Neural Basis of Cognitive Control over Movement Inhibition: Human fMRI and Primate Electrophysiology Evidence

Kitty Z Xu; Brian A Anderson; Erik E Emeric; Anthony W Sali; Veit Stuphorn; Steven Yantis; Susan M Courtney

doi:10.1016/j.neuron.2017.11.010

Neural Basis of Cognitive Control over Movement Inhibition: Human fMRI and Primate Electrophysiology Evidence

Neuron. 2017 Dec 20;96(6):1447-1458.e6. doi: 10.1016/j.neuron.2017.11.010. Epub 2017 Dec 7.

Authors

Kitty Z Xu¹, Brian A Anderson², Erik E Emeric³, Anthony W Sali⁴, Veit Stuphorn⁵, Steven Yantis⁶, Susan M Courtney⁷

Affiliations

¹ Department of Psychological & Brain Sciences, Johns Hopkins University, Baltimore, MD 21218, USA; Pinterest, Inc., San Francisco, CA 94701, USA. Electronic address: kitty.zhexu@gmail.com.
² Department of Psychological & Brain Sciences, Johns Hopkins University, Baltimore, MD 21218, USA; Department of Psychology, Texas A&M University, College Station, TX 77843, USA. Electronic address: brian.anderson@tamu.edu.
³ Department of Neuroscience, Johns Hopkins School of Medicine, Baltimore, MD 21205, USA. Electronic address: erik.emeric@gmail.com.
⁴ Department of Psychological & Brain Sciences, Johns Hopkins University, Baltimore, MD 21218, USA; Center for Cognitive Neuroscience, Duke University, Durham, NC 27708, USA. Electronic address: anthony.sali@duke.edu.
⁵ Department of Neuroscience, Johns Hopkins School of Medicine, Baltimore, MD 21205, USA. Electronic address: veit@jhu.edu.
⁶ Department of Psychological & Brain Sciences, Johns Hopkins University, Baltimore, MD 21218, USA.
⁷ Department of Psychological & Brain Sciences, Johns Hopkins University, Baltimore, MD 21218, USA; Department of Neuroscience, Johns Hopkins School of Medicine, Baltimore, MD 21205, USA; F.M. Kirby Research Center for Functional Brain Imaging, Kennedy Krieger Institute, Baltimore, MD 21205, USA. Electronic address: courtney@jhu.edu.

Abstract

Executive control involves the ability to flexibly inhibit or change an action when it is contextually inappropriate. Using the complimentary techniques of human fMRI and monkey electrophysiology in a context-dependent stop signal task, we found a functional double dissociation between the right ventrolateral prefrontal cortex (rVLPFC) and the bi-lateral frontal eye field (FEF). Different regions of rVLPFC were associated with context-based signal meaning versus intention to inhibit a response, while FEF activity corresponded to success or failure of the response inhibition regardless of the stimulus response mapping or the context. These results were validated by electrophysiological recordings in rVLPFC and FEF from one monkey. Inhibition of a planned behavior is therefore likely not governed by a single brain system as had been previously proposed, but instead depends on two distinct neural processes involving different sub-regions of the rVLPFC and their interactions with other motor-related brain regions.

Keywords: cognitive control; context manipulation; countermanding; executive control; eye movement; fMRI; frontal cortex; frontal cortex electrophysiology; primate electrophysiology; response inhibition; saccades.

Publication types

Research Support, N.I.H., Extramural

MeSH terms

Action Potentials / physiology
Adolescent
Adult
Animals
Brain Mapping*
Conditioning, Operant
Executive Function / physiology*
Female
Humans
Image Processing, Computer-Assisted
Inhibition, Psychological*
Macaca mulatta
Male
Movement / physiology*
Neurons / physiology
Oxygen / blood
Prefrontal Cortex* / cytology
Prefrontal Cortex* / diagnostic imaging
Prefrontal Cortex* / physiology
Psychomotor Performance
Reaction Time / physiology
Young Adult

Substances

Oxygen

Abstract

Publication types

MeSH terms

Substances

Grants and funding