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

Mosher, Clayton P. and Mamelak, Adam N. and Malekmohammadi, Mahsa and Pouratian, Nader and Rutishauser, Ueli (2021) Distinct roles of dorsal and ventral subthalamic neurons in action selection and cancellation. Neuron, 109 (5). pp. 869-881. ISSN 0896-6273. https://resolver.caltech.edu/CaltechAUTHORS:20201021-081440207

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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.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1016/j.neuron.2020.12.025DOIArticle
https://doi.org/10.1101/2020.10.16.342980DOIDiscussion Paper
https://doi.org/10.17605/OSF.IO/JD5UCDOIData
ORCID:
AuthorORCID
Mamelak, Adam N.0000-0002-4245-6431
Pouratian, Nader0000-0002-0426-3241
Rutishauser, Ueli0000-0002-9207-7069
Additional Information:© 2020 Elsevier Inc. Received 17 October 2020, Revised 12 December 2020, Accepted 30 December 2020, Available online 21 January 2021. We thank Michele Tagliati for patient referrals; the staff and physicians of the Movement Disorders Program at Cedars-Sinai for support; Robert Zelaya, Lori Scheinost, Andy Nguyen, and Cody Holland for assistance with intraoperative recordings; Jan Kaminski, Jeong Woo Choi, Vasileios Christopoulos, and Steven Errington for discussion and feedback on the manuscript; and Adam Aron for advice and for contributing to writing the grant that partially funded this work. This work was supported by the BRAIN initiative through grants from the NINDS (U01NS103792 to U.R. and A.N.M. and U01NS098961 to N.P. and U.R.). Author contributions: M.M., N.P., and U.R. designed experiments. N.P. and U.R acquired funding and supervised the project. M.M. wrote experimental code and organized early phases of the project. A.N.M. performed surgery. A.N.M. and C.P.M. performed experiments and recorded data. C.P.M. analyzed data and wrote the first draft of the manuscript. All authors discussed results at all stages of the project. The authors declare no competing interests. Data and code availability: The data generated in this study will be made available on Open Science Framework (https://osf.io/jd5uc) upon publication (https://doi.org/10.17605/OSF.IO/JD5UC).
Funders:
Funding AgencyGrant Number
NIHU01NS103792
NIHU01NS098961
Subject Keywords:action cancellation; subthalamic nucleus; cognitive flexibility; human intracranial recordings; single-neuron; stopping
Issue or Number:5
Record Number:CaltechAUTHORS:20201021-081440207
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20201021-081440207
Official Citation:Clayton P. Mosher, Adam N. Mamelak, Mahsa Malekmohammadi, Nader Pouratian, Ueli Rutishauser, Distinct roles of dorsal and ventral subthalamic neurons in action selection and cancellation, Neuron, Volume 109, Issue 5, 2021, Pages 869-881.e6, ISSN 0896-6273, https://doi.org/10.1016/j.neuron.2020.12.025. (https://www.sciencedirect.com/science/article/pii/S0896627320310291)
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:106179
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:21 Oct 2020 16:37
Last Modified:03 Mar 2021 22:00

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