Mirror Neurons and the Evolution of Embodied Language

ABSTRACT— Mirror neurons are a class of neurons first discovered in the monkey premotor cortex that activate both when the monkey executes an action and when it observes the same action made by another individual. These neurons enable individuals to understand actions performed by others. Two subcategories of mirror neurons in monkeys activate when they listen to action sounds and when they observe communicative gestures made by others, respectively. The properties of mirror neurons could constitute a substrate from which more sophisticated forms of communication evolved; this would make sense, given the anatomical and functional homology between part of the monkey premotor cortex and Broca's area (the "speech" area of the brain) in humans. We hypothesize that several components of human language, including some aspects of phonology and syntax, could be embedded in the organizational properties of the motor system and that a deeper knowledge of this system could shed light on how language evolved.     

Mirror neurons and the simulation theory of mind-reading

A new class of visuomotor neuron has been recently discovered in the monkey's premotor cortex: mirror neurons. These neurons respond both when a particular action is performed by the recorded monkey and when the same action, performed by another individual, is observed. Mirror neurons appear to form a cortical system matching observation and execution of goal-related motor actions. Experimental evidence suggests that a similar matching system also exists in humans. What might be the functional role of this matching system? One possible function is to enable an organism to detect certain mental states of observed conspecifics. This function might be part of, or a precursor to, a more general mind-reading ability. Two different accounts of mind-reading have been suggested. According to ‘theory theory', mental states are represented as inferred posits of a naive theory. According to ‘simulation theory', other people's mental states are represented by adopting their perspective: by tracking or matching their states with resonant states of one's own. The activity of mirror neurons, and the fact that observers undergo motor facilitation in the same muscular groups as those utilized by target agents, are findings that accord well with simulation theory but would not be predicted by theory theory.     

Mirror neurons, the representation of word meaning, and the foot of the third left frontal convolution

Previous neuroimaging research has attempted to demonstrate a preferential involvement of the human mirror neuron system (MNS) in the comprehension of effector-related action word (verb) meanings. These studies have assumed that Broca's area (or Brodmann's area 44) is the homologue of a monkey premotor area (F5) containing mouth and hand mirror neurons, and that action word meanings are shared with the mirror system due to a proposed link between speech and gestural communication. In an fMRI experiment, we investigated whether Broca's area shows mirror activity solely for effectors implicated in the MNS. Next, we examined the responses of empirically determined mirror areas during a language perception task comprising effector-specific action words, unrelated words and nonwords. We found overlapping activity for observation and execution of actions with all effectors studied, i.e., including the foot, despite there being no evidence of foot mirror neurons in the monkey or human brain. These "mirror" areas showed equivalent responses for action words, unrelated words and nonwords, with all of these stimuli showing increased responses relative to visual character strings. Our results support alternative explanations attributing mirror activity in Broca's area to covert verbalisation or hierarchical linearisation, and provide no evidence that the MNS makes a preferential contribution to comprehending action word meanings.     

镜像神经元的意义

镜像神经元是一种感觉–运动神经元。它的典型特征是在动作观察和动作执行两个阶段皆被激活。多年来, 由于研究伦理的限制, 研究恒河猴时使用的单细胞电极植入方式无法应用于人类, 因而不能确定人类大脑皮层是否也存在着具有同样功能的神经细胞。但是通过脑成像技术, 神经科学家确定人类大脑皮层存在着具有相同或类似功能的脑区, 称为“镜像神经系统”。文章对镜像神经元及其人类镜像神经系统的意义进行了深入分析, 指出：(1)由于镜像机制把动作知觉和动作执行进行匹配, 观察者仅仅通过他人行为的知觉, 就激活了执行这一动作的神经环路, 产生了一种他人动作的具身模拟, 因而可以直接把握他人的行为意图; (2)镜像神经元所表现出来的那种动作知觉与动作执行的双重激活功能支持了身心一体说, 从方法论上证明了身心二元论的缺陷, 为身心的整体观提供了神经生物学的证据; (3)镜像神经机制把他人的动作与自己的运动系统相匹配, 以自身动作的神经环路对他人的动作做出回应, 促进了人际理解和沟通, 成为社会沟通的“神经桥梁”。     

Spoken language and arm gestures are controlled by the same motor control system

Arm movements can influence language comprehension much as semantics can influence arm movement planning. Arm movement itself can be used as a linguistic signal. We reviewed neurophysiological and behavioural evidence that manual gestures and vocal language share the same control system. Studies of primate premotor cortex and, in particular, of the so-called "mirror system", including humans, suggest the existence of a dual hand/mouth motor command system involved in ingestion activities. This may be the platform on which a combined manual and vocal communication system was constructed. In humans, speech is typically accompanied by manual gesture, speech production itself is influenced by executing or observing transitive hand actions, and manual actions play an important role in the development of speech, from the babbling stage onwards. Behavioural data also show reciprocal influence between word and symbolic gestures. Neuroimaging and repetitive transcranial magnetic stimulation (rTMS) data suggest that the system governing both speech and gesture is located in Broca's area. In general, the presented data support the hypothesis that the hand motor-control system is involved in higher order cognition.     

New insights on sensorimotor integration: from hand action to speech perception

In the last two decades the integrative role of the frontal premotor cortex (a mosaic of agranular/disgranular areas lying in front of the primary motor cortex) have been more and more elucidated. Among its various functions, sensorimotor transformation, and action representation storage, also for nonstrictly motor purposes, are the most intriguing properties of this region, as shown by several researches. In this article we will mainly focus on the ventro-rostral part of the monkey premotor cortex (area F5) in which visual information describing objects and others' acting hands are associated with goal-directed motor representations of hand movements. We will describe the main characteristics of F5 premotor neurons and we will provide evidence in favor of a parallelism between monkeys and humans on the basis of new experimental observations. Finally, we will present some data indicating that, both in humans and in monkeys, action-related sensorimotor transformations are not restricted to visual information but concern also acoustic information.     

镜像神经元是认知科学的“圣杯”吗?

镜像神经元作为近二十年来神经科学领域内最重要的发现之一,相关的一系列研究掀起了一场"理解社会行为的革命"。然而,通过系统考察镜像神经元最初的操作性定义、基本功能及其实验证据,发现许多研究者对于镜像神经元的定义存在误解,人类脑中是否存在镜像神经元及其功能依然是当前学术界的争议焦点。迄今仍然缺乏令人信服的证据表明镜像神经元(或系统)就是动作理解、动作模仿、共情以及读心的直接神经机制。因此,将镜像神经元视为"认知科学的圣杯"的主张是一种落后的模块论意识形态,只能催生新的"神经神话"。     

A functional role for the motor system in language understanding: evidence from theta-burst transcranial magnetic stimulation

Does language comprehension depend, in part, on neural systems for action? In previous studies, motor areas of the brain were activated when people read or listened to action verbs, but it remains unclear whether such activation is functionally relevant for comprehension. In the experiments reported here, we used off-line theta-burst transcranial magnetic stimulation to investigate whether a causal relationship exists between activity in premotor cortex and action-language understanding. Right-handed participants completed a lexical decision task, in which they read verbs describing manual actions typically performed with the dominant hand (e.g., "to throw," "to write") and verbs describing nonmanual actions (e.g., "to earn," "to wander"). Responses to manual-action verbs (but not to nonmanual-action verbs) were faster after stimulation of the hand area in left premotor cortex than after stimulation of the hand area in right premotor cortex. These results suggest that premotor cortex has a functional role in action-language understanding.     

Mirror neurons in humans: consisting or confounding evidence?

The widely known discovery of mirror neurons in macaques shows that premotor and parietal cortical areas are not only involved in executing one's own movement, but are also active when observing the action of others. The goal of this essay is to critically evaluate the substance of functional magnetic resonance imaging (fMRI) and positron emission tomography (PET) studies whose aim has been to reveal the presence of a parallel system in humans. An inspection of this literature suggests that there is relatively weak evidence for the existence of a circuit with 'mirror' properties in humans, such as that described in monkeys.     

Action observation network in childhood: a comparative fMRI study with adults

Very little is known about the action observation network and the mirror neuron system (AON/MNS) in children and its age‐related properties compared with those observed in adults. In the present fMRI study we explored the activation of areas belonging to the AON/MNS in children and adults during observation of complex hand‐grasping actions, as compared to observation of simple grasping acts executed with the left and the right hand, seen from a first person perspective. The results indicate that during the action observation tasks in children there was activation of a cortical network similar to that found in adults, including the premotor cortex, the posterior part of the inferior frontal gyrus and the posterior parietal lobe. However, the activation in children was more widespread and showed a higher inter‐subject variability compared with adults. Furthermore, the activated network seems more lateralized to the left hemisphere in adults and more bilateral in children, with a linear growth of lateralization index as a function of age. Finally, in children the activation in the anterior intraparietal cortex (AIP) of each hemisphere was higher during observation of the contralateral hand (hand identity effect) and during the observation of complex actions relative to simple grasping acts, confirming the role of AIP for action‐related hand identity previously described in adults. These results support the assumption that structure and size of action representations are sensitive to mechanisms of development and show physiological plasticity. These properties of the AON/MNS could constitute a powerful tool for spontaneous reorganization and recovery of motor deficits after brain injury in children and in adults, as well as for specific rehabilitation programmes.     

重解动作理解的“戈尔迪之结”:镜像神经元祛魅

"动作理解"一直被视为镜像神经元功能最为保守的假设,同时也是证据链最为强健的领域之一,但其概念内涵却始终如同古希腊神话中的"戈尔迪之结"一般没有得到厘清。目前,动作理解的紧缩解释正在面临严峻的挑战。来自实验室检验与哲学拷问的证据倾向于认为,镜像神经元活动构成动作理解的观点是一种"循环论证",前者至多只能算作产生动作理解的附带原因,而不是必要与充分原因。将广义的动作分成运动、运动动作与运动动作链可以有效地澄清实现理解不同层次的动作需要具备哪些条件。回应质疑并为辩护自身立场指明前进方向,是重解动作理解"戈尔迪之结"的起点,将对镜像神经元的科学祛魅产生奠基性的影响。     

示能性:基于镜像神经元视角的理解

示能性(affordance)概念解释了人的行为与物体功能之间互动、互补的关系。但是,有关示能性生理基础却很少被提及。镜像神经元的发现为示能性生理基础提供了可能的解释。文章根据研究将示能性分为结构示能性和功能示能性,探讨了不同示能性和镜像神经元之间的关系,并提出不同神经通路中的镜像神经元是示能性生理基础的结论。背-背侧分流中的镜像神经元是结构示能性的神经基础,而腹-背侧分流中的镜像神经元是功能示能性的神经基础。     

The Two-Level Theory of verb meaning: An approach to integrating the semantics of action with the mirror neuron system

Verbs have two separate levels of meaning. One level reflects the uniqueness of every verb and is called the "root". The other level consists of a more austere representation that is shared by all the verbs in a given class and is called the "event structure template". We explore the following hypotheses about how, with specific reference to the motor features of action verbs, these two distinct levels of semantic representation might correspond to two distinct levels of the mirror neuron system. Hypothesis 1: Root-level motor features of verb meaning are partially subserved by somatotopically mapped mirror neurons in the left primary motor and/or premotor cortices. Hypothesis 2: Template-level motor features of verb meaning are partially subserved by representationally more schematic mirror neurons in Brodmann area 44 of the left inferior frontal gyrus. Evidence has been accumulating in support of the general neuroanatomical claims made by these two hypotheses-namely, that each level of verb meaning is associated with the designated cortical areas. However, as yet no studies have satisfied all the criteria necessary to support the more specific neurobiological claims made by the two hypotheses-namely, that each level of verb meaning is associated with mirror neurons in the pertinent brain regions. This would require demonstrating that within those regions the same neuronal populations are engaged during (a) the linguistic processing of particular motor features of verb meaning, (b) the execution of actions with the corresponding motor features, and (c) the observation of actions with the corresponding motor features.     

Automatic imitation of intransitive actions

Previous research has indicated a potential discontinuity between monkey and human ventral premotor-parietal mirror systems, namely that monkey mirror systems process only transitive (object-directed) actions, whereas human mirror systems may also process intransitive (non-object-directed) actions. The present study investigated this discontinuity by seeking evidence of automatic imitation of intransitive actions--hand opening and closing--in humans using a simple reaction time (RT), stimulus-response compatibility paradigm. Left-right and up-down spatial compatibility were controlled by ensuring that stimuli were presented and responses executed in orthogonal planes, and automatic imitation was isolated from simple and complex orthogonal spatial compatibility by varying the anatomical identity of the stimulus hand and response hemispace, respectively. In all conditions, action compatible responding was faster than action incompatible responding, and no effects of spatial compatibility were observed. This experiment therefore provides evidence of automatic imitation of intransitive actions, and support for the hypothesis that human and monkey mirror systems differ with respect to the processing of intransitive actions.     

Within- and between-nervous-system inhibition of return: Observation is as good as performance

Inhibition of return (IOR) has been shown to occur when an individual returns to a target location (within-person IOR) and when an individual moves to a location just engaged by another individual (between-person IOR). Although within- and between-person IOR likely result from the same inhibitory mechanisms, different processes must activate these mechanisms following the performance and observation of action. Consistent with the suggestion that the mirror neuron system may be responsible for activating the inhibitory mechanisms behind IOR on observation trials, between-person IOR was only detected under restricted viewing conditions known to activate mirror neurons. These results indicate that mirror neuron system may be involved in both higher-order and automatic cognitive behavior.     

Social perception from visual cues: role of the STS region

Social perception refers to initial stages in the processing of information that culminates in the accurate analysis of the dispositions and intentions of other individuals. Single-cell recordings in monkeys, and neurophysiological and neuroimaging studies in humans, reveal that cerebral cortex in and near the superior temporal sulcus (STS) region is an important component of this perceptual system. In monkeys and humans, the STS region is activated by movements of the eyes, mouth, hands and body, suggesting that it is involved in analysis of biological motion. However, it is also activated by static images of the face and body, suggesting that it is sensitive to implied motion and more generally to stimuli that signal the actions of another individual. Subsequent analysis of socially relevant stimuli is carried out in the amygdala and orbitofrontal cortex, which supports a three-structure model proposed by Brothers. The homology of human and monkey areas involved in social perception, and the functional interrelationships between the STS region and the ventral face area, are unresolved issues.     

Responses of the human motor system to observing actions across species: A transcranial magnetic stimulation study

Ample evidence suggests that the role of the mirror neuron system (MNS) in monkeys is to represent the meaning of actions. The MNS becomes active in monkeys during execution, observation, and auditory experience of meaningful, object-oriented actions, suggesting that these cells represent the same action based on a variety of cues. The present study sought to determine whether the human motor system, part of the putative human MNS, similarly represents and reflects the meaning of actions rather than simply the mechanics of the actions. To this end, transcranial magnetic stimulation (TMS) of primary motor cortex was used to generate motor-evoked potentials (MEPs) from muscles involved in grasping while participants viewed object-oriented grasping actions performed by either a human, an elephant, a rat, or a body-less robotic arm. The analysis of MEP amplitudes suggested that activity in primary motor cortex during action observation was greatest during observation of the grasping actions of the rat and elephant, and smallest for the human and robotic arm. Based on these data, we conclude that the human action observation system can represent actions executed by non-human animals and shows sensitivity to species-specific differences in action mechanics.     

Motor functions of the Broca's region

Broca's region in the dominant cerebral hemisphere is known to mediate the production of language but also contributes to comprehension. This region evolved only in humans and is constituted of Brodmann's areas 44 and 45 in the inferior frontal gyrus. There is, however, evidence that Broca's region overlaps, at least in part, with the ventral premotor cortex. We summarize the evidence that the motor related part of Broca's area is localized in the opercular portion of the inferior frontal cortex, mainly in area 44 of Brodmann. According to our own data, there seems to be a homology between Brodmann area 44 in humans and the monkey area F5. The non-language related motor functions of Broca's region comprise complex hand movements, associative sensorimotor learning and sensorimotor integration. Brodmann's area 44 is also a part of a specialized parieto-premotor network and interacts significantly with the neighboring premotor areas.     

Mirror neurons and the phenomenology of intersubjectivity

The neurological discovery of mirror neurons is of eminent importance for the phenomenological theory of intersubjectivity. G. Rizzolatti and V. Gallese found in experiments with primates that a set of neurons in the premotor cortex represents the visually registered movements of another animal. The activity of these mirror neurons presents exactly the same pattern of activity as appears in the movement of one's own body. These findings may be extended to other cognitive and emotive functions in humans. I show how these neurological findings might be “translated” phenomenologically into our own experienced sensations, feelings and volitions.     

镜像神经元的发现及其对身心二元论的超越

镜像神经元是意大利帕尔玛大学Rizzolatti等人在恒河猴大脑腹侧运动前皮层F5区发现的一种神经元。这种神经元在猴子操作和观察同一个指向某种目标的动作时(如伸手抓食物)皆被激活,似乎这种神经元映射了其它个体的动作,因此被命名为“镜像神经元”。镜像神经元通过具身的模拟把动作的执行和动作的知觉结合在一起,把观察过程与身体运动过程相融合,克服了二元论在身心之间所设置的障碍,为人们正确认识身心关系开辟了新的视角。