Hearing Sounds, Understanding Actions: Action Representation in Mirror Neurons
听到声音，理解动作：镜像神经元中的动作表征

In the monkey ventral premotor cortex (area F5, Fig. 1A), there are neurons that discharge both when the monkey performs a specific action and when it observes another individual performing a similar action (mirror neurons) (1–3). We investigated whether there are neurons in F5 that discharge when the monkey performs a specific hand action and also when it hears the corresponding action-related sounds.
在猴子腹侧运动前皮质(F5 区,图 1A)中,存在一些神经元,不仅在猴子执行某一特定动作时会放电,而且在观察另一个个体执行相似动作时也会放电(镜像神经元)(1-3)。我们调查了 F5 区是否存在某些神经元,当猴子执行某一特定的手部动作时会放电,同时也会在听到相应的动作相关声音时放电。

The experiments were carried out in three awake macaque monkeys (Macaca nemestrina) (4). In total, 497 neurons were recorded and their motor and visual properties were assessed (1–3). In an initial group of neurons (n = 211), we studied auditory properties by using sounds produced by the experimenter's actions and non–action-related sounds; in another group (n = 286), we used digitized action-related sounds (4).
该实验于三只清醒的猕猴(Macaca nemestrina)中进行(4)。共记录了 497 个神经元,并评估了其运动和视觉属性(1-3)。在一组初始神经元(n=211)中,我们利用实验员动作产生的声音和非动作相关声音研究了听觉属性;在另一组(n=286)中,我们使用了数字化的动作相关声音(4)。

Sixty-three neurons (13%) discharged both when the monkey performed a hand action and when it heard the action-related sound (5). An example of such a neuron is shown in Fig. 1B (neuron 1). This neuron responded to the vision and sound of a tearing action (paper ripping; V+S). The sound of the same action performed out of the monkey's sight was equally effective (S). Sounds that were non–action-related (white noise, monkey calls) did not evoke any excitatory response (control sounds: CS1, CS2). As a matter of fact, as often occurs in F5 neurons during strong arousal, a decrease in firing rate was observed.
在猴子执行手部动作并听到与动作相关的声音时,有六十三个神经元(13%)都会放电(5)。图 1B(神经元 1)示出了这样一个神经元的例子。这个神经元对撕纸的视觉和声音都有反应(V+S)。即使在猴子看不见的情况下,同样的动作发出的声音也能引发有效反应(S)。与动作无关的声音(白噪声、猴子叫声)则不会引起任何兴奋性反应(对照声音:CS1、CS2)。事实上,正如在 F5 神经元强烈兴奋时经常发生的那样,还观察到了放电率的降低。

Another example is presented in Fig. 1B (neuron 2). This neuron responded to the vision and sound of a hand dropping a stick (V+S). The response was also present when the monkey heard the sound of the stick hitting the floor (S). Non–action-related arousing sounds did not produce any consistent excitation (CS1, CS2).
另一个例子如图 1B 所示(神经元 2)。这个神经元对手掉落棍子的视觉和声音有反应(V+S)。当猴子听到棍子打到地板的声音时,也会出现反应(S)。与行动无关的刺激性声音没有产生任何一致的兴奋(CS1、CS2)。

The effect of non–action-related sounds was statistically assessed in 32 neurons, which were tested with a variety of arousing and emotional sounds such as loud noises and animal calls (4). Except for five neurons that were weakly activated in response to non–action-related sounds, none of the neurons responded significantly (P > 0.05) to these stimuli.
在 32 个神经元中评估了非动作相关声音的作用,这些神经元经受了各种唤醒和情绪声音的测试,如大声噪音和动物叫声(4)。除了 5 个神经元对非动作相关声音的反应较弱外,其他神经元对这些刺激没有显著反应(P>0.05)。

Although monkeys can perform a variety of hand actions that produce sound, breaking and tearing actions are by far the most frequent. Neuronal behavior reflected this fact. The sound of an object breaking and of paper ripping were the most effective stimuli for most tested neurons. Table 1 illustrates the types of effective action-related sounds and the number of neurons that best responded to them.
虽然猴子可以执行各种产生声音的手部动作,但打破和撕裂动作无疑是最常见的。神经行为反映了这一事实。物体破裂的声音和纸张撕裂的声音是大多数测试神经元最有效的刺激。表 1 说明了有效的动作相关声音类型以及最佳响应于它们的神经元数量。

Once having established that area F5 contains neurons that specifically respond to action-related auditory stimuli, we addressed the issue of their capacity to differentiate actions on the basis of auditory and visual characteristics (4). For this purpose, we studied a set of neurons (n = 33) with an experimental design in which two hand actions were randomly presented in vision-and-sound, sound-only, vision-only, and motor conditions (monkeys performing object-directed actions). Twenty-nine neurons showed auditory selectivity (Table 2). Of them, 22 were also visually selective for the same action (audiovisual mirror neurons). Three neurons were visually unselective, and four did not show a significant visual response. Two examples of neurons showing auditory selectivity are presented in Fig. 2A.
在确定区域 F5 包含对动作相关听觉刺激做出特异性反应的神经元之后，我们研究了它们区分基于听觉和视觉特征的动作的能力(4)。为此,我们研究了一组神经元(n = 33),实验设计包括两种手部动作在视觉-声音、仅声音、仅视觉和运动条件下(猴子执行面向对象的动作)随机呈现。二十九个神经元显示出听觉选择性(表 2)。其中,22 个也对相同的动作具有视觉选择性(双模镜像神经元)。三个神经元没有视觉选择性,四个没有显著的视觉反应。图 2A 展示了两个显示听觉选择性的神经元的例子。

Neuron 3 discharged when the monkey observed the experimenter breaking a peanut (V+S, and V) and when the monkey heard the peanut being broken without seeing the action (S). The neuron also discharged when the monkey made the same action (M). Grasping a ring and the resulting sound of this action (4) evoked small responses. A statistical criterion (4) yielded both auditory and visual selectivity for this neuron. By analyzing the vision-only and sound-only conditions separately (Newman–Keuls test,P < 0.05), selectivity was apparent in both cases.
神经元 3 在观察到猴子实验员打碎花生(V+S 和 V)时以及猴子听到花生被打碎但看不到动作(S)时会放电。当猴子做出同样的动作(M)时,该神经元也会放电。握住环和这一动作产生的声音(4)引发了较小的反应。统计标准(4)产生了该神经元对听觉和视觉的选择性。通过单独分析视觉条件和声音条件(Newman–Keuls 检验,P < 0.05),可以看出在这两种情况下都存在选择性。

Neuron 4 is another example of a selective audiovisual mirror neuron. This neuron responded vigorously when the monkey broke a peanut and much less when it ripped a sheet of paper (M). This selectivity was also observed when the monkey saw and heard the experimenter breaking a peanut (V+S). The sound alone of breaking a peanut produced a significant but smaller response (S), thus showing the importance of the visual modality for this neuron. However, the vision of breaking a peanut without the natural sound triggered no response. Indeed, the sound of a peanut breaking is an important signal that the operation is successful. The behavior of neuron 4 reflects this phenomenon. Paper ripping produced small responses in all conditions.
神经元 4 是另一个选择性视觉听觉镜像神经元的例子。这个神经元在猴子咬开花生时反应强烈,而在撕纸时反应要小得多(M)。当猴子看到并听到实验者咬开花生时,也观察到了这种选择性(V+S)。仅仅听到花生被咬开的声音也会产生显著但较小的反应(S),这表明视觉通路对这个神经元很重要。然而,在没有自然声音的情况下,看到花生被咬开也不会引起任何反应。实际上,花生被咬开的声音是一个重要信号,表明这个动作已经成功完成。神经元 4 的行为反映了这一现象。撕纸在所有条件下都会产生较小的反应。

For 16 neurons, the intensity of the discharge in vision-only, sound-only, and vision-and-sound conditions did not differ significantly (Newman–Keuls, P > 0.05, as for neuron 3). In 10 of the remaining neurons, the response in V+S was significantly larger than that in S (Newman–Keuls, P< 0.05, as for neuron 4). The latter neurons required both modalities to describe the action event, which reflects what normally occurs in nature, where, within a social environment, vision and sound of hand actions are typically coupled. Finally, in the remaining three neurons the response to sound alone was the strongest.
对于 16 个神经元来说,视觉、声音单独及视听双重条件下的放电强度没有显著差异(Newman-Keuls 检验,P>0.05,与神经元 3 相同)。在其余 10 个神经元中,V+S 条件下的响应显著大于 S 条件(Newman-Keuls 检验,P<0.05,与神经元 4 相同)。后者的神经元需要两种感觉通路来描述行为事件,这反映了自然界中正常存在的情况,在社会环境中,手部动作的视觉和声音信息通常是耦合的。最后,在剩余的 3 个神经元中,仅声音刺激引起的响应最强。

A population analysis (Fig. 2B, rightmost column) based on all 33 neurons analyzed confirmed the data observed in individual neurons (4). The population of neurons responded to the sound of actions and discriminated between the sounds of different actions. The actions whose sounds were preferred were also the actions that produced the strongest vision-only and motor responses.
根据对所分析的 33 个神经元进行的群体分析(图 2B,最右侧列),确认了在单个神经元中观察到的数据(4)。神经元群体对动作声音做出响应,并能区分不同动作的声音。偏好的动作声音也是产生最强视觉和电机响应的动作。

In conclusion, area F5 contains a population of neurons—audio-visual mirror neurons—that discharge not just to the execution or observation of a specific action but also when this action can only be heard. Multimodal neurons have been described in several cortical areas and subcortical centers, including the superior temporal sulcus region (6–8), the ventral premotor cortex (9–14), and the superior colliculus (15). These neurons, however, responded to specific stimulus locations or directions of movement. The difference with the neurons described here is that they do not code space, or some spatial characteristics of stimuli, but actions when they are only heard.
总之,F5 区域包含一群神经元——视听镜像神经元——不仅会在执行或观察某个特定动作时放电,而且在只能听到这个动作时也会放电。多感觉神经元已经在几个皮层区域和皮下中心被描述,包括上颞沟区域(6-8)、腹侧运动前区(9-14)和上丘(15)。但是,这些神经元只对特定的刺激位置或运动方向做出反应。与本文描述的神经元不同的是,它们不编码空间或某些刺激的空间特征,而是只有在听到动作时才会反应。

A further difference is that audiovisual mirror neurons also discharge during execution of specific motor actions. Therefore, they are part of the vocabulary of action previously described in area F5. This vocabulary contains not only schemas on how an action should be executed (for example, grip selection) but also the action ideas—that is, actions expressed in terms of their goals (for example, grasp, hold, or break) (16). Audiovisual mirror neurons could be used, therefore, to plan/execute actions (as in our motor conditions) and to recognize the actions of others (as in our sensory conditions), even if only heard, by evoking motor ideas.
另一个不同之处在于,视听镜像神经元在执行特定的运动动作时也会放电。因此,它们是之前在 F5 区域描述的动作词汇表的一部分。这个词汇表不仅包含了如何执行动作的模式(例如,选择握持方式),还包含了动作概念,即以其目标来表达动作(例如,抓取、握持或破坏)。因此,视听镜像神经元可以用于计划/执行动作(像我们的运动条件)以及识别他人的动作(像我们的感知条件),即使只是通过听到也能唤起运动概念。

Mirror neurons may be a key to gestural communication (17). The activity of ripping neurons in my brain leads me (if the circumstances are appropriate) to rip a sheet of paper. This overt action will activate your F5 ripping mirror neurons. The action becomes information. This information can be decoded in your brain thanks to the matching properties of your mirror neurons. What is intriguing about the discovery of audiovisual mirror neurons is that they are observed in an area that appears to be the homolog of human Broca's area (area 44) (18). The recent demonstration of a left-right asymmetry in the ventral premotor cortex of great apes (19) indicates that the human motor speech area is the result of a long evolutionary process, already started in nonhuman primates. The discovery of audiovisual mirror neurons in this location may shed light on the evolution of spoken language for two main reasons: First, these neurons have the capacity to represent action contents; second, they have auditory access to these contents so characteristic of human language.
镜像神经元可能是手势交流的关键(17)。我大脑中丢弃神经元的活动会导致我(在合适的情况下)撕扯一张纸。这个明显的动作会激活你 F5 撕扯镜像神经元。这个动作成为了信息。这一信息可以借助你的镜像神经元的匹配特性在你的大脑中得以解码。令人着迷的是,发现视听镜像神经元的区域似乎是人类布罗卡区(44 区)的同源区(18)。最近在大型类人猿腹侧运动前皮层中发现左右不对称(19)表明,人类语音运动区域是一个漫长进化过程的结果,早已经开始出现在非人类灵长类动物中。在这一区域发现视听镜像神经元的发现可能会为语言演化提供线索,主要有两个原因:首先,这些神经元具有表征行动内容的能力;其次,它们能访问这些与人类语言特征相似的内容。

Materials and Methods 材料与方法