Distinct roles of dorsal and ventral subthalamic neurons in action selection and cancellation

Clayton P Mosher; Adam N Mamelak; Mahsa Malekmohammadi; Nader Pouratian; Ueli Rutishauser

doi:10.1016/j.neuron.2020.12.025

Distinct roles of dorsal and ventral subthalamic neurons in action selection and cancellation

Neuron. 2021 Mar 3;109(5):869-881.e6. doi: 10.1016/j.neuron.2020.12.025. Epub 2021 Jan 21.

Authors

Clayton P Mosher¹, Adam N Mamelak¹, Mahsa Malekmohammadi², Nader Pouratian², Ueli Rutishauser³

Affiliations

¹ Department of Neurosurgery, Cedars-Sinai Medical Center, Los Angeles, CA 90048, USA.
² Department of Neurosurgery, University of California, Los Angeles, Los Angeles, CA 90095, USA.
³ Department of Neurosurgery, Cedars-Sinai Medical Center, Los Angeles, CA 90048, USA; Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USA; Department of Neurology, Cedars-Sinai Medical Center, Los Angeles, CA 90048, USA; Center for Neural Science and Medicine, Department of Biomedical Sciences, Cedars-Sinai Medical Center, Los Angeles, CA 90048, USA. Electronic address: ueli.rutishauser@cshs.org.

Abstract

The subthalamic nucleus (STN) supports action selection by inhibiting all motor programs except the desired one. Recent evidence suggests that STN can also cancel an already selected action when goals change, a key aspect of cognitive control. However, there is little neurophysiological evidence for dissociation between selecting and cancelling actions in the human STN. We recorded single neurons in the STN of humans performing a stop-signal task. Movement-related neurons suppressed their activity during successful stopping, whereas stop-signal neurons activated at low-latencies near the stop-signal reaction time. In contrast, STN and motor-cortical beta-bursting occurred only later in the stopping process. Task-related neuronal properties varied by recording location from dorsolateral movement to ventromedial stop-signal tuning. Therefore, action selection and cancellation coexist in STN but are anatomically segregated. These results show that human ventromedial STN neurons carry fast stop-related signals suitable for implementing cognitive control.

Keywords: action cancellation; cognitive flexibility; human intracranial recordings; single-neuron; stopping; subthalamic nucleus.

Publication types

Research Support, N.I.H., Extramural

MeSH terms

Aged
Female
Humans
Inhibition, Psychological*
Male
Middle Aged
Movement*
Neurons / physiology*
Psychomotor Performance / physiology*
Reaction Time
Subthalamic Nucleus / physiology*

Abstract

Publication types

MeSH terms

Grants and funding