Valuation and decision-making in frontal cortex: one or many serial or parallel systems?
Highlights
► We review three different accounts of frontal cortical function in reward-guided decision-making. ► A serial model proposes that value expectation is represented in ventromedial prefrontal cortex/medial orbitofrontal cortex (vmPFC/mOFC) while value comparison takes place in anterior cingulate cortex (ACC). ► A parallel model envisages parallel comparison processes occurring in both vmPFC/mOFC and ACC. ► vmPFC/mOFC and ACC may be concerned with decision-making and foraging, respectively.
Section snippets
Value assignment and prefrontal cortex
An emerging and influential account of frontal brain mechanisms of decision-making holds that what we and other animals do when we make a choice is to decide between two different goods on the basis of their independently computed reward values [1]. The lateral orbitofrontal cortex (lOFC) plays a central role in learning the values associated with different goods. LOFC lesions disrupt the assignment of precise values to stimuli [2••]. The representations of values in this area are appropriate
A possible serial circuit in frontal cortex for making a value-guided choice
In contrast to lOFC, vmPFC/mOFC appears more intimately concerned with the use of reward representations to guide behaviour (Figure 1b). Little is known about neurons in vmPFC/mOFC but it is clear that while they represent rewards they differ from lOFC neurons because they encode little about the stimuli that are associated with the rewards [14]. Several human neuroimaging studies have reported vmPFC/mOFC blood oxygen level dependent (BOLD) signals that are proportional to reward expectations
Different decisions in frontal cortex: decisions about rewards and about actions
An alternative interpretation is that vmPFC/mOFC is an important determinant of value-guided decisions (Figure 1c). Not only does vmPFC/mOFC activity level reflect the value of the goal that is currently being pursued [6, 15] but it also represents the values of both options that are being considered during the course of a decision [24, 25••, 26]. There is a positive relationship between vmPFC/mOFC BOLD and the value of the choice taken, and a negative relationship with the value of the choice
Parallel decision-making mechanisms
Perhaps the most intriguing question is whether there is a single valuation system or many valuation systems (Figure 1d). For example, a distinction has been drawn between habitual and goal-based decision-making [34••, 35] and there is evidence for differences between social and non-social decision-making [36]. There may, however, be other types of fundamental distinctions to be drawn between types of value-guided choice.
It is clear that we and other primates can make the binary comparative
Conclusions
In summary, a goods-based account of decision-making provides a persuasive description of several frontal cortical brain regions as well as of the decisions of greatest interest to economists. We may not, however, have evolved to make only such decisions. Other regions such as aPFC and ACC, that encode the best alternative action to the one that is currently being taken or the average richness of the foraging environment, also influence choice (Figure 1, Figure 3, Figure 4). Their existence
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
•• of outstanding interest
Acknowledgements
Funded by the MRC and Wellcome Trust.
References (52)
- et al.
Separable learning systems in the macaque brain and the role of orbitofrontal cortex in contingent learning
Neuron
(2010) - et al.
Appetitive and aversive goal values are encoded in the medial orbitofrontal cortex at the time of decision making
J Neurosci
(2010) - et al.
Separate value comparison and learning mechanisms in macaque medial and lateral orbitofrontal cortex
Proc Natl Acad Sci U S A
(2010) - et al.
Brain hemispheres selectively track the expected value of contralateral options
J Neurosci
(2009) - et al.
Mechanisms underlying cortical activity during value-guided choice
Nat Neurosci
(2012) - et al.
Model-based influences on humans’ choices and striatal prediction errors
Neuron
(2011) - et al.
The computation of social behavior
Science
(2009) - et al.
Fictive reward signals in the anterior cingulate cortex
Science
(2009) Neurobiology of economic choice: a good-based model
Annu Rev Neurosci
(2011)Range-adapting representation of economic value in the orbitofrontal cortex
J Neurosci
(2009)
Adaptation of reward sensitivity in orbitofrontal neurons
J Neurosci
Double dissociation of value computations in orbitofrontal and anterior cingulate neurons
Nat Neurosci
Frontal cortex and reward-guided learning and decision-making
Neuron
Obsessive–compulsive disorder: beyond segregated cortico-striatal pathways
Trends Cogn Sci
The convergence of information about rewarding and aversive stimuli in single neurons
J Neurosci
Re-evaluating the role of orbitofrontal cortex in reward and reinforcement
Eur J Neurosci
Distinct roles of three frontal cortical areas in reward-guided behavior
J Neurosci
Dissociable effects of subtotal lesions within the macaque orbital prefrontal cortex on reward-guided behavior
J Neurosci
Ventromedial and orbital prefrontal neurons differentially encode internally and externally driven motivational values in monkeys
J Neurosci
An automatic valuation system in the human brain: evidence from functional neuroimaging
Neuron
Distinct value signals in anterior and posterior ventromedial prefrontal cortex
J Neurosci
Dissociating valuation and saliency signals during decision-making
Cereb Cortex
Human reinforcement learning subdivides structured action spaces by learning effector-specific values
J Neurosci
How the brain integrates costs and benefits during decision making
Proc Natl Acad Sci U S A
A mechanistic account of value computation in the human brain
Proc Natl Acad Sci U S A
Transformation of stimulus value signals into motor commands during simple choice
Proc Natl Acad Sci U S A
Cited by (227)
Hierarchical control over foraging behavior by anterior cingulate cortex
2024, Neuroscience and Biobehavioral ReviewsBrain responses to decision-making in easy and hard choices in internet gaming disorder: Implications for irrepressible gaming behaviours
2023, Journal of Psychiatric Research