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Switching from automatic to controlled action by monkey medial frontal cortex

Nature Neuroscience volume 10, pages 240–248 (2007)Cite this article

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Abstract

Human behavior is mostly composed of habitual actions that require little conscious control. Such actions may become invalid if the environment changes, at which point individuals need to switch behavior by overcoming habitual actions that are otherwise triggered automatically. It is unknown how the brain controls this type of behavioral switching. Here we show that the presupplementary motor area (pre-SMA) in the medial frontal cortex has a function in switching from automatic to volitionally controlled action in rhesus macaque monkeys. We found that a group of pre-SMA neurons was selectively activated when subjects successfully switched to a controlled alternative action. Electrical stimulation in the pre-SMA replaced automatic incorrect responses with slower correct responses. A further test suggested that the pre-SMA enabled switching by first suppressing an automatic unwanted action and then boosting a controlled desired action. Our data suggest that the pre-SMA resolves response conflict so that the desired action can be selected.

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Figure 1: Behavioral task and animal performance.
Figure 2: Switch-selective activity of pre-SMA neurons.
Figure 3: Effects of electrical stimulation in the pre-SMA on performance of the cue-switch trials.
Figure 4: Characterization of pre-SMA switch neurons using the saccade go or no-go task.

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Acknowledgements

We are grateful to B.G. Cumming for help in statistical analysis, R.H. Wurtz, R.J. Leigh, K. Nakamura, L. Ding and M. Matsumoto for comments and discussions and M.K. Smith, J.W. McClurkin, T.W. Ruffner, A.M. Nichols, A.V. Hays and L.P. Jensen for technical assistance. This work was supported by the intramural research program of the National Eye Institute.

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Authors and Affiliations

  1. Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, 49 Convent Drive, Bethesda, 20892, Maryland, USA

    Masaki Isoda & Okihide Hikosaka

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  1. Masaki Isoda
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Contributions

M.I. and O.H. jointly designed the study, performed the experiments, conducted the data analyses and wrote the manuscript.

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Correspondence to Masaki Isoda.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

Estimation of the pre-SMA efferent conduction delay. (PDF 25 kb)

Supplementary Figure 2

Schematic illustration of the locations of neuronal recording and electrical stimulation. (PDF 178 kb)

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Isoda, M., Hikosaka, O. Switching from automatic to controlled action by monkey medial frontal cortex. Nat Neurosci 10, 240–248 (2007). https://doi.org/10.1038/nn1830

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