Reduced spontaneous facial mimicry in women with autistic traits
Introduction
Among the core characteristics of Autistic Spectrum Disorders (ASD) are pervasive deficits in socio-emotional competencies, such as empathy and perspective taking, which can become apparent already during the 1st years of life. There is much reason to believe that ASD are the extreme end of a broader spectrum of sub-syndromal autistic traits (see Baron-Cohen et al., 2001, Constantino and Todd, 2003). This conception implies a continuum of socio-emotional competency across the population. Little research, however, has directly investigated the relationship between autistic traits and markers of socio-emotional competency across the population.
One of the most influential models of ASD describes these socio-emotional abnormalities as resulting from a failure to acquire a “theory of mind” (ToM; Baron Cohen et al., 1985). ToM encompasses the attribution of mental states to other individuals as a necessary condition in order to develop an understanding of agency and intentionality. ToM has been studied abundantly in ASD (Hill and Frith, 2003), but despite its success in systematically describing of the core abnormalities of ASD, ToM dysfunction has remained somewhat unsatisfactory as an etiological account of ASD (Williams et al., 2001). Apart from the fact that not all core symptoms fit well into the ToM framework, developmental abnormalities are evident prior to the age at which normal children develop this ToM ability. Therefore, the focus of attention is shifting towards precursors of ToM deficits.
One recent hypothesis states that deficits in brain circuits that underlie perception–action coupling, or the automatic preparation of motor programs upon the perception of another individual performing that action, form the basis for impairments in mind-reading and empathy (Gallese and Goldman, 1998, Iacoboni and Dapretto, 2006, Oberman and Ramachandran, 2007, Williams et al., 2001). These notions were inspired by the discovery in macaque monkeys of mirror neurons, which respond similarly to perception and execution of the same action (di Pellegrino et al., 1992). Neuroimaging experiments in humans have revealed a network of areas, including the superior temporal sulcus, inferior frontal gyrus, and parietal lobule, that appear to subserve perception–action coupling in a similar way (Decety et al., 2002, Iacoboni et al., 1999, Iacoboni et al., 2001, Keysers and Perrett, 2004, Koski et al., 2002, Koski et al., 2003). These areas are often jointly referred to as action representation areas, and of these, the inferior frontal gyrus and the parietal lobule appear to form the center of the human mirror neuron system (MNS).
Of particular relevance for the understanding of empathy is the imitation of facial expressions. Such expressions constitute an external display of an individual's emotional state, and therefore, the ability to adopt the representation of such an action may provide a window into other people's emotional states (Gallese, 2003). In support of this notion, it is known that people tend to copy other people's facial expressions, an effect that occurs quickly (Dimberg and Thunberg, 1998), automatically (Dimberg et al., 2002), and even arises when facial expressions are not consciously registered (Dimberg et al., 2000). Underscoring the potential significance of this process for social understanding, recent investigations have shown that this facial mimicry effect is correlated with (self-reported) empathy (Sonnby-Borgström, 2002). Furthermore, in line with notions that women are more empathetic than men, gender differences have been found in facial mimicry (Dimberg and Lundquist, 1990). Recent findings moreover indicate that observation and imitation of facial expressions similarly activate both action representation networks and regions that are known to be involved in affect and facial affect recognition (Carr et al., 2003). Dysfunctions in these circuits have therefore been hypothesized to underlie the development of autistic traits (Williams et al., 2001). It remains unclear, however, whether an association indeed exists between autistic traits and spontaneous facial mimicry.
The present study investigated this question by recording spontaneous facial electromyographic responses to photographs of angry and happy facial expressions. A condition with instructed mimicry was added as a control condition to determine if all participants were equally able to perform voluntary imitation (see also McIntosh et al., 2006). Recordings were made of the zygomaticus major and corrugator supercilii muscles, which are used in smiling and frowning the eyebrows, respectively. In line with the aforementioned notion that autistic traits are continuously distributed across the population, volunteers were invited to participate in this study who had either an extremely high or low score on the Dutch version of the Autism-Spectrum Quotient (AQ; Baron-Cohen et al., 2001), and were selected from a pool of 366 (mainly) university students who had completed the AQ. Although autism is much more prevalent in men than in women, we attempted to equalize group sizes with respect to gender, which allowed us to use gender as an additional factor in statistical analyses.
Our main hypothesis was that a reduction in spontaneous imitation would be detectable in healthy, sub-clinical, participants who are high in autistic traits. We furthermore expected to replicate previously reported gender differences (i.e., stronger mimicry in women). In contrast, we anticipated no group differences in instructed voluntary mimicry.
Section snippets
Participants
366 students were recruited from different faculties of Utrecht University to complete the Dutch version of the AQ (Baron-Cohen et al., 2001). Mean score across the total sample was 15.1 with a standard deviation of 5.75 and a range of 5–33. Students who scored either extremely high or extremely low were invited to participate in this study, resulting in a low AQ group of 20 individuals (11 males, 9 females), which had an AQ-score among the lowest 30.7%. The high AQ group consisted of 21
Spontaneous mimicry condition: corrugator supercilii
Fig. 1 shows corrugator supercilii responses to angry and happy facial expressions separated for gender and AQ. The overall ANOVA demonstrated that participants in general exhibited more corrugator supercilii activity in response to angry than to happy facial expressions, as evidenced by a main effect of EXPRESSION: F(1, 30) = 11.88, P = .002, Pη2 = .28. Two-way interactions of EXPRESSION with GENDER (F(1, 30) = 2.78, P = .11, Pη2 = .09) and AQ (F(1, 30) = 1.81, P = .189, Pη2 = .06) did not reach significance,
Discussion
This study employed a spontaneous facial mimicry paradigm to investigate the hypothesis that autistic traits are related to deficits in basic mechanisms subserving coupling between perception and action (Williams et al., 2001), and therefore, to reduce spontaneous mimicry of facial expressions. Results from electromyographical recordings of the corrugator supercilii muscle revealed reduced automatic mimicry of angry facial expressions in high AQ participants, but only within the female
Acknowledgments
This research was supported by an Innovational Research Incentives Scheme Grant from the Netherlands Organization for Scientific Research (NWO) to Jack van Honk (#016-005-060). Erno Hermans and Peter Putman performed this work while employed at Utrecht University. We would like to thank Cathrien Bartels, Marjolein Spronk, and Monique de Koning. Furthermore, we would like to acknowledge anonymous reviewers for their useful comments.
References (38)
- et al.
Simultaneous recording of EEG and facial muscle reactions during spontaneous emotional mimicry
Neuropsychologia
(2008) - et al.
Does the autistic child have a “theory of mind”?
Cognition
(1985) The extreme male brain theory of autism
Trends in Cognitive Sciences
(2002)- et al.
A PET exploration of the neural mechanisms involved in reciprocal imitation
Neuroimage
(2002) - et al.
Gender differences in facial reactions to facial expressions
Biological Psychology
(1990) - et al.
Mirror neurons and the simulation theory of mind-reading
Trends in Cognitive Sciences
(1998) - et al.
Empathy and the somatotopic auditory mirror system in humans
Current Biology
(2006) - et al.
Testosterone administration reduces empathetic behavior: a facial mimicry study
Psychoneuroendocrinology
(2006) - et al.
Demystifying social cognition: a Hebbian perspective
Trends in Cognitive Sciences
(2004) - et al.
EEG evidence for mirror neuron dysfunction in autism spectrum disorders
Brain Research Cognitive Brain Research
(2005)
Imitation, mirror neurons and autism
Neuroscience and Biobehavioral Reviews
The autism-spectrum quotient (AQ): evidence from Asperger syndrome/high-functioning autism, males and females, scientists and mathematicians
Journal of Autism and Developmental Disorders
Sex differences in eye gaze and symbolic cueing of attention.
Quarterly Journal of Experimental Psychology. A: Human Experimental Psychology
Gaze and arrow cueing of attention reveals individual differences along the autism spectrum as a function of target context
British Journal of Psychology
Cognitive Therapy of Depression
Neural mechanisms of empathy in humans: a relay from neural systems for imitation to limbic areas
Proceedings of the National Academy of Sciences of the United States of America
Gender differences in the mu rhythm of the human mirror-neuron system
PLoS ONE
Autistic traits in the general population: a twin study
Archives of General Psychiatry
Gaze fixation and the neural circuitry of face processing in autism
Nature Neuroscience
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