Review
Value, pleasure and choice in the ventral prefrontal cortex

https://doi.org/10.1016/j.tics.2010.12.004Get rights and content

Rapid advances have recently been made in understanding how value-based decision-making processes are implemented in the brain. We integrate neuroeconomic and computational approaches with evidence on the neural correlates of value and experienced pleasure to describe how systems for valuation and decision-making are organized in the prefrontal cortex of humans and other primates. We show that the orbitofrontal and ventromedial prefrontal (VMPFC) cortices compute expected value, reward outcome and experienced pleasure for different stimuli on a common value scale. Attractor networks in VMPFC area 10 then implement categorical decision processes that transform value signals into a choice between the values, thereby guiding action. This synthesis of findings across fields provides a unifying perspective for the study of decision-making processes in the brain.

Section snippets

Integrating different approaches to valuation and decision-making

Consider a situation where a choice has to be made between consuming an attractive food and seeking a source of warm, pleasant touch. To decide between these fundamentally different rewards, the brain needs to compute the values and costs associated with two multisensory stimuli, integrate this information with motivational, cognitive and contextual variables and then use these signals as inputs for a stimulus-based choice process. Rapid advances have been made in understanding how these key

Reward and emotion: a Darwinian perspective

The valuation of rewards is a key component process of decision-making. The neurobiological and evolutionary context is as follows [3]. Primary rewards, such as sweet taste and warm touch, are gene-specified (i.e. unlearned) goals for action built into us during evolution by natural selection to direct behavior to stimuli that are important for survival and reproduction. Specification of rewards, the goals for action, by selfish genes is an efficient and adaptive Darwinian way for genes to

From valuation to choice in the ventromedial prefrontal cortex

The operational principles described above enable the OFC and ACC (Tier 2 in Figure 1) to provide value representations that are appropriately scaled to act as inputs into neural systems for economic decision-making, and to promote a progression through the reward space in the environment to find the range of rewards necessary for survival and reproduction [3]. We next consider how neural value representations are transformed into choices in the VMPFC. We describe evidence that choices are made

Phenomenological approaches

By examining computational models of decision-making, we now consider the processes by which the brain may make choices between rewards. One approach, which has been used mainly in the domain of sensory decision-making, can be described as phenomenological, in that a mathematical model is formulated without specifying the underlying neural mechanisms. The main such approach is the accumulator or race model, in which the noisy (variable) incoming evidence is accumulated or integrated until some

Concluding remarks and future priorities

We have linked neurophysiological and neuroimaging to computational approaches to decision-making and have shown that representations of specific rewards on a continuous and similar scale of value in the OFC and ACC (Tier 2) are followed by a noisy attractor-based system for making choices between rewards in VMPFC area 10 (Tier 3). Subjective pleasure is the state associated with the activation of representations in Tier 2, and confidence is an emergent property of the decision-making process

Acknowledgments

Some of the research described in this paper was supported by the Medical Research Council and the Oxford Centre for Computational Neuroscience. F.G. was supported by the Gottlieb-Daimler- and Karl Benz-Foundation, and by the Oxford Centre for Computational Neuroscience.

References (100)

  • J.W. Kable et al.

    The neurobiology of decision: consensus and controversy

    Neuron

    (2009)
  • F. Grabenhorst et al.

    Different representations of relative and absolute value in the human brain

    Neuroimage

    (2009)
  • I.E.T. de Araujo

    Cognitive modulation of olfactory processing

    Neuron

    (2005)
  • A. Rangel et al.

    Neural computations associated with goal-directed choice

    Curr. Opin. Neurobiol.

    (2010)
  • B. Knutson

    Neural predictors of purchases

    Neuron

    (2007)
  • J. Hornak

    Face and voice expression identification in patients with emotional and behavioural changes following ventral frontal lobe damage

    Neuropsychologia

    (1996)
  • A. Rangel

    The computation and comparison of value in goal-directed choice

  • M.F. Rushworth

    General mechanisms for making decisions? Curr

    Opin. Neurobiol.

    (2009)
  • E.D. Boorman

    How green is the grass on the other side? Frontopolar cortex and the evidence in favor of alternative courses of action

    Neuron

    (2009)
  • X.J. Wang

    Probabilistic decision making by slow reverberation in cortical circuits

    Neuron

    (2002)
  • D. Vickers et al.

    Effects of alternating set for speed or accuracy on response time, accuracy and confidence in a unidimensional discrimination task

    Acta Psychol.

    (1982)
  • M.F. Rushworth

    Functional organization of the medial frontal cortex

    Curr. Opin. Neurobiol.

    (2007)
  • E.T. Rolls

    Warm pleasant feelings in the brain

    Neuroimage

    (2008)
  • M. O’Neill et al.

    Coding of reward risk by orbitofrontal neurons is mostly distinct from coding of reward value

    Neuron

    (2010)
  • S. Kim

    Prefrontal coding of temporally discounted values during intertemporal choice

    Neuron

    (2008)
  • C. Padoa-Schioppa et al.

    Neurons in the orbitofrontal cortex encode economic value

    Nature

    (2006)
  • E.T. Rolls

    Emotion Explained

    (2005)
  • F. Grabenhorst et al.

    Selective attention to affective value alters how the brain processes taste stimuli

    Eur. J. Neurosci.

    (2008)
  • F. Grabenhorst

    How cognition modulates affective responses to taste and flavor: top down influences on the orbitofrontal and pregenual cingulate cortices

    Cereb. Cortex

    (2008)
  • E.T. Rolls

    Memory, Attention, and Decision-Making: A Unifying Computational Neuroscience Approach

    (2008)
  • F. Grabenhorst

    How the brain represents the reward value of fat in the mouth

    Cereb. Cortex

    (2010)
  • F. Grabenhorst

    From affective value to decision-making in the prefrontal cortex

    Eur. J. Neurosci.

    (2008)
  • B.W. Balleine et al.

    Human and rodent homologies in action control: corticostriatal determinants of goal-directed and habitual action

    Neuropsychopharmacology

    (2010)
  • D. Kahneman

    Back to Bentham? Explorations of experienced utility

    Q. J. Econ.

    (1997)
  • E.T. Rolls

    Functions of the orbitofrontal and pregenual cingulate cortex in taste, olfaction, appetite and emotion

    Acta Physiol. Hung.

    (2008)
  • C.H. Luk et al.

    Dynamic encoding of responses and outcomes by neurons in medial prefrontal cortex

    J. Neurosci.

    (2009)
  • M. Matsumoto

    Medial prefrontal selectivity signalling prediction errors of action values

    Nat. Neurosci.

    (2007)
  • C. Amiez

    Reward encoding in the monkey anterior cingulate cortex

    Cereb. Cortex

    (2006)
  • H. Seo et al.

    Temporal filtering of reward signals in the dorsal anterior cingulate cortex during a mixed-strategy game

    J. Neurosci.

    (2007)
  • E.T. Rolls

    The anterior and midcingulate cortices and reward

  • E.T. Rolls

    Face-selective and auditory neurons in the primate orbitofrontal cortex

    Exp. Brain Res.

    (2006)
  • S.J. Thorpe

    Neuronal activity in the orbitofrontal cortex of the behaving monkey

    Exp. Brain Res.

    (1983)
  • H.D. Critchley et al.

    Hunger and satiety modify the responses of olfactory and visual neurons in the primate orbitofrontal cortex

    J. Neurophysiol.

    (1996)
  • E.T. Rolls

    From reward value to decision-making: neuronal and computational principles

  • J. O’Doherty

    Abstract reward and punishment representations in the human orbitofrontal cortex

    Nat. Neurosci.

    (2001)
  • E.T. Rolls

    Expected value, reward outcome, and temporal difference error representations in a probabilistic decision task

    Cereb. Cortex

    (2008)
  • Bernoulli, J. (1738/1954) Exposition of a new theory on the measurement of risk. Econometrica 22,...
  • D.J. McFarland et al.

    The behavioural final common path

    Philos. Trans. R. Soc. Lond.

    (1975)
  • V.S. Chib

    Evidence for a common representation of decision values for dissimilar goods in human ventromedial prefrontal cortex

    J. Neurosci.

    (2009)
  • C. Padoa-Schioppa et al.

    The representation of economic value in the orbitofrontal cortex is invariant for changes of menu

    Nat. Neurosci.

    (2008)
  • Cited by (574)

    View all citing articles on Scopus
    View full text