Nature Communications ( IF 14.7 ) Pub Date : 2023-11-10 , DOI: 10.1038/s41467-023-43140-2 Natalya D Shelchkova 1 , John E Downey 2 , Charles M Greenspon 2 , Elizaveta V Okorokova 1 , Anton R Sobinov 2 , Ceci Verbaarschot 3, 4 , Qinpu He 1 , Caleb Sponheim 1 , Ariana F Tortolani 1 , Dalton D Moore 1 , Matthew T Kaufman 1, 2, 5 , Ray C Lee 6 , David Satzer 7 , Jorge Gonzalez-Martinez 8 , Peter C Warnke 5, 7 , Lee E Miller 9 , Michael L Boninger 3, 10, 11 , Robert A Gaunt 3, 10, 11, 12 , Jennifer L Collinger 3, 10, 11, 12 , Nicholas G Hatsopoulos 1, 2, 5 , Sliman J Bensmaia 1, 2, 5
The primary motor (M1) and somatosensory (S1) cortices play critical roles in motor control but the signaling between these structures is poorly understood. To fill this gap, we recorded – in three participants in an ongoing human clinical trial (NCT01894802) for people with paralyzed hands – the responses evoked in the hand and arm representations of M1 during intracortical microstimulation (ICMS) in the hand representation of S1. We found that ICMS of S1 activated some M1 neurons at short, fixed latencies consistent with monosynaptic activation. Additionally, most of the ICMS-evoked responses in M1 were more variable in time, suggesting indirect effects of stimulation. The spatial pattern of M1 activation varied systematically: S1 electrodes that elicited percepts in a finger preferentially activated M1 neurons excited during that finger’s movement. Moreover, the indirect effects of S1 ICMS on M1 were context dependent, such that the magnitude and even sign relative to baseline varied across tasks. We tested the implications of these effects for brain-control of a virtual hand, in which ICMS conveyed tactile feedback. While ICMS-evoked activation of M1 disrupted decoder performance, this disruption was minimized using biomimetic stimulation, which emphasizes contact transients at the onset and offset of grasp, and reduces sustained stimulation.
中文翻译:
人类体感皮层的微刺激会引起运动皮层的任务依赖性、空间模式反应
初级运动皮层 (M1) 和体感皮层 (S1) 在运动控制中发挥着关键作用,但这些结构之间的信号传导却知之甚少。为了填补这一空白,我们在一项正在进行的手部瘫痪患者人体临床试验 (NCT01894802) 的三名参与者中记录了在 S1 的手部表征中进行皮质内微刺激 (ICMS) 期间 M1 的手和手臂表征所引起的反应。我们发现 S1 的 ICMS 在短且固定的潜伏期激活一些 M1 神经元,这与单突触激活一致。此外,M1 中大多数 ICMS 诱发的反应在时间上变化更大,表明刺激的间接影响。 M1 激活的空间模式有系统地变化:在手指中引发感知的 S1 电极优先激活在手指运动期间兴奋的 M1 神经元。此外,S1 ICMS 对 M1 的间接影响是上下文相关的,因此相对于基线的大小甚至符号在不同任务中会有所不同。我们测试了这些效应对大脑控制虚拟手的影响,其中 ICMS 传达了触觉反馈。虽然 ICMS 诱发的 M1 激活破坏了解码器的性能,但使用仿生刺激可将这种破坏降至最低,仿生刺激强调抓握开始和偏移时的接触瞬态,并减少持续刺激。