Elsevier

NeuroImage

Volume 31, Issue 4, 15 July 2006, Pages 1614-1624
NeuroImage

Attention does not modulate neural responses to social stimuli in autism spectrum disorders

https://doi.org/10.1016/j.neuroimage.2006.02.037Get rights and content

Abstract

We investigated whether individuals with autism spectrum disorders (ASD) would show attentional modulation for social (face) and non-social (house) stimuli. Sixteen individuals with ASD and 16 matched control participants completed a task in which pairs of face and house stimuli were present on every trial, with one of the pairs randomly assigned to attended locations and the other to unattended locations. Both mass-univariate (SPM) and region of interest analyses suggested that responses to houses were modulated by attention in both groups, but that only the control participants demonstrated attentional modulation of face-selective regions. Thus, the participants with ASD demonstrated a lack of attentional modulation which was particularly evident for the social stimulus. Analyses of effective connectivity indicated that these results were due to a failure of attention to modulate connectivity between extrastriate areas and V1. We discuss how these results may suggest a mechanism to explain the reduced salience of social stimuli in ASD.

Introduction

Autism Spectrum Disorders (ASD) are developmental disorders which are characterized by abnormalities of social interaction, impairments in verbal and non-verbal communication, and a restricted repertoire of interests and activities (American Psychiatric Association (APA), 1994). Different symptoms associated with ASD have been explained with considerable success by three cognitive theories: that individuals with ASD lack an intuitive understanding of minds (Baron-Cohen et al., 1985); that a detailed, local processing style is preferred over a global style (Happé, 1999); and that individuals with ASD have executive function problems (Russell, 1997).

Empirical research has demonstrated that individuals with ASD may have specific problems with certain executive functions while being relatively unimpaired on others (Hill, 2004). Studies of attention, perhaps the most fundamental executive function, in ASD populations suggest particular impairments in situations in which a single stimulus, or single feature of a stimulus, must be selectively attended. Examples include allocating attention in the presence of distractors (e.g. Burack, 1994), and switching the attentional focus rapidly between sensory modalities (Courchesne et al., 1994), spatial locations (Wainwright and Bryson, 1996), or object features (Courchesne et al., 1994). On other attentional tasks that do not require rapid shifts of attention, individuals with ASD perform at normal or near-normal levels (Belmonte, 2000, Courchesne et al., 1994). Such a pattern of impairment suggests problems with higher-order attentional control networks in ASD.

Studies have indicated that attention is controlled via feedback connections from frontal and parietal regions including superior parietal lobule (SPL), intraparietal sulcus (IPS), frontal eye field (FEF), and supplementary eye field (SEF) (e.g. Corbetta et al., 1993, Fink et al., 1997). In addition, a role for the lateral prefrontal cortex in the region of the middle frontal gyrus (MFG) and the anterior cingulate cortex (ACC) has been proposed (e.g. Corbetta et al., 1993, Nobre et al., 1997). The hypothesis that these areas control attention through feedback connections to visual processing areas is supported by tract-tracing studies in monkeys which demonstrate direct feedback connections to extrastriate areas V4 and temporal–occipital area (TEO) from parietal area LIP and to inferior temporal cortex area TE from prefrontal cortex, in addition to indirect feedback connections from prefrontal cortex to areas V4 and TEO via area LIP (Cavada and Goldman-Rakic, 1989, Ungerleider et al., 1989).

The reliance of attentional control on feedback connections from fronto-parietal areas, and the poor attentional control seen in ASD, provide support for recent claims of weaker neural connectivity in ASD (Castelli et al., 2002, Just et al., 2004). Such a reduction in connectivity has been argued to lead to a failure of top-down modulation of early sensory processing (Frith, 2003). This failure may be expected to result in a lack of attentional modulation in ASD; it is this possibility that the present study was designed to investigate.

Attentional modulation of higher-order visual processing areas in extrastriate cortex has been demonstrated in a number of studies in typically developing individuals (e.g. Haxby et al., 1994, Wojciulik et al., 1998). These studies present two classes of stimuli simultaneously which are represented in separate areas of extrastriate cortex (typically faces and houses), and ask participants to selectively attend to one class of stimulus. Results indicate that the response in regions which code for a stimulus class is greater when the preferred stimulus class is attended than when it is unattended (i.e. the neural response is modulated by attention).

Based on findings of weaker connectivity between cortical areas in ASD, and the reliance of attentional control on feed-back connections from fronto-parietal networks to sensory processing areas, one may predict a general lack of attentional modulation in ASD. However, despite impairments in the allocation of attention to both social and non-social stimuli in ASD, it is possible to speculate that a lack of attentional modulation (i.e. a weaker effect of attentional allocation) may only be seen for social stimuli. Such specificity is suggested by the large number of studies that demonstrate particular impairments in processing social stimuli, coupled with unimpaired processing of non-social stimuli, in ASD. These include: impairments in visual memory for faces but not buildings (Blair et al., 2002, Boucher and Lewis, 1992); impairment in exogenous orienting of attention to social cues, but not to objects (Leekam and Moore, 2001); reduced salience of social stimuli/preference for non-social stimuli (e.g. Dawson et al., 2004, Klin et al., 2002, Swettenham et al., 1998); and a failure to show differential event-related potentials to familiar vs. unfamiliar faces while exhibiting different event-related potentials to familiar and unfamiliar objects (Dawson et al., 2002).

This study aimed to investigate attentional modulation in ASD using a paradigm that has been shown to detect attentional modulation (Vuilleumier et al., 2001). Pairs of face and house stimuli were presented around a central fixation cross and participants were required to attend selectively to either the horizontal or vertical pair of stimuli and make a same-different judgment. The location of the attended stimulus pair was constant within blocks but which stimulus class appeared at the attended location was random. Thus, pairs of faces and houses were present on each trial, but which stimulus class was attended varied unpredictably from trial to trial (see Fig. 1). Event-related functional Magnetic Resonance Imaging (efMRI) allowed the comparison of neural activity in face-selective brain areas when faces were attended relative to when they were unattended, and in house-selective brain areas when houses were attended and unattended. Any difference in activation between the attended and unattended conditions indicates attentional modulation, as visual input remains constant across trials (participants are required to fixate centrally throughout and pairs of face and house stimuli are present on every trial). If ASD results in a general lack of attentional modulation, one would expect neural responses to both faces and houses to be equal irrespective of attention. However, if a lack of attentional modulation is specific to social stimuli, one would expect neural responses to houses to show attentional modulation, but neural responses to faces to be unmodulated by attention.

Section snippets

Participants

Sixteen individuals with ASD (14m:2f) and 16 control (14m:2f) participants took part in this study. Groups were matched on gender, age (ASD M: 33.3 years SD: 11.5, control M: 35.3 years, SD: 12.1), and IQ (ASD M: 119 SD: 14, control M: 119 SD: 13.2). Full-scale IQ was measured using the Wechsler Adult Intelligence Scale-3rd UK Edition (Wechsler, 1999). All participants in the ASD group had previously received a diagnosis of autism (N = 1) or Asperger Syndrome (N = 15) from an independent

Behavioral data

All participants completed the experimental task twice, once outside the scanner, and, on a separate day, while being scanned. RT and error data did not differ on the two occasions, and so only scanner data are reported. The only significant effect in these data were a main effect of stimulus identity: errors were less frequent when judging house pairs compared to face pairs (33% errors faces, 24% errors houses, F(1,30) = 15.4, P < 0.001). There were no differences between the groups for RT or

Discussion

This study aimed to address four questions: First, are there group differences in either the selectivity or extent of face- or house-selective extrastriate areas? Second, are face- and house-selective areas modulated by attention in both the ASD and control groups? Third, are there group differences in the amount of attentional modulation of face- and house-selective areas? And fourth, can changes in effective connectivity explain any group differences in attentional modulation?

Our results

Acknowledgments

Thanks go to Jon Driver, Ray Dolan, Chloe Hutton and Steffan Kennett for many helpful discussions, and to the radiological staff at the Wellcome Department of Imaging Neuroscience for their practical help and support. We are also grateful to Patrick Vuilleumier and Paul Bentley for advice and assistance with programming. This study was supported by the Medical Research Council UK (Program grant no. G9617036) and the Wellcome Trust.

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