Clare Press

Mirror neurons: From origin to function

This article argues that mirror neurons originate in sensorimotor associative learning and therefore a new approach is needed to investigate their functions. Mirror neurons were discovered about 20 years ago in the monkey brain, and there is now evidence that they are also present in the human brain. The intriguing feature of many mirror neurons is that they fire not only when the animal is performing an action, such as grasping an object using a power grip, but also when the animal passively observes a similar action performed by another agent. It is widely believed that mirror neurons are a genetic adaptation for action understanding; that they were designed by evolution to fulfill a specific socio-cognitive function. In contrast, we argue that mirror neurons are forged by domain-general processes of associative learning in the course of individual development, and, although they may have psychological functions, they do not necessarily have a specific evolutionary purpose or adaptive function. The evidence supporting this view shows that (1) mirror neurons do not consistently encode action goals; (2) the contingency- and context-sensitive nature of associative learning explains the full range of mirror neuron properties; (3) human infants receive enough sensorimotor experience to support associative learning of mirror neurons (wealth of the stimulus); and (4) mirror neurons can be changed in radical ways by sensorimotor training. The associative account implies that reliable information about the function of mirror neurons can be obtained only by research based on developmental history, system-level theory, and careful experimentation.

Intact automatic imitation of human and robot actions in autism spectrum disorders

The existence of a specialized imitation module in humans is hotly debated. Studies suggesting a specific imitation impairment in individuals with autism spectrum disorders (ASD) support a modular view. However, the voluntary imitation tasks used in these studies (which require socio-cognitive abilities in addition to imitation for successful performance) cannot support claims of a specific impairment. Accordingly, an automatic imitation paradigm (a ‘cleaner’ measure of imitative ability) was used to assess the imitative ability of 16 adults with ASD and 16 non-autistic matched control participants. Participants performed a prespecified hand action in response to observed hand actions performed either by a human or a robotic hand. On compatible trials the stimulus and response actions matched, while on incompatible trials the two actions did not match. Replicating previous findings, the Control group showed an automatic imitation effect: responses on compatible trials were faster than those on incompatible trials. This effect was greater when responses were made to human than to robotic actions (‘animacy bias’). The ASD group also showed an automatic imitation effect and a larger animacy bias than the Control group. We discuss these findings with reference to the literature on imitation in ASD and theories of imitation.

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.

Visual enhancement of touch in spatial body representation.

Perception of our own bodies is based on integration of visual and tactile inputs, notably by neurons in the brains parietal lobes. Here we report a behavioural consequence of this integration process. Simply viewing the arm can speed up reactions to an invisible tactile stimulus on the arm. We observed this visual enhancement effect only when a tactile task required spatial computation within a topographic map of the body surface and the judgements made were close to the limits of performance. This effect of viewing the body surface was absent or reversed in tasks that either did not require a spatial computation or in which judgements were well above performance limits. We consider possible mechanisms by which vision may influence tactile processing.

The Roles of Feature-Specific Task Set and Bottom-Up Salience in Attentional Capture: An ERP Study.

We investigated the roles of top-down task set and bottom-up stimulus salience for feature-specific attentional capture. Spatially nonpredictive cues preceded search arrays that included a color-defined target. For target-color singleton cues, behavioral spatial cueing effects were accompanied by cue-induced N2pc components, indicative of attentional capture. These effects were only minimally attenuated for nonsingleton target-color cues, underlining the dominance of top-down task set over salience in attentional capture. Nontarget-color singleton cues triggered no N2pc, but instead an anterior N2 component indicative of top-down inhibition. In Experiment 2, inverted behavioral cueing effects of these cues were accompanied by a delayed N2pc to targets at cued locations, suggesting that perceptually salient but task-irrelevant visual events trigger location-specific inhibition mechanisms that can delay subsequent target selection.

Dynamic Modulation of Human Motor Activity When Observing Actions

Previous studies have demonstrated that when we observe somebody else executing an action many areas of our own motor systems are active. It has been argued that these motor activations are evidence that we motorically simulate observed actions; this motoric simulation may support various functions such as imitation and action understanding. However, whether motoric simulation is indeed the function of motor activations during action observation is controversial, due to inconsistency in findings. Previous studies have demonstrated dynamic modulations in motor activity when we execute actions. Therefore, if we do motorically simulate observed actions, our motor systems should also be modulated dynamically, and in a corresponding fashion, during action observation. Using magnetoencephalography, we recorded the cortical activity of human participants while they observed actions performed by another person. Here, we show that activity in the human motor system is indeed modulated dynamically during action observation. The finding that activity in the motor system is modulated dynamically when observing actions can explain why studies of action observation using functional magnetic resonance imaging have reported conflicting results, and is consistent with the hypothesis that we motorically simulate observed actions.

Action observation and robotic agents: Learning and anthropomorphism

The action observation network (AON), which is thought to translate observed actions into motor codes required for their execution, is biologically tuned: it responds more to observation of human, than non-human, movement. This biological specificity has been taken to support the hypothesis that the AON underlies various social functions, such as theory of mind and action understanding, and that, when it is active during observation of non-human agents like humanoid robots, it is a sign of ascription of human mental states to these agents. This review will outline evidence for biological tuning in the AON, examining the features which generate it, and concluding that there is evidence for tuning to both the form and kinematic profile of observed movements, and little evidence for tuning to belief about stimulus identity. It will propose that a likely reason for biological tuning is that human actions, relative to non-biological movements, have been observed more frequently while executing corresponding actions. If the associative hypothesis of the AON is correct, and the network indeed supports social functioning, sensorimotor experience with non-human agents may help us to predict, and therefore interpret, their movements.

Intact imitation of emotional facial actions in autism spectrum conditions.

It has been proposed that there is a core impairment in autism spectrum conditions (ASC) to the mirror neuron system (MNS): If observed actions cannot be mapped onto the motor commands required for performance, higher order sociocognitive functions that involve understanding another persons perspective, such as theory of mind, may be impaired. However, evidence of MNS impairment in ASC is mixed. The present study used an ‘automatic imitation’ paradigm to assess MNS functioning in adults with ASC and matched controls, when observing emotional facial actions. Participants performed a pre-specified angry or surprised facial action in response to observed angry or surprised facial actions, and the speed of their action was measured with motion tracking equipment. Both the ASC and control groups demonstrated automatic imitation of the facial actions, such that responding was faster when they acted with the same emotional expression that they had observed. There was no difference between the two groups in the magnitude of the effect. These findings suggest that previous apparent demonstrations of impairments to the MNS in ASC may be driven by a lack of visual attention to the stimuli or motor sequencing impairments, and therefore that there is, in fact, no MNS impairment in ASC. We discuss these findings with reference to the literature on MNS functioning and imitation in ASC, as well as theories of the role of the MNS in sociocognitive functioning in typical development.

The Role of Alexithymia in Reduced Eye-Fixation in Autism Spectrum Conditions

Eye-tracking studies have demonstrated mixed support for reduced eye fixation when looking at social scenes in individuals with Autism Spectrum Conditions (ASC). We present evidence that these mixed findings are due to a separate condition—alexithymia—that is frequently comorbid with ASC. We find that in adults with ASC, autism symptom severity correlated negatively with attention to faces when watching video clips. However, only the degree of alexithymia, and not autism symptom severity, predicted eye fixation. As well as potentially resolving the contradictory evidence in this area, these findings suggest that individuals with ASC and alexithymia may form a sub-group of individuals with ASC, with emotional impairments in addition to the social impairments characteristic of ASC.

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.