Autism spectrum disorder (ASD) is a behaviorally defined neurodevelopmental disorder that affects as many as 1 in 86 children (Baird et al.
). Its defining features include mild to severe impairments in communication and reciprocal social interaction as well as repetitive and stereotyped behaviors children. Difficulty in recognizing and appropriately reacting to other people's emotions, whether they are communicated by facial expressions, vocal tone, gestures or bodily postures, counts among the most frequently noted anomalies in the social-communicative skills of people with ASD.
To date, research on these issues has focused primarily on impairments in the neurofunctional processes associated with viewing facial expressions. Face perception involves a network of subcortical and cortical areas, including the superior colliculus, the pulvinar nucleus of the thalamus, the amygdala, the insula, the inferior occipital gyrus, the lateral fusiform gyrus, the superior temporal sulcus, the somato-motor cortex, the inferior frontal gyrus and the orbitofrontal cortex [for review, see Ishai (2008
)]. Functional abnormalities have been found in the face perception network in ASD in response to emotionally neutral (Golarai et al.
; Hadjikhani et al.
; Kleinhans et al.
) as well as emotionally expressive (Dapretto et al.
; Hall et al.
; Pelphrey et al.
) faces, particularly in the amygdala and the mirror neuron system (MNS). Although earlier behavioral studies did not consistently find emotion perception deficits [(Hobson et al.
; Braverman et al.
; Macdonald et al.
; Tantam et al.
; Capps et al.
; Davies et al.
), but see (Ozonoff et al.
; Baron-Cohen et al.
; Grossman et al.
; Gepner et al.
; Adolphs et al.
)], recent studies taking a more fine-grained approach have documented emotion recognition impairments mainly in the perception of negative emotions, especially fear (Baron-Cohen et al.
; Dawson et al.
; Welchew et al.
; Ashwin et al.
, 2007; Corden et al.
; Gaigg and Bowler, 2007
; Humphreys et al.
Emotion perception deficits in autistic individuals are not necessarily limited to the perception of faces, but may involve perception of other emotion signals abundantly available in the social environment, such as emotions expressed by the whole body. In a recent study, Hubert et al.
) demonstrated that ASD individuals performed significantly worse than controls in recognizing emotions from point-light displays even though they performed as well as control participants in recognizing simple actions and objects manipulations. The authors interpreted their findings as evidence that emotional perception difficulties are not restricted to faces but also affect the perception of body expression of emotion.
Investigations focusing on neutral body postures and movements have revealed some intriguing similarities between visual perception of faces and of bodies. For example, inverted presentation has been shown to have similarly disruptive effects on perception and processing of bodies and faces, suggesting that body perception, like face perception, depends on configural perceptual processes (Reed et al.
; Stekelenburg and de Gelder, 2004
). In addition, an inversion effect has been shown in the recognition of emotions expressed by whole-body movement (Atkinson et al.
). A recent study by Van de Riet and colleagues (2008) that specifically compared processing of affective information from faces and bodies has further underlined the similarities between perception of emotions in faces and bodies and its neurofunctional bases. This study showed that the amygdala and the fusiform gyrus are involved in recognizing emotional signals, whether expressed via the face or the whole body, and that the extrastriate body area of the middle occipital–temporal region is not sensitive to emotion. In addition, specific parts of the superior temporal sulcus (STS), parietal lobe and subcortical structures were found to be selectively responsive to facial and body expression.
In previous studies with neurotypical (NT) individuals (Hadjikhani and de Gelder, 2003
; de Gelder et al.
), we found that bodily expressions of emotion, in which no information was available from the face, activated a network of brain regions similar to those activated by facial expressions of emotion. These areas included the fusiform face area (FFA), the Inferior Occipital Gyrus (IOG), areas of the MNS, including the inferior frontal cortex (IFC) and the inferior parietal lobule (IPL), as well as subcortical structures, including the superior colliculus, pulvinar and amygdala. These findings suggest an overlap in the neural mechanisms subserving emotional perception whether expressed in the face or in the body. In addition, these stimuli activated areas involved in representation of movement, suggesting fear contagion and automatic preparation of the brain for action in the presence of body expression of fear.
The amygdala plays an important role in the perception of emotion, and there are indications from neuropathology, lesion and neuroimaging studies that it plays a role in the social cognition deficits in autism. Numerous studies have found abnormalities in the amygdala of autistic participants (Bauman and Kemper, 1985
; Abell et al.
; Aylward et al.
; Howard et al.
; Pierce et al.
; Nacewicz et al.
; Schumann and Amaral, 2006
) and some have suggested that amygdala dysfunction may play a causal role in autistic social impairment (Baron-Cohen et al.
; Adolphs et al.
; Schultz, 2005
). Interestingly, however, prior studies (Adolphs et al.
; Atkinson et al.
) have demonstrated that the amygdala is not necessary for the normal recognition of emotions in whole bodies.
In addition, other components of the ‘structural encoding system’ for faces (Bruce and Young, 1986
) are also involved in the early stages of body perception (Gliga and Dehaene-Lambertz, 2005
; Johnson, 2005
; Skuse, 2006
; Tsuchiya and Adolphs, 2007
). These include the superior colliculus and the pulvinar nucleus of the thalamus. The pulvinar plays an important role in fear recognition, as shown in lesion studies (Ward et al.
). It receives inputs from the superior colliculus and the retina, and has reciprocal connections with higher cortical areas, including the extrastriate cortex, the frontal cortex and the amygdala (Grieve et al.
). To date, only one study has examined these structures in ASD and reported decreased connectivity between the midline thalamus, the superior colliculus and the FFA during face perception (Kleinhans et al.
Here, we tested the hypothesis that abnormalities in emotional perception in ASD are not confined to faces, but that they also pertain to the perception of bodily expression. To do so, we examined behavior and brain activation in individuals viewing bodies expressing emotion, specifically fear, as compared with emotionally neutral bodies engaged in everyday actions.