Geoffrey Bird*, Jane Leighton, Clare Press and Cecilia Heyes (2007)
Department of Psychology UCL
Intact automatic imitation of human and robot actions in autism spectrum disorders
Proc. R. Soc. B, 274, 3027-3031
Abstract
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.
Keywords: imitation; autism; mirror neuron; mirror system; animacy
P3027 (Introduction)
Theories that address imitation fall into two categories: specialist and generalist theories (Brass & Heyes 2005). Specialist theories propose that imitation is mediated by a
special-purpose imitation module, whereas generalist theories suggest that it is mediated by task-general learning and motor control mechanisms. It has been known for some
time that children and adults with ASD perform poorly in a variety of imitation tasks (see Williams et al. (2004) for a review).However, it is not clear whether their weak imitative
performance is due to specific or non-specific factors. Abnormal performance in imitation tasks could be due to either impairment of the mechanisms that translate observed into executed actions (specific factors) or impairment of mechanisms that are recruited by both the imitative and the non-imitative tasks (non-specific factors).
Most of the imitation tasks used in the studies of ASD make substantial demands on non specific mechanisms because they assess intentional or ‘voluntary’ imitation. In tests of voluntary imitation, the experimenter asks the participant to copy an action that has many temporal and spatial features, and does not specify exactly which features of the action are to be reproduced. For example, Rogers et al. (2003) instructed participants simply to ‘do
this’. Determining the appropriate action dimensions for imitation, and therefore what constitutes successful performance, is accomplished through the interpretation
of subtle cues relating to the social context and the experimenter’s mental states. The ability to focus on the selected action dimensions, so that performance is not impaired by imitation of task-irrelevant action dimensions, relies on good executive function and attentional
control. Interpretation of social cues, theory of mind, executive functions and attentional control have all been shown to be impaired in autism (Russell 1997; Bird et al.
2006; Frith & Frith 2006). Therefore, they are all candidate non-specific mechanisms that could account for poor performance on voluntary imitation tasks.
Neurological evidence in support of the specific factors hypothesis has come from studies suggesting that ASD are characterized by dysfunction of the mirror system (e.g.
Dapretto et al. 2006; Williams et al. 2006). The mirror system, comprising bilateral inferior frontal gyrus and parietal cortex, active when actions are both executed and
observed, is maximally activated during imitation (Iacoboni et al. 1999). This characteristic makes it plausible that the mirror system translates observed into executed actions, and is consistent with evidence that lesions to the mirror system result in poor performance on
imitation tasks (Heilman et al. 1982). Therefore, reports of abnormal mirror system activity in individuals with ASD support the view that their difficulties in imitation tasks are due, at least in part, to specific factors.
However different studies have localized the mirror system deficit in ASD to different neurological areas.
P3028 (Discussion)
The present study assessed imitation in high-functioning adults with ASD using an automatic imitation procedure. We chose an automatic, rather than a voluntary, imitation
test in order to minimize the demands that it would make on non-specific mechanisms. In tests of automatic imitation, participants are not asked, and do not intend,
to imitate modelled movements. Instead, they are required merely to observe actions, either passively or with a simple movement task, while the experimenter measures involuntary
muscular responses (passive observation tasks) or involuntary differences in speed to execute prespecified actions (simple movement tasks). As far as we are aware, only one previous study has tried to investigate automatic imitation in ASD. McIntosh et al.
(2006) used electromyography (EMG) to measure muscular activity in the face while participants were presented with emotional facial expressions. Compared with controls, individuals with ASD showed less expression-compatible muscular activation. However,
this study did not distinguish automatic imitation from emotional contagion. It is not clear whether, in the controls, observation of a smiling face promoted smiling directly, or by inducing positive affect. The results are also difficult to interpret because face stimuli were presented, and there is a growing body of evidence that gaze patterns to faces are abnormal in autism (Klin et al. 2002). Specifically, individuals with ASD spend less time looking
at the eye region of the face, which has been shown to be crucial in emotion recognition (Spezio et al. 2007). To overcome these problems, we used affectively neutral hand movements in our automatic imitation task.
The present study assessed imitation in high-functioning adults with ASD using an automatic imitation procedure. We chose an automatic, rather than a voluntary, imitation test in order to minimize the demands that it would make on non-specific mechanisms. In tests of automatic
imitation, participants are not asked, and do not intend, to imitate modelled movements. Instead, they are required merely to observe actions, either passively or with a simple
movement task, while the experimenter measures involuntary muscular responses (passive observation tasks) or involuntary differences in speed to execute prespecified
actions (simple movement tasks). As far as we are aware, only one previous study has tried
to investigate automatic imitation in ASD. McIntosh et al. (2006) used electromyography (EMG) to measure muscular activity in the face while participants were presented with emotional facial expressions. Compared with controls, individuals with ASD showed less
expression-compatible muscular activation. However, this study did not distinguish automatic imitation from emotional contagion. It is not clear whether, in the controls, observation of a smiling face promoted smiling directly, or by inducing positive affect. The results are also
difficult to interpret because face stimuli were presented, and there is a growing body of evidence that gaze patterns to faces are abnormal in autism (Klin et al. 2002). Specifically, individuals with ASD spend less time looking at the eye region of the face, which has been shown to be crucial in emotion recognition (Spezio et al. 2007). To overcome these problems, we used affectively neutral hand movements in our automatic imitation task. imitation effect is greater when the observed action is performed by a human effector than when it is performed
by a human-like mechanical device, or ‘robot’ (Kilner et al. 2003; Press et al. 2005). It has been argued that the latter effect is a direct consequence of increased mirror system activity in response to observation of human, compared with robotic, action (Tai et al. 2004). Thus, this study sought to investigate automatic imitation and the animacy effect in both a group of high-functioning adults with ASD and typically developing matched controls.
For both open and close responses, response onset was measured by recording the electromyogram (EMG) from the first dorsal interosseous muscle
P3030
This study tested automatic imitation of affectively neutral hand actions in ASD. In comparison with matched, typically developing controls, the ASD group showed an
equivalent automatic imitation effect, and signs of an increased animacy bias, namely, a greater difference in automatic imitation of human and robot actions.
The principal finding of the present study was that individuals with ASD did not show an impairment of automatic imitation of affectively neutral hand actions. This finding contrasts with reports of an imitation impairment in this group (Williams et al. 2004), but it is
not wholly anomalous with respect to studies of imitation in ASD. Several studies have found imitative performance to be unimpaired (e.g. Carpenter et al. 2001; Hamilton
et al. 2007; see also Sebanz et al. 2005) and, as noted in §1, performance in tests of voluntary imitation is vulnerable to the effects of non-specific factors such as theory of mind
and executive function impairments. Therefore, whether or not a particular voluntary imitation task presents a challenge to individuals with ASD may depend upon the interaction between two factors: the extent to which the task requires non-specific abilities and the degree to which these abilities are impaired in the particular sample of individuals recruited for the study.
Brass et al. 2003). The authors of these studies argue that distinguishing the self from
others, which relies on the theory of mind system, is a crucial component of imitation inhibition. Theories of mind deficits are well documented in ASD (for a review
see Frith & Frith 2003). Therefore, this hypothesis suggests that the ASD group showed a greater compatibility effect because they had problems inhibiting imitation of human actions. Such a suggestion is consonant with two clinical features of autism which indicate problems with imitation inhibition: echolalia (involuntary imitation of the speech patterns of others)
and echopraxia (involuntary imitation of observed actions; Russell 1997).
