Neural Mechanism Underlying Task-Specific Enhancement of Motor Learning by Concurrent Transcranial Direct Current Stimulation

Ying Wang; Jixian Wang; Qing-Fang Zhang; Ke-Wei Xiao; Liang Wang; Qing-Ping Yu; Qing Xie; Mu-Ming Poo; Yunqing Wen

doi:10.1007/s12264-022-00901-1

Neural Mechanism Underlying Task-Specific Enhancement of Motor Learning by Concurrent Transcranial Direct Current Stimulation

Neurosci Bull. 2023 Jan;39(1):69-82. doi: 10.1007/s12264-022-00901-1. Epub 2022 Jul 30.

Authors

Ying Wang^#^{1

2

3

4}, Jixian Wang^#⁵, Qing-Fang Zhang¹, Ke-Wei Xiao¹, Liang Wang¹, Qing-Ping Yu¹, Qing Xie⁵, Mu-Ming Poo^{6

7

8

9}, Yunqing Wen¹⁰

Affiliations

¹ Institute of Neuroscience, State Key Laboratory of Neuroscience, Key Laboratory of Primate Neurobiology, Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai, 200031, China.
² University of Chinese Academy of Sciences, Beijing, 100049, China.
³ School of Life Science and Technology, ShanghaiTech University, Shanghai, 201210, China.
⁴ Shanghai Center for Brain Science and Brain-Inspired Intelligence Technology, Lingang Laboratory, Shanghai, 201210, China.
⁵ Department of Rehabilitation Medicine, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, 200025, China.
⁶ Institute of Neuroscience, State Key Laboratory of Neuroscience, Key Laboratory of Primate Neurobiology, Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai, 200031, China. mpoo@ion.ac.cn.
⁷ University of Chinese Academy of Sciences, Beijing, 100049, China. mpoo@ion.ac.cn.
⁸ School of Life Science and Technology, ShanghaiTech University, Shanghai, 201210, China. mpoo@ion.ac.cn.
⁹ Shanghai Center for Brain Science and Brain-Inspired Intelligence Technology, Lingang Laboratory, Shanghai, 201210, China. mpoo@ion.ac.cn.
¹⁰ Institute of Neuroscience, State Key Laboratory of Neuroscience, Key Laboratory of Primate Neurobiology, Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai, 200031, China. wenyq@ion.ac.cn.

^# Contributed equally.

Abstract

The optimal protocol for neuromodulation by transcranial direct current stimulation (tDCS) remains unclear. Using the rotarod paradigm, we found that mouse motor learning was enhanced by anodal tDCS (3.2 mA/cm²) during but not before or after the performance of a task. Dual-task experiments showed that motor learning enhancement was specific to the task accompanied by anodal tDCS. Studies using a mouse model of stroke induced by middle cerebral artery occlusion showed that concurrent anodal tDCS restored motor learning capability in a task-specific manner. Transcranial in vivo Ca²⁺ imaging further showed that anodal tDCS elevated and cathodal tDCS suppressed neuronal activity in the primary motor cortex (M1). Anodal tDCS specifically promoted the activity of task-related M1 neurons during task performance, suggesting that elevated Hebbian synaptic potentiation in task-activated circuits accounts for the motor learning enhancement. Thus, application of tDCS concurrent with the targeted behavioral dysfunction could be an effective approach to treating brain disorders.

Keywords: Motor learning; Neural mechanism of tDCS; Neuronal excitability; Stroke model mouse; tDCS effect.

MeSH terms

Motor Cortex* / physiology
Neurons
Transcranial Direct Current Stimulation* / methods
Transcranial Magnetic Stimulation