Representations of Action Monitoring and Cognitive Control by Single Neurons in the Human Brain

Author: Fu, Zhongzheng

Year: 2019

Degree: Dissertation (Ph.D.)

Advisors: Adolphs, Ralph; Rutishauser, Ueli

Committee Members: Murray, Richard M.; Adolphs, Ralph; Rutishauser, Ueli; Burdick, Joel Wakeman; Allman, John Morgan

Option: Control and Dynamical Systems

DOI: 10.7907/RG37-G744

Abstract

Cognitive control arises whenever a prepotent and often automatic response needs to be overcome by another response. Control is usually effortful and relies on monitoring processes that detect when control is needed and/or when it failed. Control is one of the most important aspects of human behavior in everyday life and is a critical component of executive function. In a series of three empirical chapters, I present results from invasive single-neuron recordings from the frontal cortex of neurosurgical human patients while they perform tasks requiring cognitive control. I show that a substantial proportion of neurons in the pre-supplementary motor area (pre-SMA), and in the dorsal anterior cingulate cortex (dACC), signal response errors shortly after they occurred, but well before onset of feedback. Here I demonstrate that these error neurons signal self-detected errors and that they were separate from neurons signaling conflict. The response of error neurons correlated trial-by-trial with the simultaneously recorded intracranial error-related negativity (iERN), thereby establishing a single-neuron correlate of this important scalp potential. iERN-error neuron synchrony in dACC, but not pre-SMA, predicted whether post-error slowing, which is a measure of control, occurred or not. Spike-field coherence between action potentials and local field potentials in specific frequency bands, and latency differences between the different brain regions, suggest a mechanistic model whereby information relevant to control is passed between sectors of the medial frontal cortex. Multiplexing of different ex-post monitoring signals by individual neurons further documents that control relies on multiple sources of information, which can be dynamically routed in the brain depending on task demands. These findings provide the most complete set of single-neuron data on how errors and conflict signals at the single neuron level contribute to cognitive controls in humans. They provide a first-single neuron correlate of an extensively utilized scalp EEG potential. Together, this work provides a strong complement to investigations of this topic using fMRI in humans, and using electrophysiology in monkeys, and suggests specific future directions.

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