Trends in Neurosciences
INMED/TINS special issueAutism, the superior temporal sulcus and social perception
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.
Section snippets
The social brain: the new role of the temporal lobe
The ability to recognize a specific individual within a social context is the foundation of social behavior. In non-primate mammals, recognition of a specific individual is based largely on recognizing its specific individual smell. By contrast, monkeys and humans recognize individuals mostly by their facial features and the tone of their vocalizations. Consequently, our brain must have developed a specialized ability for social cognition [3].
Since the end of the 1970s, studies of single cells
Voice perception – a social perception in the auditory world
The human voice is probably the most important sound category of our auditory environment. Evidently, it carries speech, which makes humans a unique species. Voices are also an ‘auditory face’, rich in information concerning the identity and affective state of the speaker [34]. Humans can extract this information – sometimes to a surprising degree – and consequently form representations in long-term memory that enable us to recognize voices on the telephone, for example. Although these ‘vocal
Complex social cognition: analysis and interpretation of the intention of others
Activation of the STS in subjects presented with images of humans making movements is greater when the movements are physically possible than when they are impossible [37]; activation of the STS is also greater in response to meaningful hand motions than in response to non-meaningful ones [33]. These data thus indicate that STS processing is concerned with more than just perceptual aspects of moving or movable body parts. Rather, networks in this brain region might analyze gaze and other
Temporal lobe abnormalities in autism: new brain imaging findings
Children with autism have deficits in the perception of eye gaze, poor eye contact during communication, and difficulties accessing information to infer the mental state of others. ‘I had no idea that other people communicated through subtle eye movements,’ said an adult with autism, ‘until I read it in a magazine five years ago.’ Such a capacity might be a prerequisite for higher-level appreciation of the minds of others and is part of the larger cognitive domain of theory of mind and social
Face perception
Schultz et al. were the first to use fMRI to study face perception in autistic persons. They found significantly less activation of the middle aspect of the right fusiform face area (FFA) than in controls [48] in 14 high-functioning individuals with ASD. Hypoactivation of the FFA was replicated in a series of functional studies 48, 49, 50, 51, 52. In the same vein, Critchley et al. investigated whether high-functioning people with ASD showed a different pattern of cortical activation when
Theory-of-mind studies
Castelli et al. have studied cortical activation enhanced by animation of geometric figures [13]. The animations depicted two triangles moving about on a screen in three different conditions: moving randomly, moving in a goal-directed fashion (chasing or fighting) and moving interactively with implied intentions (coaxing or tricking). This third condition frequently elicited descriptions in terms of mental states that viewers attributed to the triangles (mentalizing). Ten adults with ASD and
Concluding remarks
Several brain-imaging studies have found anatomical and functional STS abnormalities in ASD. These are characterized by decreased gray matter concentration, rest hypoperfusion and abnormal activation patterns during social cognition tasks. The STS is crucial for social cognition and is implicated in several steps of social interactions – in auditory and visual social perception (i.e. eye gazes, gestures, facial displays of emotions and voice perception) and in more complex social cognition
References (54)
Social perception from visual cues: role of the STS region
Trends Cogn. Sci.
(2000)Response of neurons in the macaque amygdala to complex social stimuli
Behav. Brain Res.
(1990)Superior temporal sulcus anatomical abnormalities in childhood autism: a voxel-based morphometry MRI study
NeuroImage
(2004)- et al.
Vagaries of visual perception in autism
Neuron
(2005) - et al.
Demystifying social cognition: a Hebbian perspective
Trends Cogn. Sci.
(2004) A direct demonstration of functional specialization within motion-related visual and auditory cortex of the human brain
Curr. Biol.
(1996)Brain regions involved in the perception of gaze: a PET study
NeuroImage
(1998)Cortical substrates for the perception of face actions: an fMRI study of the specificity of activation for seen speech and for meaningless lower-face acts (gurning)
Cogn. Brain Res.
(2001)- et al.
Distinct functional substrates along the right superior temporal sulcus for the processing of voices
NeuroImage
(2004) Movement and mind: a functional imaging study of perception and interpretation of complex intentional movement patterns
NeuroImage
(2000)
Reading the mind in cartoons and stories: an fMRI study of ‘theory of mind’ in verbal and nonverbal tasks
Neuropsychologia
Brain activation evoked by perception of gaze shifts: the influence of context
Neuropsychologia
The cognitive basis of a biological disorder: autism
Trends Neurosci.
Afferent cortical connections and architectonics of the superior temporal sulcus and surrounding cortex in rhesus monkey
Brain Res.
Autistic disturbances of affective contact
Nervous Child
Cognitive neuroscience of human social behaviour
Nat. Rev. Neurosci.
Temporal lobe dysfunction in childhood autism: a PET study
Am. J. Psychiatry
Abnormal regional cerebral blood flow in childhood autism
Brain
Autism severity and temporal lobe functional abnormalities
Ann. Neurol.
Cortical sulcal maps in autism
Cereb. Cortex
The neuroanatomy of autism: a voxel-based whole brain analysis of structural scans
NeuroReport
Abnormal cortical voice processing in autism
Nat. Neurosci.
Autism, Asperger syndrome and brain mechanisms for the attribution of mental states to animated shapes
Brain
Neural basis of eye gaze processing deficits in autism
Brain
Recognition of mental state terms. Clinical findings in children with autism and a functional neuroimaging study of normal adults
Br. J. Psychiatry
Interacting minds – a biological basis
Science
Cited by (290)
Unveiling the development of human voice perception: Neurobiological mechanisms and pathophysiology
2024, Current Research in NeurobiologyEarly prediction of Autism Spectrum Disorders through interaction analysis in home videos and explainable artificial intelligence
2023, Computers in Human Behavior