Brain activity, disruption and connectivity comparisons identify origins of human metacognition in other primates

Planning requires anticipating the environmental contingencies that we will encounter and also our own future behaviour in those scenarios. The evolutionary origins of such prospective decision simulations have, however, been difficult to investigate. Moreover, in humans, these metacognitive processes are associated with a distinctively human brain region in the anterior lateral prefrontal cortex. Here we demonstrate these capacities in macaques and their neural bases in two complementary patterns of brain activity in different ventrolateral prefrontal areas: areas 45a and 47/12o. We also examine the impact of ultrasonic disruption of each area. We compare behavioural, brain activity and disruption patterns in humans and macaques. Finally, comparative connectional analysis revealed similarities between the conjunction of the two circuits associated with areas 45a and 47/12o in macaques and the human anterior lateral prefrontal area. In combination, the results suggest behavioural and anatomical origins of metacognitive processes that have become especially sophisticated in humans.

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Publication Details

Journal
Nature Human Behaviour
Published
2026-05-18
DOI
https://doi.org/10.1038/s41562-026-02473-w
Primary Topic
Memory and Neural Mechanisms
Type
article
Field-Weighted Citation Impact
0.00

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article

Brain activity, disruption and connectivity comparisons identify origins of human metacognition in other primates

Nicole Eichert, Nima Khalighinejad, Kentaro Miyamoto, Andrew Emberton et al.
Nature Human Behaviour
Memory and Neural Mechanisms
article

Brain activity, disruption and connectivity comparisons identify origins of human metacognition in other primates

Nicole Eichert, Nima Khalighinejad, Kentaro Miyamoto, Andrew Emberton, Urs Schüffelgen, Simone D’Ambrogio, Caroline Harbison, Rogier B Mars, Matthew FS Rushworth, Jerome Sallet
article en

Abstract

Planning requires anticipating the environmental contingencies that we will encounter and also our own future behaviour in those scenarios. The evolutionary origins of such prospective decision simulations have, however, been difficult to investigate. Moreover, in humans, these metacognitive processes are associated with a distinctively human brain region in the anterior lateral prefrontal cortex. Here we demonstrate these capacities in macaques and their neural bases in two complementary patterns of brain activity in different ventrolateral prefrontal areas: areas 45a and 47/12o. We also examine the impact of ultrasonic disruption of each area. We compare behavioural, brain activity and disruption patterns in humans and macaques. Finally, comparative connectional analysis revealed similarities between the conjunction of the two circuits associated with areas 45a and 47/12o in macaques and the human anterior lateral prefrontal area. In combination, the results suggest behavioural and anatomical origins of metacognitive processes that have become especially sophisticated in humans.

Nature Human Behaviour
Radboud University Nijmegen (NL), RIKEN Center for Brain Science (JP), John Radcliffe Hospital (GB), University of Oxford (GB), Wellcome Centre for Integrative Neuroimaging (GB)
Wellcome, Japan Agency for Medical Research and Development, Wellcome Trust, Ministry of Education, Culture, Sports, Science and Technology, Medical Research Council, Biotechnology and Biological Sciences Research Council, Japan Society for the Promotion of Science
Openalex Percentile: Top 5%
Memory and Neural Mechanisms
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