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Neurophysiological mechanisms of error monitoring in human and non-human primates

Nature Reviews Neuroscience volume 24, pages 153–172 (2023)Cite this article

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Abstract

Performance monitoring is an important executive function that allows us to gain insight into our own behaviour. This remarkable ability relies on the frontal cortex, and its impairment is an aspect of many psychiatric diseases. In recent years, recordings from the macaque and human medial frontal cortex have offered a detailed understanding of the neurophysiological substrate that underlies performance monitoring. Here we review the discovery of single-neuron correlates of error monitoring, a key aspect of performance monitoring, in both species. These neurons are the generators of the error-related negativity, which is a non-invasive biomarker that indexes error detection. We evaluate a set of tasks that allows the synergistic elucidation of the mechanisms of cognitive control across the two species, consider differences in brain anatomy and testing conditions across species, and describe the clinical relevance of these findings for understanding psychopathology. Last, we integrate the body of experimental facts into a theoretical framework that offers a new perspective on how error signals are computed in both species and makes novel, testable predictions.

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Fig. 1: Locations of medial frontal lobe areas implicated in performance monitoring and typical recording approaches.
Fig. 2: Error neurons and error-related negativity in macaques and humans.
Fig. 3: Reliability and latency of error responses in macaques and humans.
Fig. 4: Tasks for studying performance monitoring in macaques and humans.
Fig. 5: Conceptual framework for action error computation.
Fig. 6: Circuit model for action error computation.

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Acknowledgements

The authors thank R. Adolphs, K. Silm and J. Brown for discussion and C. Holroyd for valuable comments. J.D.S. has been supported by the US National Institutes of Health and by the E. Bronson Ingram Chair in Neuroscience and is currently supported by the Natural Sciences and Engineering Research Council of Canada (RGPIN-2022-04592). U.R. has been supported by the US National Institutes of Health (R01MH110831 and U01NS117839) and the NSF (BCS-2219800). A.S. has been supported by a Canadian Institutes of Health Research Postdoctoral Fellowship award.

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Authors and Affiliations

  1. Department of Neurosurgery, Cedars-Sinai Medical Center, Los Angeles, CA, USA

    Zhongzheng Fu & Ueli Rutishauser

  2. Division of Humanities and Social Sciences, California Institute of Technology, Pasadena, CA, USA

    Zhongzheng Fu

  3. Center for Integrative & Cognitive Neuroscience, Vanderbilt University, Nashville, TN, USA

    Amirsaman Sajad, Steven P. Errington & Jeffrey D. Schall

  4. Vanderbilt Vision Research Center, Vanderbilt University, Nashville, TN, USA

    Amirsaman Sajad & Steven P. Errington

  5. Department of Psychology, Vanderbilt University, Nashville, TN, USA

    Amirsaman Sajad, Steven P. Errington & Jeffrey D. Schall

  6. Centre for Vision Research, York University, Toronto, Ontario, Canada

    Jeffrey D. Schall

  7. Vision: Science to Applications (VISTA), York University, Toronto, Ontario, Canada

    Jeffrey D. Schall

  8. Department of Biology, Faculty of Science, York University, Toronto, Ontario, Canada

    Jeffrey D. Schall

  9. Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA, USA

    Ueli Rutishauser

  10. Center for Neural Science and Medicine, Department of Biomedical Sciences, Cedars-Sinai Medical Center, Los Angeles, CA, USA

    Ueli Rutishauser

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Glossary

Action errors

Errors made owing to a failure of cognitive control, so that goal-directed responses yield to more automatic responses.

Control command

The identity and intensity of control mechanisms used in a given trial, including contributions from the control inverse model and the feedback controller.

Cognitive control

Ability to adjust behaviour according to the desired goal and to avoid repeating errors through detection of conflict, errors and success.

Corollary discharge

Copy of efferent signals that is provided to sensory or higher-level cognitive structures to enable forward models.

Error-related negativity

(ERN). Evoked potential that is measured over the medial frontal cortex shortly after an action error.

Forward models

Internal models that predict the future state of the motor effector or action selection process on the basis of the current state and a copy of a control or motor command (obtained as a corollary discharge).

Feedback controllers

Controllers that are activated by internally generated feedback (such as action errors). They provide control in a reactive manner.

Inverse models

Internal models that compute which control command is most likely to lead to a desired future state of the system on the basis of knowledge of the dynamics of the system. Used to provide control in a proactive manner.

Medial frontal cortex

(MFC). Areas along the midline of the frontal lobe, including the pre-supplementary motor area, supplementary eye field and middle cingulate cortex.

Middle cingulate cortex

(MCC). A region in the medial frontal cortex, located ventral to the primary motor cortex, supplementary eye field, supplementary motor area, and pre-supplementary motor area in Brodmann area 24. This area contributes to diverse functions, including performance monitoring and cognitive control.

Paracingulate sulcus

(PCS). A sulcus found in some people but not in macaques that is aligned parallel to and located dorsal to the cingulate sulcus in the medial frontal cortex.

Performance monitoring

Ability to monitor one’s own performance, either by self-monitoring or on the basis of external feedback.

Post-error slowing

A delay of response time in the trial following commission of an error response that is found commonly but not uniformly in various choice tasks.

Pre-supplementary motor area

(pre-SMA). An area in the medial frontal lobe, located anterior to the supplementary motor area in Brodmann area 6aβ, that contributes to cognitive control of action.

Superior frontal gyrus

(SFG). Dorsomedial gyrus of the frontal lobe situated along the midline. It includes the medial part of Brodmann area 6, within which the pre-supplementary motor area, supplementary motor area and frontal eye field are located.

Supplementary motor area

(SMA). An area in the medial frontal lobe, located anterior to the primary motor cortex in Brodmann area 6aα, that contributes to the production of self-generated actions.

Supplementary eye field

(SEF). An area in the superior frontal gyrus. It is distinguished from surrounding cortical areas by denser connections with visual and ocular motor structures and by its functional relationship with eye movements.

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Fu, Z., Sajad, A., Errington, S.P. et al. Neurophysiological mechanisms of error monitoring in human and non-human primates. Nat Rev Neurosci 24, 153–172 (2023). https://doi.org/10.1038/s41583-022-00670-w

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