Research ReportEnlarged right superior temporal gyrus in children and adolescents with autism
Research Highlights
►Right STG was significantly larger after controlling for age and total brain volume. ►Right posterior STG was significantly larger in post hoc analyses. ►Left STG volumes was not significantly different. ►Results suggest a neuroanatomical basis for social perceptual deficits of autism.
Introduction
Autism is a pervasive developmental disorder characterized by impairments in reciprocal social interaction, verbal and nonverbal language and communication, and a restricted range of interests and repetitive behavior (A.P.A., 2000). Sensory and motor signs and symptoms, inattention with hyperactivity, emotion dysregulation, and intellectual disability are also integral aspects of this syndrome in many, though not all, affected individuals (Rogers and Dawson, 2009). The myriad social, language, cognitive, emotional, and behavioral problems observed in autism suggest that the syndrome affects a functionally diverse and widely distributed set of neural systems as evidenced by the wide range of structural abnormalities that have been reported (Brambilla et al., 2003, Palmen and van Engeland, 2004). Several brain regions have been examined extensively; however, the superior temporal gyrus (STG), an established node in the “social brain” network (Baron-Cohen et al., 1999, Bigler et al., 2007, Brothers and Ring, 1992), has received relatively little attention. In fact, a very limited number of morphometric investigations have been conducted to examine the size of the STG, a key structure that has been implicated in several neuropsychological and physiological functions thought to be abnormal in this severe neurodevelopmental disorder (Pelphrey et al., 2004).
Investigating STG abnormalities in autism is a logical endeavor given its important roles in language processing and social perception. The STG is perhaps best known for the former as it consists of the primary auditory cortex and Wernicke's area. Abnormalities in these regions can result in profound language difficulties as illustrated in the extreme cases of cortical deafness and receptive aphasia (Eggert, 1977, Wernicke, 1874). Since the description of cortical deafness, it has been known that the STG is bilaterally involved in the initial stages of auditory perception (Zilbovicius et al., 1995). While the STG's important role in language processing has been known since the 19th century, its role in social perception has a much more recent history. There exists now an extensive body of literature demonstrating the STG's role in social perception. The STG's importance in social perception was spawned by the use of functional magnetic resonance imaging (fMRI) in cognitive neuroscience research. Numerous tasks tapping social perception have been used in conjunction with fMRI to demonstrate the involvement of the superior temporal region such as the STG and superior temporal sulcus, and these studies have been reviewed extensively elsewhere (Pelphrey and Carter, 2008b, Redcay, 2008). Furthermore, the STG is highly connected to other key regions of the brain such as the superior temporal sulcus, frontal and parietal lobes, and the limbic and associated sensory systems (Gloor, 1997, Pandya and Yeterian, 1985, Seltzer and Pandya, 1978). Therefore, the STG may play a critical role in processing and integrating different types of information in order to give proper meaning to the surrounding world, and it has been suggested that temporal region dysfunction is implicated in almost all deficits observed in autism (Boddaert and Zilbovicius, 2002).
Numerous studies implementing a wide range of research modalities have reported different types of STG abnormalities in autism. In an influential postmortem study of the cytoarchitecture of the cerebral cortex, Casanova et al. (2002) reported abnormal cortical minicolumns (a basic functional neuronal unit) in the STG of patients with autism when compared to healthy controls. In voxel-based MRI investigations, Waiter et al. (2004) and Salmond et al. (2003) also reported STG abnormalities such as increased gray matter volume. Moreover, a number of positron emission tomography (PET) (Boddaert et al., 2003, Castelli et al., 2002, Muller et al., 1999, Zilbovicius et al., 1995), single photon emission computed tomography (SPECT) (Mountz et al., 1995, Ohnishi et al., 2000), fMRI (Baron-Cohen et al., 1999, Boddaert et al., 2003, Gomot et al., 2006, Pelphrey and Carter, 2008a, Pelphrey et al., 2005), event-related potential (ERP) (Bruneau et al., 2003, Bruneau et al., 1999), and magnetoencephalography (MEG) (Gage et al., 2003, Roberts et al., 2010, Rojas et al., 2008) studies have also revealed STG abnormalities in autism, reporting abnormal STG activation/activity both during rest and while performing various tasks.
Despite this broad array of evidence supporting STG abnormalities in autism, a limited number of studies have been conducted specifically examining the size of this structure. Of these limited number of studies, most looked exclusively at asymmetry rather than group comparison of STG volume (De Fosse et al., 2004, Gage et al., 2009, Herbert et al., 2002, Herbert et al., 2005). There are, however, at least two studies directly comparing STG volume between autism and control groups. One volumetric study examined total STG volume in autism and found no significant volumetric differences when compared to a matched control group (Bigler et al., 2007). In contrast, the voxel-based MRI study mentioned previously, found increased STG gray matter volume when compared to controls (Waiter et al., 2004). In light of these inconsistent findings, this study was carried out to examine the total left and right STG size in high-functioning male children and adolescents with autism. Given that overgrowth has been associated with dysfunction at least during young ages (Courchesne et al., 2004), the replicable finding of increased brain volume (Piven et al., 1995), and evidence suggesting the frontal/temporal lobes are most affected (Courchesne et al., 2004), it is hypothesized that STG volumes will be increased in subjects with autism when compared to healthy controls.
Section snippets
Results
Examination of the scatter plots depicting all participants' STG volumetric data by study group (Fig. 1) revealed one typically-developing control (TDC) subject who was an outlier in all volumetric measures, including left STG (TDC mean = 18.67 ± 2.41 cc, outlier value = 25.06 cc) and right STG (TDC mean = 17.76 ± 2.26 cc, outlier value = 23.89 cc). No outliers were present in the high-functioning autism (HFA) group. This outlier is clearly identified using box plots as depicted in Fig. 2.
In light of the
Discussion
Given the STG's important roles in language processing (left hemisphere) and social perception (right hemisphere), the main goal of this study was to examine STG volumes in a sample of children and adolescents with autism. It was hypothesized that STG volumes would be greater in subjects with autism compared to healthy controls based on the replicable finding of brain overgrowth (which is associated with dysfunction) which is more prominent in frontal/temporal lobes. The results of this study
Participants
Subjects were 18 individuals with HFA between the ages of 8 and 18 years of age and 20 TDC individuals between 9 and 18 years of age. The study was confined to right-handed males because the sample size was insufficient to accommodate for the structural variability associated with handedness and gender. While restricting the study to high-functioning individuals generally leads to greater success in completing MRI scanning procedures, it does exclude a larger number of individuals with autism who
Acknowledgments
This work was supported by a National Institute of Mental Health (NIMH) grant MH 64027 (Dr. Hardan), National Institute of Child Health and Human Development (NICHD) grant HD 35469 (Dr. Minshew), and NICHD Collaborative Program of Excellence in Autism (CPEA). This work was also supported, in part, by the ANA/Pfizer Fellowships in Clinical Practice from Pfizer's Medical and Academic Partnership program (Dr. Jou).
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