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Abnormal Attention in Autism Shown by Steady-State Visual Evoked Potentials

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Abnormal Attention in Autism Shown by Steady-State Visual Evoked Potentials 04belmonte (ds) 18/7/00 9:44 am Page 269 autism © 2000 SAGE Publications Abnormal attention in autism and The National Autistic Society Vol 4(3) 269–285; 013642 shown by steady-state visual 1362-3613(200009)4:3 evoked potentials MATTHEW BELMONTE McLean Hospital Brain Imaging Centre, Belmont, MA, USA KEYWORDS ABSTRACT This study examined brain electrical responses as a asymmetry; physiological measure of speed and specificity of attentional shifting in EEG; eight adult males with autism. Subjects were required to shift attention spatial between rapidly flashed targets alternating between left and right visual attention; hemifields. When targets were separated by less than 700 ms, steady- steady-state state brain electrical response in both hemispheres was augmented and background EEG decreased for rightward shifts as compared with left- evoked ward shifts. At longer separations, persons with autism showed no potential; modulation of background EEG, and high variability in steady-state vision response. These results contrast with those in normal controls, where in each hemisphere separately steady-state response increased and background EEG descreased for shifts directed contralaterally to that hemisphere. Group differences were significant at p < 0.04 for the steady-state response and p < 0.0001 for the background EEG. Lack of hemispherically independent modulation in autism may reflect the operation of a non-specific mechanism of sensory gating. ADDRESS Correspondence should be addressed to: MATTHEW BELMONTE, MIT 14E-303, 77 Massachusetts Avenue, Cambridge, MA 02139-4307, USA The ability to attend to relevant stimuli and to filter out irrelevant ones is fundamental to the normal development of a child. Joint social attention, in particular, rests on an ability to shift the attentive focus rapidly between a caregiver and some external object (Bakeman and Adamson, 1984).When a parent shows an infant a toy, for example, the infant must register not only the image of the toy,the texture of the toy and the sound made by the toy, but also the parent’s voice, facial expression and gestures in response to the infant and the toy. In order to integrate all these stimuli into coher- ent percepts, the developing child must rapidly alter the scope and focus of attention among many sensory modalities and locations. An accumulation of behavioural evidence indicates that such task-based control over the scope of attention is lacking in autism (Burack et al., 1997). Physiological 269 Downloaded from aut.sagepub.com at CAMBRIDGE UNIV LIBRARY on June 19, 2015 04belmonte (ds) 18/7/00 9:44 am Page 270 AUTISM 4(3) studies suggest that this deficit in attentional control reflects a lack of specificity in perceptual gating, that is, in the process of selecting a few rel- evant stimuli from the large set of sensory inputs and conveying those stimuli into higher-order perceptual processing.A complete exploration of this hypothesis requires physiological measures of changes in perceptual gating in response to changing task demands. Poor control over the scope of attention is most evident in tasks that demand rapid reorganization of perceptual resources in response to changes in incoming stimuli. In a widely applied task developed by Posner et al. (1984), a cue informs subjects about the likely location of a subse- quently appearing target. The cue may be spatial, as in a highlighting of the target area, or symbolic, as in an arrow pointing to the target area. After a variable delay from the onset of the cue, the target may appear in the cued (valid) location or in the uncued (invalid) location. The reaction times of normal subjects to these targets show a validity effect, that is, a cost of invalid cueing and a benefit of valid cueing. In a high-functioning group of adolescents and young adults with diagnoses of autism or Asperger syn- drome, Wainwright-Sharp and Bryson (1993) found no validity effect when the target was presented after a short (100 ms) delay, and a larger than normal validity effect at a long (800 ms) delay. These results are consistent with a model of slowed reorienting of attention: the 100 ms cue-to-target delay gives persons with autism too little time to apply the information given by the cue, and as a result, there is no difference in reac- tion time between valid and invalid trials. Conversely, at the 800 ms delay, persons with autism, having had sufficient time to shift their attention to the cued location, must implement another slow shift in order to respond to a target at the uncued location. These abnormal validity effects in autism are overlaid on a pattern of overall slowed responding due to motor apraxia. The two effects, one a general slowing and the other an interaction with cue-to-target delay, can sometimes be difficult to separate. However, the autistic pattern of validity effects is present even when accuracy of dis- crimination is used as a measure instead of speed of response (Townsend et al., 1996), thus completely removing any motor confound. Although differences in diagnostic criteria, age groups, IQ and control groups make individual studies difficult to compare, the finding of dis- ordered control over the scope of attention in autism is in general cor- roborated by other studies. High-functioning adults with diagnoses of autism or Asperger syndrome show a difficulty distributing attention in order to detect targets at central and lateral positions (Wainwright-Sharp & Bryson, 1996). In low-functioning children with autism, an attention- directing frame around the relevant region of the visual field improves per- formance, but presentation of distractor stimuli within the frame negates 270 Downloaded from aut.sagepub.com at CAMBRIDGE UNIV LIBRARY on June 19, 2015 04belmonte (ds) 18/7/00 9:44 am Page 271 BELMONTE: ABNORMAL ATTENTION IN AUTISM this effect (Burack et al., 1997). In 10 adult savants with diagnoses of autism or PDD-NOS, Casey et al. (1993) found a heightened validity effect not only at the 800 ms cue-to-target delay but also at 100 ms, illustrating the potential for variability in results when diagnostic criteria are loose. Even more important than diagnostic stringency is the question of the eco- logical validity of the tasks employed: any experiment in which individual stimuli are presented in discrete trials separated by long pauses is a poor reflection of real-world tasks, which demand continuous reorienting of attention within a constant stream of stimuli. In a paradigm more reflective of the constant shifting demanded by real-world situations, Courchesne et al. (1994a) measured the accuracy of target detection in two simultaneously presented streams of information, one auditory and the other visual.A target in the currently attended modal- ity served as a cue to shift attention to the other modality. So, for example, a high tone in a background of low tones signalled subjects to stop attend- ing to tones and to begin watching for a red flash in a background of green flashes. On detecting the red flash, subjects had to begin ignoring the flashes and listening to the tones again. Adolescents with autism uncom- plicated by severe mental retardation (PIQ > 70) showed a deficit in responding to targets in different modalities when those targets were sep- arated by less than 2.5 seconds. A like result was obtained for the case of shifting between separate visual attributes (form and colour) of a single stimulus (Courchesne et al., 1994b). Reinforcing these results is the impairment of persons with autism at distributing attention across simul- taneous auditory and visual continuous performance tests (Casey et al., 1993). These complex tasks are an advance over single-trial paradigms in addressing the problem of ecological validity. However, behavioural methods are limited in their ability to relate task performance to the under- lying biology. Electrophysiological results on autism associate the aforementioned behavioural pathologies with abnormal modulation of excitability. In response to an attended stimulus, the normal brain produces a series of electrical potentials (voltages) which can be recorded from electrodes on the scalp. Over the frontal cortex, salient stimuli that call for responses or that differ from context during periods of sustained attention evoke nega- tive potentials.At more posterior scalp sites, attention modulates a series of potentials evoked by sensory stimuli. One of the earliest of these sensory potentials, the P1, is a positive voltage appearing over the occipital cortex about 100 ms after presentation of a visual stimulus. The P1 becomes gradually smaller as stimulation occurs farther away from the spatial focus of attention (Mangun and Hillyard, 1988). A later, negative potential over the parietal cortex, the N2, is augmented during attentional selection of 271 Downloaded from aut.sagepub.com at CAMBRIDGE UNIV LIBRARY on June 19, 2015 04belmonte (ds) 18/7/00 9:44 am Page 272 AUTISM 4(3) task-relevant stimuli (Eimer, 1996). Finally, at a latency of about 400 ms, a positive potential P3b appears with presentation of a task-relevant stimulus but not with irrelevant stimuli. Autism presents a remarkable disruption of all these attention-related potentials. Despite normal behavioural performance in tasks of static rather than shifting attention, frontal negativities are entirely absent (Ciesielski et al., 1990; Courchesne et al., 1989) and the visual P3b is highly variable (Courchesne et al., 1989) with a slightly low average amplitude (Ciesielski et al., 1990; Novick et al., 1979; Verbaten et al., 1991). The P1, instead of declining gradually with distance from the focus of attention, decreases either precipitously or not at all (Townsend and Courchesne, 1994). In addition to these failures of normal modulation, neural systems in the autistic brain often are inappropriately activated. The visual N2 to novel stimuli is larger when the person with autism is performing a task than when (s)he is passively observing, even when these novel stimuli are not relevant to the task in ques- tion (Kemner et al., 1994).
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