Autism, the superior temporal sulcus and social perception

The most common clinical sign of autism spectrum disorders (ASD) is social interaction impairment, which is associated with communication deficits and stereotyped behaviors. Based on recent brain-imaging results, our hypothesis is that abnormalities in the superior temporal sulcus (STS) are highly implicated in ASD. STS abnormalities are characterized by decreased gray matter concentration, rest hypoperfusion and abnormal activation during social tasks. STS anatomical and functional anomalies occurring during early brain development could constitute the first step in the cascade of neural dysfunction underlying ASD. We will focus this review on the STS, which has been highly implicated in social cognition. We will review recent data on the contribution of the STS to normal social cognition and review brain-imaging data implicating this area in ASD. This review is part of the INMED/TINS special issue Nature and nurture in brain development and neurological disorders, based on presentations at the annual INMED/TINS symposium (http://inmednet.com/).

Introduction

Autism is a neurodevelopmental disorder with a range of clinical presentations, from mild to severe, referred to as autism spectrum disorders (ASD). The most common clinical ASD sign is social-interaction impairment, which is associated with verbal and non-verbal communication deficits and stereotyped obsessive behaviors [1]. Thanks to recent brain-imaging studies, scientists are getting a better idea of the neural circuits involved in ASD. Brain-imaging studies have also enabled a better understanding of the neural circuits involved in normal human social interaction. They have identified brain regions involved in social perception and the networks underlying theory of mind (analysis and interpretation of the intentions of others) [2], which are both impaired in ASD. As defined by Allison et al., social perception refers to initial stages in ‘the processing of information which culminates in the accurate analysis of the dispositions and intentions of other individuals’ [2]. At the end of the 20th century, if we had asked most neuroscientists about the ‘social brain’ they would have immediately identified the frontal lobe and limbic system, and more specifically structures such as the orbitofrontal cortex, the amygdala and the striatum. These structures are indeed deeply involved in mood, motivation and decision processing. More recently, researchers have also focused on another aspect of the social brain, which can broadly be called ‘social perception’, in which it is now clear that the superior temporal sulcus (STS) is a major player. Therefore, Brothers et al. [3] proposed that the amygdala, the orbitofrontal cortex (OFC), inferotemporal face-responsive regions and the STS represent areas primarily involved in the processing of socially relevant information. Adolphs [4] extended this proposal by differentiating between higher-order sensory cortices such as the fusiform gyrus and superior temporal sulcus, which are involved in detailed perceptual processing, and the amygdala, ventral striatum and orbitofrontal cortex, which link sensory representations of stimuli to their motivational value.

Based on recent brain-imaging results obtained for ASD 5, 6, 7, 8, 9, 10, 11, 12, 13, 14, abnormalities in the STS are strongly implicated in ASD. Therefore, anatomical and functional anomalies in the STS during early brain development could constitute the first step in the cascade of abnormal neural phenomena underlying ASD. We will focus this review on the STS, which has been strongly implicated in social perception and more specifically in eye-gaze processing. Indeed, two of the most striking social impairments in ASD are deficits in joint attention (being directed to observe an event by following the eye gaze or pointing gestures of another individual) and in using information concerning eye gaze to understand others' mental states and intentions 15, 16.

In a seminal review about the role of the STS in social perception, Allison et al. stated that it is plausible that there are STS anomalies in autism, although they also pointed out that there were ‘no studies specifically implicating the STS region in autism’ [2]. Five years later, new brain-imaging techniques enabled Dakin and Frith to suggest that ‘abnormalities in the STS may provide a neural basis for the range of motion processing deficits observed in ASD, including biological motion perception’ [17]. They went on to say that, ‘such an explanation may also provide a link between perceptual abnormalities and specific deficits in social cognition associated with autism’. In the present paper, we will briefly review data about the STS contribution to social cognition that were published after the article of Allison et al. [2], and then review brain-imaging data implicating the STS in ASD.