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Autism, the Superior Temporal Sulcus and Social Perception

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Autism, the Superior Temporal Sulcus and Social Perception Review TRENDS in Neurosciences Vol.29 No.7 July 2006 INMED/TINS special issue Autism, the superior temporal sulcus and social perception Monica Zilbovicius1, Isabelle Meresse1,2, Nadia Chabane3, Francis Brunelle4, Yves Samson2 and Nathalie Boddaert1,4 1URM 0205 Brain Imaging in Psychiatry, INSERM-CEA, Service Hospitalier Fre´de´ ric Joliot, CEA, 4 Place du General Leclerc, Orsay 91406, France 2Service des Urgences Cerebro-Vasculaires, Groupe Hospitalier Pitie´ -Salpeˆ trie` re, AP-HP, 47 Bl. de l’Hoˆ pital, Paris 75013, France 3Service de Pe´ dopsychiatrie, Hoˆ pital Robert Debre´ , AP-HP, 48 Bl. Serurier, Paris 75019, France 4Hoˆ pital Necker Enfants Malades, AP-HP, Paris V, 149 Rue de Sevre, Paris 75007, France The most common clinical sign of autism spectrum accurate analysis of the dispositions and intentions of disorders (ASD) is social interaction impairment, which other individuals’ [2]. At the end of the 20th century, if we is associated with communication deficits and stereo- had asked most neuroscientists about the ‘social brain’ typed behaviors. Based on recent brain-imaging results, they would have immediately identified the frontal lobe our hypothesis is that abnormalities in the superior and limbic system, and more specifically structures such temporal sulcus (STS) are highly implicated in ASD. STS as the orbitofrontal cortex, the amygdala and the abnormalities are characterized by decreased gray striatum. These structures are indeed deeply involved in matter concentration, rest hypoperfusion and abnormal mood, motivation and decision processing. More recently, activation during social tasks. STS anatomical and researchers have also focused on another aspect of the functional anomalies occurring during early brain social brain, which can broadly be called ‘social percep- development could constitute the first step in the tion’, in which it is now clear that the superior temporal cascade of neural dysfunction underlying ASD. We will sulcus (STS) is a major player. Therefore, Brothers et al. focus this review on the STS, which has been highly [3] proposed that the amygdala, the orbitofrontal cortex implicated in social cognition. We will review recent (OFC), inferotemporal face-responsive regions and the data on the contribution of the STS to normal social STS represent areas primarily involved in the processing cognition and review brain-imaging data implicating of socially relevant information. Adolphs [4] extended this this area in ASD. This review is part of the INMED/TINS proposal by differentiating between higher-order sensory special issue Nature and nurture in brain development cortices such as the fusiform gyrus and superior temporal and neurological disorders, based on presentations at sulcus, which are involved in detailed perceptual proces- the annual INMED/TINS symposium (http://inmednet. sing, and the amygdala, ventral striatum and orbitofron- com/). tal cortex, which link sensory representations of stimuli to their motivational value. Based on recent brain-imaging results obtained for Introduction ASD [5–14], abnormalities in the STS are strongly Autism is a neurodevelopmental disorder with a range of implicated in ASD. Therefore, anatomical and functional clinical presentations, from mild to severe, referred to as anomalies in the STS during early brain development autism spectrum disorders (ASD). The most common could constitute the first step in the cascade of abnormal clinical ASD sign is social-interaction impairment, which neural phenomena underlying ASD. We will focus this is associated with verbal and non-verbal communication review on the STS, which has been strongly implicated in deficits and stereotyped obsessive behaviors [1]. Thanks to social perception and more specifically in eye-gaze recent brain-imaging studies, scientists are getting a processing. Indeed, two of the most striking social better idea of the neural circuits involved in ASD. Brain- impairments in ASD are deficits in joint attention (being imaging studies have also enabled a better understanding directed to observe an event by following the eye gaze or of the neural circuits involved in normal human social pointing gestures of another individual) and in using interaction. They have identified brain regions involved in information concerning eye gaze to understand others’ social perception and the networks underlying theory of mental states and intentions [15,16]. mind (analysis and interpretation of the intentions of In a seminal review about the role of the STS in social others) [2], which are both impaired in ASD. As defined by perception, Allison et al. stated that it is plausible that Allison et al., social perception refers to initial stages in there are STS anomalies in autism, although they also ‘the processing of information which culminates in the pointed out that there were ‘no studies specifically Corresponding author: Zilbovicius, M. ([email protected]). implicating the STS region in autism’ [2]. Five years later, new brain-imaging techniques enabled Dakin and www.sciencedirect.com 0166-2236/$ - see front matter Q 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.tins.2006.06.004 360 Review TRENDS in Neurosciences Vol.29 No.7 July 2006 Frith to suggest that ‘abnormalities in the STS may can extract this information – sometimes to a surprising provide a neural basis for the range of motion processing degree – and consequently form representations in long- deficits observed in ASD, including biological motion term memory that enable us to recognize voices on the perception’ [17]. They went on to say that, ‘such an telephone, for example. Although these ‘vocal cognition’ explanation may also provide a link between perceptual skills have a fundamental role in social interaction, little abnormalities and specific deficits in social cognition is known about the underlying cerebral mechanisms. associated with autism’. In the present paper, we will Research suggests that vocal cognition involves voice- briefly review data about the STS contribution to social selective regions of the auditory cortex located along the cognition that were published after the article of Allison STS, analogous to the ‘face areas’ of the visual cortex, and et al. [2], and then review brain-imaging data implicating possibly organized in functionally distinct cortical the STS in ASD. pathways [34,35]. Dedicated neural territories that selectively respond to voices rather than to other natural The social brain: the new role of the temporal lobe sounds are located along both superior temporal sulci [34], The ability to recognize a specific individual within a with a right hemispheric predominance [34–36]. Recog- social context is the foundation of social behavior. In non- nition of both familiar and non-familiar voices has also primate mammals, recognition of a specific individual is been found to activate the posterior STS [36]. In this voice- based largely on recognizing its specific individual smell. recognition study, Kriegstein and Giraud delineated three By contrast, monkeys and humans recognize individuals distinct areas along the right STS involved in different mostly by their facial features and the tone of their aspects of voice processing. These areas respond and vocalizations. Consequently, our brain must have interact differentially depending on (i) acoustic infor- developed a specialized ability for social cognition [3]. mation of the speech stimulus, (ii) the specific task, and Since the end of the 1970s, studies of single cells have (iii) the familiarity with the speaker. The mid-anterior indicated that specialized visual mechanisms in the STS of STS carry out a spectral analysis of voices. More posterior non-human primates produce selective neural responses and anterior areas emphasize voice processing over to such things as the movement of natural images of faces linguistic analysis of speech sounds and are both and bodies [2,18]. In humans, nothing was known about functionally connected to the mid-anterior area during the functions of the STS [19] until Howard et al. published voice recognition. However, the anterior and posterior a functional magnetic resonance imaging (fMRI) study in areas show different response properties: the anterior 1996 showing unexpected STS activation induced by a area responds specifically to voice recognition whereas the point-light display depicting a moving body [20]. At the posterior area shows a less-specific role in voice processing time, this was regarded as surprising because this – that is, sensitivity to the temporal complexity of sounds superior temporal lobe region was considered to be including non-vocal and non-linguistic sounds. Whereas dedicated to auditory processing of speech sounds. A recognition of familiar voices predominantly modulates positron emission tomography (PET) study published in connectivity between the anterior STS and the medial the same year by Bonda et al. [21] demonstrated that temporal lobe memory system, recognizing non-familiar human motion stimuli selectively activated the inferior voices predominantly involves functional interactions parietal region and the STS. Since these publications, between bilateral mid-anterior and posterior STS regions, many papers further implicated the STS in the perception and of these regions with a frontoparietal network [36]. of moving natural images of faces and bodies. STS activation was found during the perception of eye, face, Complex social cognition: analysis and interpretation of mouth, hand and body movement [22–33]. Together,
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