Scientific Understanding of Consciousness
Consciousness as an Emergent Property of Thalamocortical Activity

Decision-Making in Frontal Lobes

 

PloS Biology, March 2012

Reasoning, Learning, and Creativity: Frontal Lobe Function and Human Decision-Making

Anne Collins, Etienne Koechlin

1 Département d'Etudes Cognitives, Ecole Normale Superieure, Paris, France,

2 Department of Cognitive, Linguistic and Psychological Sciences, Brown University, Providence, Rhode Island, United States of America,

3 Université Pierre et Marie Curie, Paris, France,

4 Laboratoire de Neurosciences Cognitives, Institut National de la Santé et de la Recherche Médicale, Paris, France

[paraphrase]

The frontal lobes subserve decision-making and executive control — i.e., the selection and coordination of goal-directed behaviors. Current models of frontal executive function, however, do not explain human decision-making in everyday environments featuring uncertain, changing, and especially open-ended situations. Here, we propose a computational model of human executive function that clarifies this issue. Using behavioral experiments, we show that unlike others, the proposed model predicts human decisions and their variations across individuals in naturalistic situations. The model reveals that for driving action, the human frontal function monitors up to three/four concurrent behavioral strategies and infers online their ability to predict action outcomes: whenever one appears more reliable than unreliable, this strategy is chosen to guide the selection and learning of actions that maximize rewards. Otherwise, a new behavioral strategy is tentatively formed, partly from those stored in long-term memory, then probed, and if competitive confirmed to subsequently drive action. Thus, the human executive function has a monitoring capacity limited to three or four behavioral strategies. This limitation is compensated by the binary structure of executive control that in ambiguous and unknown situations promotes the exploration and creation of new behavioral strategies. The results support a model of human frontal function that integrates reasoning, learning, and creative abilities in the service of decision-making and adaptive behavior.

Reasoning, learning, and creativity are hallmarks of human intelligence. These abilities involve the frontal lobe of the brain, but it remains unclear how the frontal lobes function in uncertain or open-ended situations. We propose here a computational model of human executive function that integrates multiple processes during decision-making, such as expectedness of uncertainty, task switching, and reinforcement learning. The model was tested in behavioral experiments and accounts for human decisions and their variations across individuals. The model reveals that executive function is capable of monitoring three or four concurrent behavioral strategies and infers online strategies' ability to predict action outcomes. If one strategy appears to reliably predict action outcomes, then it is chosen and possibly adjusted; otherwise a new strategy is tentatively formed, probed, and chosen instead. Thus, human frontal function has a monitoring capacity limited to three or four behavioral strategies. The results support a model of frontal executive function that explains the role and limitations of human reasoning, learning, and creative abilities in decision-making and adaptive behavior.

We provided a computational formulation named the PROBE model. We tested the model predictions in behavioral experiments inspired from the standard neuropsychological test of frontal executive function. We compared the PROBE model to alternative models, and found that the PROBE model predicts human decisions and their variations across individuals. Moreover, the PROBE model that best fits human data is endowed with a monitoring capacity of three or four task sets.

We found that the best account of human decisions is the PROBE model combining forward Bayesian inference for evaluating task set reliability and choosing the most reliable actor set and hypothesis-testing for possibly creating new task sets when facing ambiguous or unknown situations.

Human executive function monitors up to three or four task sets and, when one appears reliable, selects it for driving behavior. Otherwise, the executive function directly creates a new task set and probes it as an actor rather than exploiting only the collection of behavioral strategies associated with current task sets. The probe actor forms a new strategy that recombines previously learned strategies stored in long-term memory and collected according to external cues.

The present study suggests that the prefrontal cortex monitors at most three or four task sets. The frontal network described above selects the unique task set appearing reliable for driving behavior and adjusts it according to action outcomes. When none appear reliable, this frontal network presumably enters in controlled exploration; a new task set is probed but initially appears unreliable, thereby requiring an additional control system to enforce or discard this probe actor. This system needs to monitor at least the second most reliable task set. When both the actor and its best alternative appear unreliable (or no alternative sets are monitored), the system enforces exploration; a new task set is created from long-term memory in the frontal network and drives behavior. Exploration then terminates when either this probe actor or its current best alternative becomes reliable.

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