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Social error monitoring in macaque frontal cortex

Abstract

Although much learning occurs through direct experience of errors, humans and other animals can learn from the errors of other individuals. The medial frontal cortex (MFC) processes self-generated errors, but the neuronal architecture and mechanisms underlying the monitoring of others' errors are poorly understood. Exploring such mechanisms is important, as they underlie observational learning and allow adaptive behavior in uncertain social environments. Using two paired monkeys that monitored each other's action for their own action selection, we identified a group of neurons in the MFC that exhibited a substantial activity increase that was associated with another's errors. Nearly half of these neurons showed activity changes consistent with general reward-omission signals, whereas the remaining neurons specifically responded to another's erroneous actions. These findings indicate that the MFC contains a dedicated circuit for monitoring others' mistakes during social interactions.

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Figure 1: Behavioral task and analysis.
Figure 2: Identification of partner-error neurons.
Figure 3: Response of partner-error neurons to type 2 no reward.
Figure 4: Response of partner-error neurons to self-generated errors.
Figure 5: Selectivity of partner-error neurons for partner's errors.
Figure 6: Lack of response to event infrequency.
Figure 7: Relationship of partner error–related activity with correctness of animals' next choices.

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Acknowledgements

We are grateful to O. Hikosaka and C. Yokoyama for valuable comments. This work was supported by a Grant-in-Aid for Japan Society for the Promotion of Science Fellows (K.Y.) and a Precursory Research for Embryonic Science and Technology (M.I.). The monkeys used in this study were provided by the National BioResource Project 'Japanese Monkeys' of the Ministry of Education, Culture, Sports, Science and Technology, Japan.

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K.Y. and M.I. performed all aspects of the study, including the design of the experiment, collecting and analyzing the data, and writing the manuscript. N.S. and A.I. assisted in experimental design and manuscript preparation.

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Correspondence to Atsushi Iriki or Masaki Isoda.

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The authors declare no competing financial interests.

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Yoshida, K., Saito, N., Iriki, A. et al. Social error monitoring in macaque frontal cortex. Nat Neurosci 15, 1307–1312 (2012). https://doi.org/10.1038/nn.3180

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