Noel Jean-Paul, Bockbrader Marcie, Bertoni Tommaso, Colachis Sam, Solca Marco, Orepic Pavo, Ganzer Patrick D, Haggard Patrick, Rezai Ali, Blanke Olaf, Serino Andrea
Department of Neuroscience, University of Minnesota, Minneapolis, Minnesota, United States of America.
Minnesota Robotics Institute, University of Minnesota, Minneapolis, Minnesota, United States of America.
PLoS Biol. 2025 Apr 17;23(4):e3003118. doi: 10.1371/journal.pbio.3003118. eCollection 2025 Apr.
Self-initiated behavior is accompanied by the experience of intending our actions. Here, we leverage the unique opportunity to examine the full intentional chain-from intention to action to environmental effects-in a tetraplegic person outfitted with a primary motor cortex (M1) brain-machine interface (BMI) generating real hand movements via neuromuscular electrical stimulation (NMES). This combined BMI-NMES approach allowed us to selectively manipulate each element of the intentional chain (intention, action, effect) while probing subjective experience and performing extra-cellular recordings in human M1. Behaviorally, we reveal a novel form of intentional binding: motor intentions are reflected in a perceived temporal attraction between the onset of intentions and that of actions. Neurally, we demonstrate that evoked spiking activity in M1 largely coincides in time with the onset of the experience of intention and that M1 spike counts and the onset of subjective intention may co-vary on a trial-by-trial basis. Further, population-level dynamics, as indexed by a decoder instantiating movement, reflect intention-action temporal binding. The results fill a significant knowledge gap by relating human spiking activity in M1 with the onset of subjective intention and complement prior human intracranial work examining pre-motor and parietal areas.
自发行为伴随着我们对自身行动的意图体验。在此,我们利用一个独特的机会,对一名四肢瘫痪患者进行研究,该患者配备了通过神经肌肉电刺激(NMES)产生真实手部运动的初级运动皮层(M1)脑机接口(BMI),以此来考察从意图到行动再到环境影响的完整意图链条。这种BMI与NMES相结合的方法使我们能够在探究主观体验并在人类M1中进行细胞外记录的同时,选择性地操纵意图链条的每个要素(意图、行动、结果)。在行为层面,我们揭示了一种新的意图绑定形式:运动意图体现在意图开始与行动开始之间的一种感知到的时间吸引力上。在神经层面,我们证明M1中诱发的尖峰活动在时间上与意图体验的开始基本一致,并且M1的尖峰计数与主观意图的开始可能在逐次试验的基础上共同变化。此外,由实例化运动的解码器所索引的群体水平动态反映了意图 - 行动的时间绑定。这些结果通过将人类M1中的尖峰活动与主观意图的开始联系起来,填补了一个重大的知识空白,并补充了之前在人类颅内进行的关于运动前区和顶叶区域的研究。