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Scientific Understanding of Consciousness |
Decision-Making, ACC and vmPFC
Science 6 April 2012: Nils Kolling1, Timothy E. J. Behrens1,2, Rogier B. Mars1,2, Matthew F. S. Rushworth1,2 1Department of Experimental Psychology, University of Oxford, Oxford OX1 3UD, UK. 2Oxford Centre for Functional Magnetic Resonance Imaging of the Brain (FMRIB), University of Oxford, Oxford OX3 9DU, UK. [paraphrase] Recent insights into the neural mechanisms of decision-making have come from investigations in behavioral economics. Participants typically decide between limited numbers of options differing in probability, risk, and amount of reward. Despite their success in explaining the choices animals make, the optimal foraging models of ecology have had little impact on cognitive neuroscience or economics. The key foraging choice is usually not a binary one between currently available options; instead, it is whether or not to engage with options as they are encountered. It depends not just on (i) the value of the option encountered (encounter value) but also on estimates of (ii) the environment’s average value (search value), and (iii) the cost of leaving to forage for alternatives (search cost). We used functional magnetic resonance imaging to examine the neural mechanisms mediating foraging. Human participants made foraging-style choices (forages) to either engage with current options of known value or search among a set of potential alternatives also of known value. Logistic regression identified factors weighing on forages and decisions. Comparison of average activity during foraging and decisions identified anterior cingulate cortex (ACC) among other regions. Usually in decisions, the most common signal observed in ACC is inversely related to the value difference between chosen and unchosen options. Such inverse value difference effects have been interpreted as indicating that ACC or dorsomedial frontal cortex is a “comparator” comparing choice values. Our task allowed us to test whether the ACC signal reflects the relative benefit of the alternative course of action or the value of exploring the environment. This hypothesis predicts that ACC during forages will stop reflecting the value of the unchosen option and will always represent the value of searching. The blood-oxygen-level–dependent (BOLD) contrast for ACC was positively correlated with the value of searching the environment and negatively correlated with the value of engaging with the current encounter option. Knowledge of environmental richness, which is normally pertinent to foraging but irrelevant to binary decision-making, impinges on, and impairs, simultaneous binary decision-making in behavioral experiments. Conflict and comparator-based theories remain the most influential accounts of decision-related activity in ACC. We suggest that ACC codes the value of switching to a course of action alternative to the one in progress. Ventromedial prefrontal cortex (vmPFC) encodes the value of the option in progress in comparison with alternative options. During foraging, however, vmPFC activity only reflected the chosen option value when participants engaged, and there was no representation of search value. Reward prediction error signals associated with the ventral striatum and its interactions with orbitofrontal cortex allow decision-making to change with experience. We examined whether forage prediction errors were also encoded by the striatum and its interactions with the ACC. An ACC region overlapping with, but anterior to, the search value effect was more coupled with left ventral striatum when search costs increased and search was chosen. VmPFC and ACC have been thought to operate in sequence during choice, but our results suggest that ACC represents choice in a manner at odds with intuitions of how comparative decisions are made. Because ACC value representations are anchored to response strategy (engage or search), our results confirm that it is well placed to guide response selection. However, the different signals in ACC and vmPFC attest to independent roles in forages and decisions. The implication of ACC in foraging and encoding of the average value of the foraging environment may facilitate understanding of the reward signal it carries, its prominence during exertion of effort, in go–no go decisions, in exploration, and in representing alternative and counterfactual choice values. Some action value learning tasks previously used to investigate ACC may have been treated as foraging tasks, and animals may have been choosing whether to stay with the current choice or switch to an alternative. Such a perspective also makes it possible to reinterpret ACC activation recorded during exploration tasks as reflecting estimates of richness of alternatives in the environment. ACC activity is frequently recorded and might reflect the value of alternative choices in other tasks and the inclination to refrain from engaging in the currently offered choice. Foraging entails energetic costs, and we found that ACC activity also reflected the cost of foraging. ACC neurons have been shown to encode value signals that integrate both cost and reward. By contrast, vmPFC, a primate specialization, may underpin fine-grained, accurate, and flexible decision-making. [end of paraphrase]
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