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.     

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.     

The mirror neuron system and action recognition

Mirror neurons, first described in the rostral part of monkey ventral premotor cortex (area F5), discharge both when the animal performs a goal-directed hand action and when it observes another individual performing the same or a similar action. More recently, in the same area mirror neurons responding to the observation of mouth actions have been also found. In humans, through an fMRI study, it has been shown that the observation of actions performed with the hand, the mouth and the foot leads to the activation of different sectors of Broca's area and premotor cortex, according to the effector involved in the observed action, following a somatotopic pattern which resembles the classical motor cortex homunculus. These results strongly support the existence of an execution-observation matching system (mirror neuron system). It has been proposed that this system is involved in action recognition. Experimental evidence in favor of this hypothesis both in the monkey and humans are shortly reviewed.     

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”。     

镜像等效或守恒及其打破：从行为到认知神经机制的研究证据

镜像等效或守恒是动物与人类个体对两侧对称自然物体的一种进化自适应加工。但是, 这种知觉特性会妨碍包含镜像字符的文字阅读学习。阅读者有必要学会利用镜像泛化抑制的“去学习”机制, 打破镜像等效或守恒, 以获得识别镜像字符的能力。这一过程中, 左侧梭状回皮层通过与早期视觉皮层、顶叶皮层和口语脑网络的交互作用, 逐渐发展出一个可以识别镜像字符的视觉词形区(visual word form area, VWFA)。今后的研究需要关注两半球及其连合纤维在镜像等效或守恒加工中的作用、镜像泛化与抑制的详尽加工机制及其对镜像书写的影响、正常汉语儿童的汉字镜像泛化加工等问题。     

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"。     

Multimodal action representation in human left ventral premotor cortex

We used functional magnetic resonance imaging (fMRI) to investigate the neural systems responding to the sight and to the sound of an action. Subjects saw a video of paper tearing in silence (V), heard the sound of paper tearing (A), and saw and heard the action simultaneously (A + V). Compared to a non-action control stimulus, we found that hearing action sounds (A) activated the anterior inferior frontal gyrus and middle frontal gyrus in addition to primary auditory cortex. The anterior inferior frontal gyrus, which is known to be activated by environmental sounds, also seems to be involved in recognizing actions by sound. Consistent with previous research, seeing an action video (V) compared with seeing a non-action video activated the premotor cortex, intraparietal cortex, and the pars opercularis of the inferior frontal gyrus. An A + V facilitation effect was found in the ventral premotor cortex on the border of areas 44, 6, 3a, and 3b for the action stimuli but not for the control stimuli. This region may be involved in integrating multimodal information about actions. These data provide evidence that the ventral premotor cortex may provide an action representation that abstracts across both agency (self and other) and sensory modality (hearing and seeing). This function may be an important precursor of language functions.     

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.     

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.     

Beyond sensorimotor segregation: On mirror neurons and social affordance space tracking

Mirror neuron research has come a long way since the early 1990s, and many theorists are now stressing the heterogeneity and complexity of the sensorimotor properties of fronto-parietal circuits. However, core aspects of the initial ‘mirror mechanism’ theory, i.e. the idea of a symmetric encapsulated mirroring function translating sensory action perceptions into motor formats, still appears to be shaping much of the debate. This article challenges the empirical plausibility of the sensorimotor segregation implicit in the original mirror metaphor. It is proposed instead that the teleological organization found in the broader fronto-parietal circuits might be inherently sensorimotor. Thus the idea of an independent ‘purely perceptual’ goal understanding process is questioned. Further, it is hypothesized that the often asymmetric, heterogeneous and contextually modulated mirror and canonical neurons support a function of multisensory mapping and tracking of the perceiving agents affordance space. Such a shift in the interpretative framework offers a different theoretical handle on how sensorimotor processes might ground various aspects of intentional action choice and social cognition. Mirror neurons would under the proposed “social affordance model” be seen as dynamic parts of larger circuits, which support tracking of currently shared and competing action possibilities. These circuits support action selection processes—but also our understanding of the options and action potentials that we and perhaps others have in the affordance space. In terms of social cognition ‘mirror’ circuits might thus help us understand not only the intentional actions others are actually performing—but also what they could have done, did not do and might do shortly.     

Making sense of mirror neurons

The discovery of mirror neurons has been hailed as one of the most exciting developments in neuroscience in the past few decades. These neurons discharge in response to the observation of others’ actions. But how are we to understand the function of these neurons? In this paper I defend the idea that mirror neurons are best conceived as components of a sensory system that has the function to perceive action. In short, mirror neurons are part of a hitherto unrecognized “sixth sense”. In this spirit, research should move toward developing a psychophysics of mirror neurons.     

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.     

Programmed to learn? The ontogeny of mirror neurons

Mirror neurons are increasingly recognized as a crucial substrate for many developmental processes, including imitation and social learning. Although there has been considerable progress in describing their function and localization in the primate and adult human brain, we still know little about their ontogeny. The idea that mirror neurons result from Hebbian learning while the child observes/hears his/her own actions has received remarkable empirical support in recent years. Here we add a new element to this proposal, by suggesting that the infant's perceptual‐motor system is optimized to provide the brain with the correct input for Hebbian learning, thus facilitating the association between the perception of actions and their corresponding motor programs. We review evidence that infants (1) have a marked visual preference for hands, (2) show cyclic movement patterns with a frequency that could be in the optimal range for enhanced Hebbian learning, and (3) show synchronized theta EEG (also known to favour synaptic Hebbian learning) in mirror cortical areas during self‐observation of grasping. These conditions, taken together, would allow mirror neurons for manual actions to develop quickly and reliably through experiential canalization. Our hypothesis provides a plausible pathway for the emergence of mirror neurons that integrates learning with genetic pre‐programming, suggesting new avenues for research on the link between synaptic processes and behaviour in ontogeny.     

Mirror neurons: their implications for group psychotherapy

Recently discovered mirror neurons in the motor cortex of the brain register the actions and intentions of both the organism and others in the environment. As such, they may play a significant role in social behavior and groups. This paper considers the potential implications of mirror neurons and related neural networks for group therapists, proposing that mirror neurons and mirror systems provide "hard-wired" support for the group therapist's belief in the centrality of relationships in the treatment process and exploring their value in accounting for group-as-a-whole phenomena. Mirror neurons further confirm the holistic, social nature of perception, action, and intention as distinct from a stimulus-response behaviorism. The implications of mirror neurons and mirroring processes for the group therapist role, interventions, and training are also discussed.     

Intentional and Skillful Neurons

Abstract

In the mid-1990s, there was a major neuroscientific discovery which might drastically alter sport science in general and philosophy of sport in particular. The discovery of mirror neurons by Giacomo Rizzolatti and colleagues in Parma, Italy, is a substantial contribution to understanding brains, movements, and humans. Famous neuroscientist V. S. Ramachandran believes the discovery of mirror neurons ‘will do for psychology what DNA did for biology’ (http://www.edge.org/3rd_culture/ramachandran/ramachandran_p1.html). Somehow mirror neurons have not received the deserved attention in the philosophy of sport, but perhaps now is the time to reflect on some implications and consequences. The discovery of mirror neurons may increase our insights about our ability to learn, understand, intend, and produce skillful motor actions. In this article I will first examine what mirror neurons are and how they function in monkeys and humans. Second, I will review some objections to the so-called mirror neuron theory of action understanding, and try to reconcile some of these objections. Third, I will inquire into some implications for philosophy, which I believe are also fundamental to several topics in the philosophy of sport. I will then try to relate some of the most interesting aspects of mirror neurons to recent debates in the philosophy of sport. Finally, I will speculate on what further neuroscientific research might teach us about the nature of being a moving subject.     

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。     

Fronto-parietal mirror neuron system modeling: Visuospatial transformations support imitation learning independently of imitator perspective

Although the human mirror neuron system (MNS) is critical for action observation and imitation, most MNS investigations overlook the visuospatial transformation processes that allow individuals to interpret and imitate actions observed from differing perspectives. This problem is not trivial since accurately reaching for and grasping an object requires a visuospatial transformation mechanism capable of precisely remapping fine motor skills where the observer’s and imitator’s arms and hands may have quite different orientations and sizes. Accordingly, here we describe a novel neural model to investigate the dynamics between the fronto-parietal MNS and visuospatial processes during observation and imitation of a reaching and grasping action. Our model encompasses i) the inferior frontal gyrus (IFG) and inferior parietal lobule (IPL), regions that are postulated to produce neural drive and sensory predictions, respectively; ii) the middle temporal (MT) and middle superior temporal (MST) regions that are postulated to process visual motion of a particular action; and iii) the superior parietal lobule (SPL) and intra-parietal sulcus (IPS) that are hypothesized to encode the visuospatial transformations enabling action observation/imitation based on different visuospatial viewpoints. The results reveal that when a demonstrator executes an action, an imitator can reproduce it with similar kinematics, independently of differences in anthropometry, distance, and viewpoint. As with prior empirical findings, similar model synaptic activity was observed during both action observation and execution along with the existence of both view-independent and view-dependent neural populations in the frontal MNS. Importantly, this work generates testable behavioral and neurophysiological predictions. Namely, the model predicts that i) during observation/imitation the response time increases linearly as the rotation angle of the observed action increases but remain similar when performing both clockwise and counterclockwise rotation and ii) IPL embeds essentially view-independent neurons while SPL/IPS includes both view-independent and view-dependent neurons. Overall, this work suggests that MT/MST visuomotion processes combined with the SPL/IPS allow the MNS to observe and imitate actions independently of demonstrator-imitator spatial relationships.     

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.     

Implicit biases in visually guided action

For almost half a century dual-stream advocates have vigorously defended the view that there are two functionally specialized cortical streams of visual processing originating in the primary visual cortex: a ventral, perception-related ‘conscious’ stream and a dorsal, action-related ‘unconscious’ stream. They furthermore maintain that the perceptual and memory systems in the ventral stream are relatively shielded from the action system in the dorsal stream. In recent years, this view has come under scrutiny. Evidence points to two overlapping action pathways: a dorso-dorsal pathway that calculates features of the object to be acted on, and a ventro-dorsal pathway that transmits stored information about skilled object use from the ventral stream to the dorso-dorsal pathway. This evidence suggests that stored information may exert significantly more influence on visually guided action than hitherto assumed. I argue that this, in turn, supports the notion of skilled automatic action that is nonetheless agential. My focus here will be on actions influenced by implicit biases (stereotypes/prejudices). Action that is biased in this way, I argue, is in an important sense intentional and agential.

     

Predictive coding: an account of the mirror neuron system

Is it possible to understand the intentions of other people by simply observing their actions? Many believe that this ability is made possible by the brain’s mirror neuron system through its direct link between action and observation. However, precisely how intentions can be inferred through action observation has provoked much debate. Here we suggest that the function of the mirror system can be understood within a predictive coding framework that appeals to the statistical approach known as empirical Bayes. Within this scheme the most likely cause of an observed action can be inferred by minimizing the prediction error at all levels of the cortical hierarchy that are engaged during action observation. This account identifies a precise role for the mirror system in our ability to infer intentions from actions and provides the outline of the underlying computational mechanisms.