Elsevier

Research in Autism Spectrum Disorders

Volume 5, Issue 1, January–March 2011, Pages 201-209
Research in Autism Spectrum Disorders

Top-down and bottom-up visual information processing of non-social stimuli in high-functioning autism spectrum disorder

https://doi.org/10.1016/j.rasd.2010.03.012Get rights and content

Abstract

Individuals with high-functioning autism spectrum disorder (HF-ASD) often show superior performance in simple visual tasks, despite difficulties in the perception of socially important information such as facial expression. The neural basis of visual perception abnormalities associated with HF-ASD is currently unclear. We sought to elucidate the functioning of bottom-up and top-down visual information processing in HF-ASD using event-related potentials (ERPs). Eleven adults with HF-ASD and 11 age-matched normal controls (NC) participated in this study. Visual ERPs were recorded using 128-channel EEG. The P1 and P300 were recorded in response to target stimuli. Visual mismatch negativity (vMMN) potentials were obtained by subtracting responses to standard from those to deviant stimuli. Behaviorally, individuals with HF-ASD showed faster target detection than NCs. However, vMMN amplitude and latency were the same between the two groups. In contrast, P1 and P300 amplitudes were significantly decreased in HF-ASD compared with NCs. In addition, P300 latency was significantly delayed in HF-ASD. Individuals with HF-ASD exhibit altered visual information processing. Intact bottom-up attention (vMMN) may contribute to their superior simple visual task performance in spite of abnormal low-level (P1) and top-down (P300) visual information processing.

Introduction

Autism spectrum disorder (ASD) is a developmental neuropsychiatric disorder characterized by deficits in socialization, communication, and repetitive/stereotyped behaviors. Over the past several decades, extensive studies using various genetic, neurobiological, cognitive and behavioral approaches have sought a single explanation for the heterogeneous manifestations of ASD, but no consensus on the etiology of ASD has emerged (Happé & Frith, 2006). Although there are prominent symptoms of ASD within the social domain, several researchers have proposed that abnormalities also exist in basic (lower level) sensory processing as well as attention and cortical (higher level) processing (Dakin and Frith, 2005, Mottron and Burack, 2001, Tuchman and Rapin, 2006). Indeed, a number of studies have shown atypical performance of individuals with ASD in a wide range of perceptual tasks (e.g. for a review, Mottron, Dawson, & Soulières, 2009). In terms of research findings in the visual modality, evidence emerging over the past few decades has indicated that ASD is associated with both unique abilities and unique deficits in higher level visual processing (Dakin & Frith, 2005). For instance, individuals with ASD generally perform well on the Wechsler Intelligence Scale for Children (WISC) Block Design test (Shah and Frith, 1983, Shah and Frith, 1993), the embedded figures test (Jolliffe & Baron-Cohen, 1997), visual search (Plaisted, O’Riordan, & Baron-Cohen, 1998), and copying impossible figures (Mottron, Burack, Stauder, & Robaey, 1999). In contrast, their performance tends to be poor for detecting biological motion (Blake, Turner, Smoski, Pozdol, & Stone, 2003), integrating rapid visual motion (Gepner & Mastre, 2002), and perceiving coherent motion (Spencer, O’Brien, Riggs, Baraddick, Atkinson, & Wattam-Bell, 2002). These findings have often been interpreted from the viewpoint of local vs. global processing (Frith, 1989, Happé, 1999, Mottron and Burack, 2001, Plaisted, 2001). One persuasive theoretical account to explain the range of abilities and deficits characterizing ASD is “weak central coherence” (WCC). This theory proposes that the bias toward detail-focused, local processing over global processing results in a failure to extract global form/meaning (Happé & Frith, 2006). Alternatively, the concept of top-down and bottom-up attention may be related to the peculiar visual task performance of individuals with ASD. At present a conclusive explanation remains unclear due to the limited time resolution of the psychobehavioral techniques used so far.

Visual sensory information is first processed at a low level, with information flowing from the retina to the primary visual cortex (V1). The information then passes into a higher level of neural processing. It is well known that the P1 (i.e. the first positive peak from the stimulus onset) reflects the lower level visual information processing stage (i.e. V1 or earlier; for a review, Tobimatsu & Celesia, 2006). Previous studies have suggested that lower level visual information processing may be affected in ASD, because affected individuals exhibit a decreased and delayed P1 (Boeschoten et al., 2007, Hoeksma et al., 2004, Hoeksma et al., 2006, Itier and Taylor, 2002, Itier and Taylor, 2004, O’Conner et al., 2005, Taylor et al., 2001, Webb et al., in press). Alternatively, selective attention may be involved. Selective attention is the process whereby a subset of the input is selected preferentially for further processing and has two major aspects: bottom-up attention and top-down attention. Bottom-up attention is elicited or driven by the properties of stimuli automatically whereas top-down attention refers to a volitional focusing of attention on a location and/or an object based on current behavioral goals (Ciaramelli, Grady, & Moscovitch, 2008). These streams can operate in parallel but bottom-up attention occurs more quickly than top-down attention (e.g. Treisman, Vieira, & Hayes, 1992). Event-related potentials (ERPs), which have the benefit of a very high-temporal resolution (in the order of milliseconds), are an appropriate technique for recording electrophysiological signals from the scalp. ERPs allow us to temporally characterize human sensory information processing. Two specific components of the ERP, the visual mismatch negativity (vMMN) and the visual P300, are candidates for biomarkers of bottom-up and top-down attention, respectively (Maekawa et al., 2005, Maekawa et al., 2009). To the best of our knowledge, there have been no ERP studies focusing on the bottom-up and top-down attention in ASD. Therefore, the aim of this study was to characterize visual information processing in high-functioning ASD (HF-ASD) individuals and to determine whether or not bottom-up and/or top-down attention is affected by the disorder. To this end, we measured early visual ERP components including the P1 and P300, as well as the vMMN.

Section snippets

Participants

Eleven individuals with HF-ASD (eight males and three females, aged 18–40 years, mean age 28.0), and 11 healthy controls (HCs) matched for chronological age (CA) and sex (four males and seven females, aged 20–38 years, mean age 28.9) participated in the study. The HF-ASD group included six individuals with Asperger's disorder, three individuals with autistic disorder, and three individuals with a pervasive developmental disorder not otherwise specified (PDD-NOS). The HF-ASD participants were

Results

Although the behavioral performance of all participants was successfully measured, EEG data from two participants in each group were excluded from the ERP analyses because of excessive artifacts in their ERP recordings. Following these exclusions, there were nine participants in each group. Although the gender ratio appeared to be quite different between the two groups (i.e. female to male ratio in HF-ASD was 7:2 and that in NC was 4:5), there were no significant between-group differences in

Discussion

The major differences we found between the HF-ASD group and the NC group are summarized as follows. In HF-ASD individuals, (1) behavioral target detection was significantly faster, (2) the P1 response (80–120 ms) to standard and deviant stimuli was significantly smaller, (3) the P300 latency (300–500 ms) was significantly prolonged and its amplitude was decreased, and (4) both the mean amplitude and latency of vMMN (150–300 ms) were within the normal range. These findings suggest that individuals

Conclusion

The present study is the first report focusing on bottom-up and top-down attention in HF-ASD using vMMN and the P300. Our results suggested that bottom-up involuntary attention is unaffected in HF-ASD, while lower level and top-down visual information processing are impaired in the condition.

Acknowledgments

This study was supported in part by grants from the Research Institute of Science and Technology for Society, Japan (RISTEX), the Naito Foundation and the Sankyo Foundation of Life Science.

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