Single-Neuron Correlates of Error Monitoring and Post-Error Adjustments in Human Medial Frontal Cortex

Zhongzheng Fu; Daw-An J Wu; Ian Ross; Jeffrey M Chung; Adam N Mamelak; Ralph Adolphs; Ueli Rutishauser

doi:10.1016/j.neuron.2018.11.016

Single-Neuron Correlates of Error Monitoring and Post-Error Adjustments in Human Medial Frontal Cortex

Neuron. 2019 Jan 2;101(1):165-177.e5. doi: 10.1016/j.neuron.2018.11.016. Epub 2018 Dec 4.

Authors

Zhongzheng Fu¹, Daw-An J Wu², Ian Ross³, Jeffrey M Chung⁴, Adam N Mamelak⁵, Ralph Adolphs⁶, Ueli Rutishauser⁷

Affiliations

¹ Division of Engineering and Applied Sciences, California Institute of Technology, Pasadena, CA, USA; Control and Dynamical Systems Program, California Institute of Technology, Pasadena, CA, USA; Department of Neurosurgery, Cedars-Sinai Medical Center, Los Angeles, CA, USA. Electronic address: zzbrooksfu@gmail.com.
² Division of Humanities and Social Sciences, California Institute of Technology, Pasadena, CA, USA.
³ Department of Neurosurgery, Huntington Memorial Hospital, Pasadena, CA, USA.
⁴ Department of Neurology, Cedars-Sinai Medical Center, Los Angeles, CA, USA.
⁵ Department of Neurosurgery, Cedars-Sinai Medical Center, Los Angeles, CA, USA.
⁶ Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA, USA; Division of Humanities and Social Sciences, California Institute of Technology, Pasadena, CA, USA; Computation and Neural Systems Program, California Institute of Technology, Pasadena, CA, USA.
⁷ Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA, USA; Computation and Neural Systems Program, California Institute of Technology, Pasadena, CA, USA; Department of Neurology, Cedars-Sinai Medical Center, Los Angeles, CA, USA; Department of Neurosurgery, Cedars-Sinai Medical Center, Los Angeles, CA, USA; Center for Neural Science and Medicine, Department of Biomedical Sciences, Cedars-Sinai Medical Center, Los Angeles, CA, USA. Electronic address: rutishauseru@csmc.edu.

Abstract

Humans can self-monitor errors without explicit feedback, resulting in behavioral adjustments on subsequent trials such as post-error slowing (PES). The error-related negativity (ERN) is a well-established macroscopic scalp EEG correlate of error self-monitoring, but its neural origins and relationship to PES remain unknown. We recorded in the frontal cortex of patients performing a Stroop task and found neurons that track self-monitored errors and error history in dorsal anterior cingulate cortex (dACC) and pre-supplementary motor area (pre-SMA). Both the intracranial ERN (iERN) and error neuron responses appeared first in pre-SMA, and ∼50 ms later in dACC. Error neuron responses were correlated with iERN amplitude on individual trials. In dACC, such error neuron-iERN synchrony and responses of error-history neurons predicted the magnitude of PES. These data reveal a human single-neuron correlate of the ERN and suggest that dACC synthesizes error information to recruit behavioral control through coordinated neural activity.

Keywords: anterior cingulate cortex; cognitive control; error monitoring; executive function; human intracranial; human single-neuron; medial frontal cortex; post-error slowing; pre-supplementary motor area.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Action Potentials / physiology
Electroencephalography / methods*
Female
Humans
Magnetic Resonance Imaging / methods
Male
Neurons / physiology*
Photic Stimulation / methods
Prefrontal Cortex / diagnostic imaging*
Prefrontal Cortex / physiology*
Psychomotor Performance / physiology*
Reaction Time / physiology*

Abstract

Publication types

MeSH terms

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