Adenosine A2A receptor blockade improves neuroprosthetic learning by volitional control of population calcium signal in M1 cortical neurons. (1st November 2020)

• Record Type: Journal Article
• Authors: Zhang, Liping; Zhou, Yuling; Liu, Chengwei; Zheng, Wu; Yao, Zhimo; Wang, Qin; Jin, Yile; Zhang, Shaomin; Chen, Weidong; Chen, Jiang-Fan
• Is Part Of: Neuropharmacology. Volume 178(2020)
• Publication Date: 2020-11-01
• Subjects: Volitional control -- Brain-machine interfaces -- Population calcium signal -- Adenosine A2A receptor -- Neuroprosthetic learning -- Representation neuroplasticity; Neuropsychopharmacology -- Periodicals; Autonomic Agents -- Periodicals; Neuropsychopharmacologie -- Périodiques; Neuropsychopharmacology; Periodicals; Electronic journals; 615.78
• DOI: 10.1016/j.neuropharm.2020.108250
• Languages: English
• ISSNs: 0028-3908

Abstract

Abstract: Volitional control is at the core of brain-machine interfaces (BMI) adaptation and neuroprosthetic-driven learning to restore motor function for disabled patients, but neuroplasticity changes and neuromodulation underlying volitional control of neuroprosthetic learning are largely unexplored. To better study volitional control at annotated neural population, we have developed an operant neuroprosthetic task with closed-loop feedback system by volitional conditioning of population calcium signal in the M1 cortex using fiber photometry recording. Importantly, volitional conditioning of the population calcium signal in M1 neurons did not improve within-session adaptation, but specifically enhanced across-session neuroprosthetic skill learning with reduced time-to-target and the time to complete 50 successful trials. With brain-behavior causality of the neuroprosthetic paradigm, we revealed that proficiency of neuroprosthetic learning by volitional conditioning of calcium signal was associated with the stable representational (plasticity) mapping in M1 neurons with the reduced calcium peak. Furthermore, pharmacological blockade of adenosine A2A receptors facilitated volitional conditioning of neuroprosthetic learning and converted an ineffective volitional conditioning protocol to be the effective for neuroprosthetic learning. These findings may help to harness neuroplasticity for better volitional control of neuroprosthetic training and suggest a novel pharmacological strategy to improve neuroprosthetic learning in BMI adaptation by targeting striatal A2A receptors. Highlights: The development of a population calcium-based neuroprosthetic task by volitional control. Calcium signal in M1 neurons supports across-session neuroprosthetic learning. Proficiency of volitional control is associated with stable representational mapping. Adenosine A2A receptors blockade improves volitional control of neuroprosthetic task.