Contribution of somatosensory input to mechanisms of movement suppression during action observation

日常动作的执行，比如抓一个物体，看起来和感觉上都很轻松，但需要复杂的肌肉和关节机械，以及包括脊髓和大脑回路在内的复杂控制系统。越来越多的证据表明，在运动观察期间，这个控制系统的很大一部分是活跃的。20多年前，里佐拉蒂教授和他的同事们在猕猴大脑的F5区发现了单个神经元，不仅对猴子抓取做出反应，而且对人类实验者进行的相同抓取的观察也有反应。这些神经元被称为“镜像神经元”。我们小组在镜像神经元领域做出了重大贡献，发现在F5区和初级运动皮质，即使是直接连接到脊髓运动神经元的神经元，也可以仅通过观察一个动作来调节。在观察动作的过程中，运动系统是活跃的，而没有产生任何动作，这一明显的悖论挑战了我们对运动是如何产生的理解，并促使研究确定运动执行与动作观察的区别。一个明显的候选是对身体表面或内部状态的变化做出反应的体感系统。体感输入在观察手静止时的抓握和在手移动并触摸物体时的抓握执行之间显然是非常不同的。这种差异可能是为什么尽管运动区存在镜像神经元活动，但在动作观察过程中没有发生运动的一个重要因素。体感输入对感知有多么强大的一个戏剧性的例子是“橡皮手”错觉：受试者手的轻抚摸加上对假手同步抚摸的观察，迫使受试者相信人造橡胶手是他们自己的，他们可以控制它。为了了解体感输入对动作观察中运动抑制机制的可能贡献，我们建议研究镜像神经元系统(MNS)的体感特性。这包括单一镜像神经元对光触摸、刷头和被动手部运动的反应。F5区的一些神经元，也就是发现镜像神经元的地方，被证明对这种刺激有反应，但到目前为止还没有对镜像神经元进行测试。更具体地说，我们将调查我们实验室发现的促进和抑制镜像神经元的体感特性的差异。众所周知，在运动过程中，我们对感官输入不那么敏感，比如触摸。这种敏感度的降低表现为，与静息反应相比，对神经的电刺激反应的神经元信号更小。这种现象被称为感觉衰减，但没有对镜像神经元进行测试。旨在揭示动作观察过程中感觉衰减的非侵入性研究是相互矛盾的。一些研究报告了衰减，而另一些研究则报告了增强。要解决这一争议，在局部神经元信号水平上研究感觉衰减是至关重要的。在对MNS的经典研究中，受试者只是被动地观察参与者的动作。在现实生活中，这往往是一种积极的观察。当我们执行一个动作时，我们同时观察到一个相似的动作，例如在一个共同的运动任务中，比如两个外科医生一起工作。在这里，动作观察是在存在体感输入的情况下进行的，这类似于演员的体感输入。由行动执行和行动观察同时驱动的MN会发生什么？为了回答这个问题，我们将结合对非人类灵长类动物的侵入性神经生理学研究和对人类志愿者的非侵入性经颅磁刺激(TMS)研究。

Execution of everyday movements as for example grasping of an object appears and feels effortless but requires a sophisticated mechanical machinery of muscles and joints and a complex control system including spinal cord and brain circuits. There is accumulating evidence that large part of this control system is active during movement observation. More than twenty years ago Prof Rizzolatti and colleagues discovered single neurons in area F5 of macaque monkeys brain responding not only to monkey grasping but also to observation of the same grasp performed by human experimenter. These neurons were called "mirror neurons". Our group made a major contribution to the field of mirror neurons by discovering that in area F5 and in primary motor cortex even neurons directly connected to the spinal motor neurons can be modulated just by observation of an action. This apparent paradox of the motor system being active during action observation without production of any movement challenges our understanding of how movements are generated and prompts research to identify what separate movement execution from action observation.An obvious candidate is somatosensory system that responds to changes to the surface or internal state of the body. Somatosensory input is clearly very different between observation of a grasp when hand is at rest and grasp execution when hand is moving and touching an object. This difference might be an important contributing factor to why movements do not occur during action observation despite mirror neuronal activity present in motor areas. A dramatic examples of how powerful the somatosensory input is for perception is the "rubber hand" illusion: light stroking of subject hand combined with observation of synchronous stroking of an artificial hand forces subjects to believe that an artificial rubber hand is their own and that they can control it. To understand the possible contribution of somatosensory input to the mechanisms of movement suppression during action observation, we suggest to investigate the somatosensory properties of the mirror neuron system (MNS). This includes responses of single mirror neurons to light touch, hair brushing and passive hand movement. Some neurons in area F5, where mirror neurons where discovered, have been shown to respond to such stimulation but it was not so far tested for mirror neurons. And more specifically we will investigate differences in somatosensory properties of facilitation and suppression mirror neurons discovered in our laboratory. It is well established that during movement we are less sensitive to the sensory input, eg touch. This reduced sensitivity manifests itself in a smaller neuronal signal in response to electrical stimulation of the nerve in comparison to the response at rest. This phenomenon is called sensory attenuation but it was not tested for mirror neurons. Non-invasive studies aiming at revealing sensory attenuation during action observation are contradictory. Some studies report attenuation while others enhancement. To resolve this controversy it is critical to investigate sensory attenuation on the level of local neuronal signals.In classical studies of the MNS, subjects just passively observe the actors' movements. In real life, it is quite often an active observation. While we execute an action we simultaneously observe a similar action, e.g. in a shared motor task such as two surgeons working together. Here action observation happens in the presence of somatosensory input, which resembles somatosensory input of an actor. What happens to the MNS simultaneously driven by action execution and action observation? To answer this question we will combine invasive neurophysiological investigation of non-human primates with non-invasive transcranial magnetic stimulation (TMS) studies of human volunteers.