Corticospinal mirror neurons

Here, we report the properties of neurons with mirror-like characteristics that were identified as pyramidal tract neurons (PTNs) and recorded in the ventral premotor cortex (area F5) and primary motor cortex (M1) of three macaque monkeys. We analysed the neurons’ discharge while the monkeys performed active grasp of either food or an object, and also while they observed an experimenter carrying out a similar range of grasps. A considerable proportion of tested PTNs showed clear mirror-like properties (52% F5 and 58% M1). Some PTNs exhibited ‘classical’ mirror neuron properties, increasing activity for both execution and observation, while others decreased their discharge during observation (‘suppression mirror-neurons’). These experiments not only demonstrate the existence of PTNs as mirror neurons in M1, but also reveal some interesting differences between M1 and F5 mirror PTNs. Although observation-related changes in the discharge of PTNs must reach the spinal cord and will include some direct projections to motoneurons supplying grasping muscles, there was no EMG activity in these muscles during action observation. We suggest that the mirror neuron system is involved in the withholding of unwanted movement during action observation. Mirror neurons are differentially recruited in the behaviour that switches rapidly between making your own movements and observing those of others.     

Hebbian learning and predictive mirror neurons for actions,sensations and emotions

Spike-timing-dependent plasticity is considered the neurophysiological basis of Hebbian learning and has been shown to be sensitive to both contingency and contiguity between pre- and postsynaptic activity. Here, we will examine how applying this Hebbian learning rule to a system of interconnected neurons in the presence of direct or indirect re-afference (e.g. seeing/hearing one''s own actions) predicts the emergence of mirror neurons with predictive properties. In this framework, we analyse how mirror neurons become a dynamic system that performs active inferences about the actions of others and allows joint actions despite sensorimotor delays. We explore how this system performs a projection of the self onto others, with egocentric biases to contribute to mind-reading. Finally, we argue that Hebbian learning predicts mirror-like neurons for sensations and emotions and review evidence for the presence of such vicarious activations outside the motor system.     

Sensorimotor learning configures the human mirror system

Cells in the "mirror system" fire not only when an individual performs an action but also when one observes the same action performed by another agent [1-4]. The mirror system, found in premotor and parietal cortices of human and monkey brains, is thought to provide the foundation for social understanding and to enable the development of theory of mind and language [5-9]. However, it is unclear how mirror neurons acquire their mirror properties -- how they derive the information necessary to match observed with executed actions [10]. We address this by showing that it is possible to manipulate the selectivity of the human mirror system, and thereby make it operate as a countermirror system, by giving participants training to perform one action while observing another. Before this training, participants showed event-related muscle-specific responses to transcranial magnetic stimulation over motor cortex during observation of little- and index-finger movements [11-13]. After training, this normal mirror effect was reversed. These results indicate that the mirror properties of the mirror system are neither wholly innate [14] nor fixed once acquired; instead they develop through sensorimotor learning [15, 16]. Our findings indicate that the human mirror system is, to some extent, both a product and a process of social interaction.     

The mirror mechanism: recent findings and perspectives

Mirror neurons are a specific type of visuomotor neuron that discharge both when a monkey executes a motor act and when it observes a similar motor act performed by another individual. In this article, we review first the basic properties of these neurons. We then describe visual features recently investigated which indicate that, besides encoding the goal of motor acts, mirror neurons are modulated by location in space of the observed motor acts, by the perspective from which the others’ motor acts are seen, and by the value associated with the object on which others’ motor acts are performed. In the last part of this article, we discuss the role of the mirror mechanism in planning actions and in understanding the intention underlying the others’ motor acts. We also review some human studies suggesting that motor intention in humans may rely, as in the monkey, on the mirror mechanism.     

灵长类镜像神经元系统起源及其争议研究进展

在灵长类镜像神经元系统的研究中,关于镜像神经元系统的产生主要存在两种观点,基因假说认为镜像神经元系统的出现基于一定的演化压力,服务于动作理解这一社会性功能;而联想学习假说则认为镜像神经元系统是感觉运动学习的产物,并不服务于动作理解。在联想学习的阵营中,联想序列学习主张一种极端的后天论立场,并通过刺激-反应范式提供大量的实证证据。但是,联想序列学习虽然能够解释大部分镜像神经元的研究,却无法否定其发生机制中的基因成分。比较镜像神经元系统在多个物种中的演化历史,探索个体早期发展对社会性信息的偏好均显示出联想序列学习存在局限,而联想序列学习提供的证据也不具有生态学效度。因此,对镜像神经元的基因基础如何影响其产生、发展与演化的探讨仍将是一个极具意义和生命力的主题。     

Auditory–vocal mirroring in songbirds

Mirror neurons are theorized to serve as a neural substrate for spoken language in humans, but the existence and functions of auditory–vocal mirror neurons in the human brain remain largely matters of speculation. Songbirds resemble humans in their capacity for vocal learning and depend on their learned songs to facilitate courtship and individual recognition. Recent neurophysiological studies have detected putative auditory–vocal mirror neurons in a sensorimotor region of the songbird''s brain that plays an important role in expressive and receptive aspects of vocal communication. This review discusses the auditory and motor-related properties of these cells, considers their potential role on song learning and communication in relation to classical studies of birdsong, and points to the circuit and developmental mechanisms that may give rise to auditory–vocal mirroring in the songbird''s brain.     

Mirror neurons in the tree of life: mosaic evolution,plasticity and exaptation of sensorimotor matching responses

Considering the properties of mirror neurons (MNs) in terms of development and phylogeny, we offer a novel, unifying, and testable account of their evolution according to the available data and try to unify apparently discordant research, including the plasticity of MNs during development, their adaptive value and their phylogenetic relationships and continuity. We hypothesize that the MN system reflects a set of interrelated traits, each with an independent natural history due to unique selective pressures, and propose that there are at least three evolutionarily significant trends that gave raise to three subtypes: hand visuomotor, mouth visuomotor, and audio–vocal. Specifically, we put forward a mosaic evolution hypothesis, which posits that different types of MNs may have evolved at different rates within and among species. This evolutionary hypothesis represents an alternative to both adaptationist and associative models. Finally, the review offers a strong heuristic potential in predicting the circumstances under which specific variations and properties of MNs are expected. Such predictive value is critical to test new hypotheses about MN activity and its plastic changes, depending on the species, the neuroanatomical substrates, and the ecological niche.     

Frequency and topography in monkey electroencephalogram during action observation: possible neural correlates of the mirror neuron system

The observation of actions executed by others results in desynchronization of electroencephalogram (EEG) in the alpha and beta frequency bands recorded from the central regions in humans. On the other hand, mirror neurons, which are thought to be responsible for this effect, have been studied only in macaque monkeys, using single-cell recordings. Here, as a first step in a research programme aimed at understanding the parallels between human and monkey mirror neuron systems (MNS), we recorded EEG from the scalp of two monkeys during action observation. The monkeys were trained to fixate on the face of a human agent and subsequently to fixate on a target upon which the agent performed a grasping action. We found that action observation produced desynchronization in the 19–25 Hz band that was strongest over anterior and central electrodes. These results are in line with human data showing that specific frequency bands within the power spectrum of the ongoing EEG may be modulated by observation of actions and therefore might be a specific marker of MNS activity.     

Dissociating object directed and non-object directed action in the human mirror system; implications for theories of motor simulation

Mirror neurons are single cells found in macaque premotor and parietal cortices that are active during action execution and observation. In non-human primates, mirror neurons have only been found in relation to object-directed movements or communicative gestures, as non-object directed actions of the upper limb are not well characterized in non-human primates. Mirror neurons provide important evidence for motor simulation theories of cognition, sometimes referred to as the direct matching hypothesis, which propose that observed actions are mapped onto associated motor schemata in a direct and automatic manner. This study, for the first time, directly compares mirror responses, defined as the overlap between action execution and observation, during object directed and meaningless non-object directed actions. We present functional MRI data that demonstrate a clear dissociation between object directed and non-object directed actions within the human mirror system. A premotor and parietal network was preferentially active during object directed actions, whether observed or executed. Moreover, we report spatially correlated activity across multiple voxels for observation and execution of an object directed action. In contrast to predictions made by motor simulation theory, no similar activity was observed for non-object directed actions. These data demonstrate that object directed and meaningless non-object directed actions are subserved by different neuronal networks and that the human mirror response is significantly greater for object directed actions. These data have important implications for understanding the human mirror system and for simulation theories of motor cognition. Subsequent theories of motor simulation must account for these differences, possibly by acknowledging the role of experience in modulating the mirror response.     

fMRI adaptation reveals mirror neurons in human inferior parietal cortex

Mirror neurons, as originally described in the macaque, have two defining properties [1, 2]: They respond specifically to a particular action (e.g., bringing an object to the mouth), and they produce their action-specific responses independent of whether the monkey executes the action or passively observes a conspecific performing the same action. In humans, action observation and action execution engage a network of frontal, parietal, and temporal areas. However, it is unclear whether these responses reflect the activity of a single population that represents both observed and executed actions in a common neural code or the activity of distinct but overlapping populations of exclusively perceptual and motor neurons [3]. Here, we used fMRI adaptation to show that the right inferior parietal lobe (IPL) responds independently to specific actions regardless of whether they are observed or executed. Specifically, responses in the right IPL were attenuated when participants observed a recently executed action relative to one that had not previously been performed. This adaptation across action and perception demonstrates that the right IPL responds selectively to the motoric and perceptual representations of actions and is the first evidence for a neural response in humans that shows both defining properties of mirror neurons.     

Learning to understand others' actions

Despite nearly two decades of research on mirror neurons, there is still much debate about what they do. The most enduring hypothesis is that they enable 'action understanding'. However, recent critical reviews have failed to find compelling evidence in favour of this view. Instead, these authors argue that mirror neurons are produced by associative learning and therefore that they cannot contribute to action understanding. The present opinion piece suggests that this argument is flawed. We argue that mirror neurons may both develop through associative learning and contribute to inferences about the actions of others.     

Effect of a vasopressin analog on the chemoreactive properties of sensorimotor cortex neurons

Subcutaneous injection of 10 micrograms desglycilargininvasopressin (DG-AVP) does not alter the mean frequency of background unit activity of sensorimotor cortical neurons. However, the pattern of impulse activity is essentially changed. At the same time the reactions of sensorimotor cortical neurons to microiontophoretic administration of acetylcholine and noradrenaline experience definite changes. It is suggested that the DG-AVP-induced changes in chemoreactive properties of neurons underlie the effect of this peptide on the learning and memory.     

View-based encoding of actions in mirror neurons of area f5 in macaque premotor cortex

Converging experimental evidence indicates that mirror neurons in the monkey premotor area F5 encode the goals of observed motor acts [1-3]. However, it is unknown whether they also contribute to encoding the perspective from which the motor acts of others are seen. In order to address this issue, we recorded the visual responses of mirror neurons of monkey area F5 by using a novel experimental paradigm based on the presentation of movies showing grasping motor acts from different visual perspectives. We found that the majority of the tested mirror neurons?(74%) exhibited view-dependent activity with responses tuned to specific points of view. A minority of the tested mirror neurons (26%) exhibited view-independent responses. We conclude that view-independent mirror neurons encode action goals irrespective of the details of the observed motor acts, whereas the view-dependent ones might either form an intermediate step in the formation of view independence or contribute to a modulation of view-dependent representations in higher-level visual areas, potentially linking the goals of observed motor acts with their pictorial aspects.     

Mark tests for mirror self-recognition in capuchin monkeys (Cebus apella) trained to touch marks

In Experiment 1, three capuchin monkeys (Cebus apella) were exposed to a mirror in their home cage for 3 days and then given food treats for touching orange marks located on the surface of an experimental chamber. Following training, a mirror was added to the chamber to see if the monkeys would use it to guide non-reinforced contacts with an orange mark on their foreheads that was only visible as a mirror reflection (mark test). Two monkeys touched the head-mark more often with the mirror present than absent, but no mark touches were emitted while looking at the mirror. In Experiment 2, the monkeys were rewarded for touching orange marks on their bodies that were directly visible, followed by another head-mark test. Again, two monkeys touched the mark more often with the mirror present than absent, but these contacts were not emitted while looking at the mirror. Since facing the mirror while mark touching was not required for reinforcement during training, Experiment 3 further tested the possibility that increased mark touching in the presence of the mirror during Experiments 1 and 2 was the result of a memorial process. For this, a final, novel mark test was conducted using an orange mark on the neck that was only visible as a reflection (Experiment 3). No monkeys passed this test. These are the first mark tests given to capuchin monkeys. The results are consistent with the finding that no monkey species is capable of spontaneous mirror self-recognition. The implications of sequential training and mark testing for comparative evaluations of mirror self-recognition capacity are discussed.     

Social neuroscience: mirror neurons recorded in humans

New single-cell recordings show that humans do have mirror neurons, and in more brain regions than previously suspected. Some action-execution neurons were seen to be inhibited during observation, possibly preventing imitation and helping self/other discrimination.     

Human cortex: reflections of mirror neurons

Claims to have identified mirror neurons in human cortex have been controversial. A recent study has applied an fMRI adaptation protocol to the problem and come up with novel evidence for the existence of movement-selective mirror neurons in human cortex.     

Tinbergen on mirror neurons

Fifty years ago, Niko Tinbergen defined the scope of behavioural biology with his four problems: causation, ontogeny, survival value and evolution. About 20 years ago, there was another highly significant development in behavioural biology—the discovery of mirror neurons (MNs). Here, I use Tinbergen''s original four problems (rather than the list that appears in textbooks) to highlight the differences between two prominent accounts of MNs, the genetic and associative accounts; to suggest that the latter provides the defeasible ‘best explanation’ for current data on the causation and ontogeny of MNs; and to argue that functional analysis, of the kind that Tinbergen identified somewhat misleadingly with studies of ‘survival value’, should be a high priority for future research. In this kind of functional analysis, system-level theories would assign MNs a small, but potentially important, role in the achievement of action understanding—or another social cognitive function—by a production line of interacting component processes. These theories would be tested by experimental intervention in human and non-human animal samples with carefully documented and controlled developmental histories.     

Sensorimotor experience enhances automatic imitation of robotic action

Recent research in cognitive neuroscience has found that observation of human actions activates the 'mirror system' and provokes automatic imitation to a greater extent than observation of non-biological movements. The present study investigated whether this human bias depends primarily on phylogenetic or ontogenetic factors by examining the effects of sensorimotor experience on automatic imitation of non-biological robotic, stimuli. Automatic imitation of human and robotic action stimuli was assessed before and after training. During these test sessions, participants were required to execute a pre-specified response (e.g. to open their hand) while observing a human or robotic hand making a compatible (opening) or incompatible (closing) movement. During training, participants executed opening and closing hand actions while observing compatible (group CT) or incompatible movements (group IT) of a robotic hand. Compatible, but not incompatible, training increased automatic imitation of robotic stimuli (speed of responding on compatible trials, compared with incompatible trials) and abolished the human bias observed at pre-test. These findings suggest that the development of the mirror system depends on sensorimotor experience, and that, in our species, it is biased in favour of human action stimuli because these are more abundant than non-biological action stimuli in typical developmental environments.     

Hub and switches: endocannabinoid signalling in midbrain dopamine neurons

The last decade has provided a wealth of experimental data on the role played by lipids belonging to the endocannabinoid family in several facets of physiopathology of dopamine neurons. We currently suggest that these molecules, being intimately connected with diverse metabolic and signalling pathways, might differently affect various functions of dopamine neurons through activation not only of surface receptors, but also of nuclear receptors. It is now emerging how dopamine neurons can regulate their constituent biomolecules to compensate for changes in either internal functions or external conditions. Consequently, dopamine neurons use these lipid molecules as metabolic and homeostatic signal detectors, which can dynamically impact cell function and fitness. Because dysfunctions of the dopamine system underlie diverse neuropsychiatric disorders, including schizophrenia and drug addiction, the importance of better understanding the correlation between an unbalanced endocannabinoid signal and the dopamine system is even greater. Particularly, because dopamine neurons are critical in controlling incentive-motivated behaviours, the involvement of endocannabinoid molecules in fine-tuning dopamine cell activity opened new avenues in both understanding and treating drug addiction. Here, we review recent advances that have shed new light on the understanding of differential roles of endocannabinoids and their cognate molecules in the regulation of the reward circuit, and discuss their anti-addicting properties, particularly with a focus on their potential engagement in the prevention of relapse.     

Extending the mirror neuron system model, II: what did I just do? A new role for mirror neurons

A mirror system is active both when an animal executes a class of actions (self-actions) and when it sees another execute an action of that class. Much attention has been given to the possible roles of mirror systems in responding to the actions of others but there has been little attention paid to their role in self-actions. In the companion article (Bonaiuto et al. Biol Cybern 96:9–38, 2007) we presented MNS2, an extension of the Mirror Neuron System model of the monkey mirror system trained to recognize the external appearance of its own actions as a basis for recognizing the actions of other animals when they perform similar actions. Here we further extend the study of the mirror system by introducing the novel hypotheses that a mirror system may additionally help in monitoring the success of a self-action and may also be activated by recognition of one’s own apparent actions as well as efference copy from one’s intended actions. The framework for this computational demonstration is a model of action sequencing, called augmented competitive queuing, in which action choice is based on the desirability of executable actions. We show how this “what did I just do?” function of mirror neurons can contribute to the learning of both executability and desirability which in certain cases supports rapid reorganization of motor programs in the face of disruptions.