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Managing competing goals — a key role for the frontopolar cortex

Key Points

  • In primates, the foremost part of prefrontal cortex (the frontopolar cortex) contains cortical 'area 10', which is of special interest because it is exclusive to primates and proportionally larger in humans than in non-human primates and because it has a pattern of anatomical connections that suggests it sits at the top of a prefrontal hierarchy.

  • Although there are many influential theories of frontopolar function based on human neuroimaging and neuropsychological investigations, its contribution to cognition has not yet been specified.

  • Importantly, lesions of the frontopolar cortex in monkeys lead to a distinct pattern of spared, impaired and, in some cases, enhanced cognitive abilities.

  • Considering all these animal experiments, we conclude that a key specialization of primate frontopolar cortex is in managing competing goals, in part by keeping track of the importance of current and alternative goals, and therefore enabling switching away from ongoing behaviour.

  • A particular set of recent studies in humans combining human neuroimaging and computational modelling has provided a synergistic view with these recent animal studies while also revealing new insights about specific features of the human frontopolar cortex, which we argue has acquired additional but related roles in allowing monitoring of the importance of several competing goals in parallel and switching between them.

  • We consider whether these new functions may be linked to a lateral subdivision of cytoarchitectural area 10, which some data suggest might have no clear monkey counterpart; however, if this is the case, then this function may explain the activation of the lateral frontopolar cortex in several key cognitive paradigms, such as exploration, cognitive branching, abstract reasoning and problem-solving.

Abstract

Humans are set apart from other animals by many elements of advanced cognition and behaviour, including language, judgement and reasoning. What is special about the human brain that gives rise to these abilities? Could the foremost part of the prefrontal cortex (the frontopolar cortex), which has become considerably enlarged in humans during evolution compared with other animals, be important in this regard, especially as, in primates, it contains a unique cytoarchitectural field, area 10? The first studies of the function of the frontopolar cortex in monkeys have now provided critical new insights about its precise role in monitoring the significance of current and alternative goals. In human evolution, the frontopolar cortex may have acquired a further role in enabling the monitoring of the significance of multiple goals in parallel, as well as switching between them. Here, we argue that many other forms of uniquely human behaviour may benefit from this cognitive ability mediated by the frontopolar cortex.

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Figure 1: Neuroanatomy of the frontopolar cortex.
Figure 2: Adaptive goal-directed behaviour requires a balance between exploitation of the current goal and the tendency to shift towards an alternative goal.
Figure 3: Neuronal activity in posterior and anterior prefrontal cortex of the macaque monkey.
Figure 4: Behavioural consequences of selective and bilateral lesions within the frontopolar cortex.
Figure 5: Functional model of the frontopolar cortex in monkeys.
Figure 6: Functional model of the frontopolar cortex in humans.

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Acknowledgements

We would like to thank Keiji Tanaka (at RIKEN Brain Science Institute) for his contribution to our proposed functional model of the frontopolar cortex in monkeys. We would like to thank R. Tweedale for editorial suggestions..

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The authors all wrote the article, and all authors researched data for it. The authors all made a substantial contribution to the discussion of content and reviewed and/or edited the manuscript before submission.

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PowerPoint slides

Glossary

Episodic memory

A memory of events enriched by contextual information such as the associated emotion, place and time.

Working memory

A process of short-term storage of information to support ongoing or upcoming actions.

Analogical reasoning

A process of reasoning based on comparison between objects, events or models to help in understanding, learning and decision-making.

Transitive inference

A process of reasoning based on relationships between objects or events to help in understanding, learning and decision-making.

Theory of mind

Cognitive ability that allows one to infer someone else's beliefs, intents, desires and feelings.

Tower of London test

A cognitive test of planning in which participants must plan the order of balls on a peg based on a given template.

Conflict cost

The adverse effects on speed and accuracy that arise as a result of competition or conflict between behavioural choices in experimental tasks.

Conflict adaptation

The behavioural effects of conflict that affect performance in the subsequent trial, where they are manifested as a behavioural improvement if the subject is faced with conflict again.

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Mansouri, F., Koechlin, E., Rosa, M. et al. Managing competing goals — a key role for the frontopolar cortex. Nat Rev Neurosci 18, 645–657 (2017). https://doi.org/10.1038/nrn.2017.111

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