Article | Published:

Oscillatory dynamics coordinating human frontal networks in support of goal maintenance

Nature Neuroscience volume 18, pages 13181324 (2015) | Download Citation

Abstract

Humans have a capacity for hierarchical cognitive control—the ability to simultaneously control immediate actions while holding more abstract goals in mind. Neuropsychological and neuroimaging evidence suggests that hierarchical cognitive control emerges from a frontal architecture whereby prefrontal cortex coordinates neural activity in the motor cortices when abstract rules are needed to govern motor outcomes. We utilized the improved temporal resolution of human intracranial electrocorticography to investigate the mechanisms by which frontal cortical oscillatory networks communicate in support of hierarchical cognitive control. Responding according to progressively more abstract rules resulted in greater frontal network theta phase encoding (4–8 Hz) and increased prefrontal local neuronal population activity (high gamma amplitude, 80–150 Hz), which predicts trial-by-trial response times. Theta phase encoding coupled with high gamma amplitude during inter-regional information encoding, suggesting that inter-regional phase encoding is a mechanism for the dynamic instantiation of complex cognitive functions by frontal cortical subnetworks.

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Acknowledgements

We thank A. Flinker, J. Hoffman and A. Shestyuk for assistance with data collection, and C. Hamamé, T. Lee and B. Postle for useful comments and suggestions. B.V. is funded by a US National Institutes of Health (NIH) Institutional Research and Academic Career Development Award and the Society for Neuroscience Scholars Program. B.V. is funded by a US National Institutes of Health Institutional Research and Academic Career Development Award (GM081266) and the Society for Neuroscience Scholars Program. A.S.K. is funded by the Department of Veterans Affairs and the National Eye Institute. D.B., E.F.C., N.E.C., J.P. and R.T.K. are funded by the National Institute of Neurological Disorders and Stroke (NS065046, NS065120, NS40596, NS07839601, NS21135). R.T.K. is funded by the Nielsen Corporation. M.D. is funded by the Department of Veterans Affairs and the National Institute of Mental Health (MH063901).

Author information

Affiliations

  1. Helen Wills Neuroscience Institute, University of California, Berkeley, California, USA.

    • Bradley Voytek
    • , David Fegen
    • , Robert T Knight
    •  & Mark D'Esposito
  2. Division of Neurology, Department of Veterans Affairs, Martinez, California, USA.

    • Andrew S Kayser
    •  & Mark D'Esposito
  3. Department of Neurology, UCSF Center for Integrative Neuroscience, University of California, San Francisco, California, USA.

    • Andrew S Kayser
  4. Department of Cognitive, Linguistic and Psychological Sciences, Brown University, Providence, Rhode Island, USA.

    • David Badre
  5. Brown Institute for Brain Science, Brown University, Providence, Rhode Island, USA.

    • David Badre
  6. Department of Neurological Surgery, UCSF Center for Integrative Neuroscience, University of California, San Francisco, California, USA.

    • Edward F Chang
  7. Department of Physiology, UCSF Center for Integrative Neuroscience, University of California, San Francisco, California, USA.

    • Edward F Chang
  8. Department of Neurology, Johns Hopkins Medical Institutions, Baltimore, Maryland, USA.

    • Nathan E Crone
  9. Stanford Human Intracranial Cognitive Electrophysiology Program (SHICEP), Department of Neurology and Neurological Sciences, Stanford University, Stanford, California, USA.

    • Josef Parvizi
  10. Department of Psychology, University of California, Berkeley, California, USA.

    • Robert T Knight
    •  & Mark D'Esposito

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Contributions

B.V., D.B., A.S.K., D.F., R.T.K. and M.D. conceived the study. D.B. and M.D. designed the experiments. D.F. collected the data. B.V. analyzed the data. E.F.C., N.E.C. and J.P. examined the subjects. All of the authors wrote the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Bradley Voytek.

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DOI

https://doi.org/10.1038/nn.4071

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