the OFC and VLFC.
Fig. 2: Selected behavioural tasks used to assess value-based decision-making.
Fig. 3: Effects of selective, excitotoxic lesions of the OFC and VLFC on availability-based or desirability-based choices.
Fig. 4: Independent contributions of the medial and lateral OFC to value-based decision-making.
Fig. 5: Effect of amygdala lesions on value coding in the OFC.

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Acknowledgements

The authors thank P.-Y. Chen for help with the preparation of figures and S. P. Wise for comments on an earlier version of this manuscript. This work was supported by the Intramural Research Program of the US National Institute of Mental Health (NIMH; ZIAMH002887 (E.A.M.)), an NIMH BRAINS award (R01 MH110822 (P.H.R.)) and a NARSAD Young Investigator Award (NARSAD grant 23638 (P.H.R.)).

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E.A.M. and P.H.R. researched data for the article, made substantial contributions to discussions of the content and wrote the article. E.A.M. reviewed and/or edited the manuscript before submission.

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Correspondence to Elisabeth A. Murray.

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Glossary

Reward-guided learning

A general term that refers to any kind of learning facilitated by reward, including stimulus–outcome learning, action–outcome learning and stimulus–response learning.

Inhibitory control

The ability to inhibit choices or responses that have previously been rewarded. The concept of behavioural inhibition includes the ability to suppress default, habitual and prepotent behaviours.

Flexible stimulus–reward learning

The ability to quickly make and break associative links between objects (or other cues) and rewards.

Value-based decision-making

The ability to make facultative choices that optimize subjective value.

Credit assignment

The ability to learn that a particular outcome (in experiments, this is typically food or fluid) was produced by a particular choice.

Cognitive map

A neural representation of stimuli, actions and other sensory features that occur in association with outcomes in a multidimensional array. The cognitive map has been theorized to guide value-based decision-making.

Value updating

The process of registering a change in the neural representation of the desirability or availability of foods.

Cortical coupling

A pattern of correlated activity between different brain areas discerned from resting-state fMRI. Cortical coupling has been used to identify brain areas in macaques and humans that have similar connectivity profiles and perhaps comparable functions.

Aspiration lesion

A technique for removing grey matter (that is, neurons) that is based on subpial aspiration of tissue. Lesions are typically carried out with the aid of an operating microscope.

Reversal learning

A task in which, after subjects learn to choose a rewarded item over an unrewarded item, the stimulus–outcome contingencies switch without warning. Thus, the subject must now learn to choose the object that was initially unrewarded. The only feedback to guide choices is the occurrence of reward or nonreward.

Excitotoxic lesions

Lesions created using a technique for selectively removing grey matter (that is, neurons) and sparing white matter (that is, axons) that is based on the injection of neurotoxins. Injections are often carried out via a stereotaxic approach based on coordinates obtained from magnetic resonance images of the brain.

Attentional selection

Concentration of visual or other (for example, somatosensory or auditory) sensory processing resources towards behaviourally important spatial locations or visual features. This process enhances sensory perception so that responses can be faster and more accurate.

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Murray, E.A., Rudebeck, P.H. Specializations for reward-guided decision-making in the primate ventral prefrontal cortex. Nat Rev Neurosci 19, 404–417 (2018). https://doi.org/10.1038/s41583-018-0013-4

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