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Autism

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

Matthew Belmonte Autism 2000 4: 269 DOI: 10.1177/1362361300004003004 The online version of this article can be found at: http://aut.sagepub.com/content/4/3/269

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The National Autistic Society

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Abnormal attention in autism shown by steady-state visual evoked potentials

M AT T H E W B E L M O N T E
Centre, Belmont, MA, USA McLean Hospital Brain Imaging

autism 2000 SAGE Publications and The National Autistic Society Vol 4(3) 269285; 013642 1362-3613(200009)4:3

K E Y WO R D S

This study examined brain electrical responses as a physiological measure of speed and specicity of attentional shifting in eight adult males with autism. Subjects were required to shift attention between rapidly ashed targets alternating between left and right visual hemields. When targets were separated by less than 700 ms, steadystate brain electrical response in both hemispheres was augmented and background EEG decreased for rightward shifts as compared with leftward shifts. At longer separations, persons with autism showed no modulation of background EEG, and high variability in steady-state 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 signicant 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 reect the operation of a non-specic mechanism of sensory gating.
A B S T R AC T ADDRESS

asymmetry; EEG; spatial attention; steady-state evoked potential; vision

Correspondence should be addressed to: M A T T H E W B E L M O N T E , MIT 14E-303, 77 Massachusetts Avenue, Cambridge, MA 02139-4307, USA

The ability to attend to relevant stimuli and to lter 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 parents voice, facial expression and gestures in response to the infant and the toy. In order to integrate all these stimuli into coherent 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

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4(3) studies suggest that this decit in attentional control reects a lack of specicity in perceptual gating, that is, in the process of selecting a few relevant 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 subsequently 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 benet of valid cueing. In a high-functioning group of adolescents and young adults with diagnoses of autism or Asperger syndrome, 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 reaction time between valid and invalid trials. Conversely, at the 800 ms delay, persons with autism, having had sufcient 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 difcult to separate. However, the autistic pattern of validity effects is present even when accuracy of discrimination 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 difcult to compare, the nding of disordered control over the scope of attention in autism is in general corroborated by other studies. High-functioning adults with diagnoses of autism or Asperger syndrome show a difculty distributing attention in order to detect targets at central and lateral positions (Wainwright-Sharp & Bryson, 1996). In low-functioning children with autism, an attentiondirecting frame around the relevant region of the visual eld improves performance, but presentation of distractor stimuli within the frame negates
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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 ecological validity of the tasks employed: any experiment in which individual stimuli are presented in discrete trials separated by long pauses is a poor reection of real-world tasks, which demand continuous reorienting of attention within a constant stream of stimuli. In a paradigm more reective 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 modality 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 attending to tones and to begin watching for a red ash in a background of green ashes. On detecting the red ash, subjects had to begin ignoring the ashes and listening to the tones again. Adolescents with autism uncomplicated by severe mental retardation (PIQ > 70) showed a decit in responding to targets in different modalities when those targets were separated 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 simultaneous 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 underlying 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 negative 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

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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 question (Kemner et al., 1994). This inappropriate activation occurs across modalities also: when a response is required to an auditory stimulus, autistic children manifest an enhanced P3 at occipital sites overlying visual processing areas (Kemner et al., 1995). Perceptual gating in autism seems to occur in an all-or-none manner, with little specicity for the location of the stimulus, for the behavioural relevance of the stimulus, or even for the sensory modality in which the stimulus appears. Lacking normal mechanisms for gating sensory signals into higher-order processing, the autistic brain seems to accomplish attentional tasks by some other, substitute mechanism. The aforementioned studies have assessed statically allocated attention, but by themselves they have little to say about what goes on in the autistic brain when a demand is made to shift attention. The application of evokedpotential methods to such shifts is not straightforward, since the most obvious electrophysiological indications of a shift in attention appear only after the shift has occurred. A cue to shift attention evokes a P3 response, but this response cannot be closely associated with the attentional shift itself since in normal subjects the shift is already fully implemented when the P3 is only just beginning. The P700 shift-difference (Sd) potential appears specically in circumstances in which an attentional shift has occurred (Akshoomoff and Courchesne, 1994), but again, it can furnish only retrospective information on the process of attentional shifting. One way around this problem is to use perturbations of a steady-state visual evoked potential (SSVEP) as an index of attentional modulation. The SSVEP is an electrical resonance of the visual system, produced when stimuli are ashed periodically at frequencies in the alpha band (Regan, 1977). Just as the height attained by a childs swing grows large if the swing is pushed at appropriate intervals, the voltage generated by the visual system
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grows large if a visual stimulus is ashed at a resonant frequency, about 10 times per second. The backward and forward swings are synchronized to the pushes, just as the SSVEP voltage peaks are phase-locked to the ashing stimulus. In normal subjects, the SSVEP is augmented in the hemisphere contralateral to the attended visual hemield (Belmonte, 1998; Morgan et al., 1996). Conversely, background oscillations occurring in the same frequency band as the SSVEP, which are not phase-locked to the stimulus and probably index the level of task-irrelevant processing, are decreased contralateral to the attended hemield (Belmonte, 1998). When a subject is asked to shift attention across the midline, the pattern of SSVEP modulation inverts beginning at about 300 ms (Belmonte, 1998). The hypothesis of non-specic sensory gating in autism predicts an absence of hemispheric specicity in the modulation of the SSVEP and of background amplitude during rapid attentional shifts. Instead of being modulated in opposite directions, amplitude measures in the two hemispheres should be similar to each other when the stimulus onset asynchrony (SOA) between the cue in the previously attended location and the target in the newly attended location is brief. At longer SOAs, when people with autism are not so drastically impaired, a pattern of modulation similar to normal may emerge, but with a prolonged latency reecting the prolonged time course of the attentional shift.

Methods
The eight autistic subjects were members of a long-standing subject pool recruited from a regional centre for developmental disabilities and from clinical referrals.All the autistic subjects were male, with a mean age of 26.7 years and a standard deviation of 5.4 years (range 19.4 to 32.3). Of these, seven were right-handed and one was left-handed. None were medicated, and none had any history of comorbid psychiatric disease. The diagnosis of autism was made by experienced clinicians, including a clinical psychologist and a paediatric neurologist, according to the structured observations of the Autism Diagnostic Observation Schedule (ADOSG) (Lord et al., 1989). In addition, all subjects were administered the Wechsler Adult Intelligence ScaleRevised and the Childhood Autism Rating Scale (CARS) (Schopler et al., 1988), and each subjects parent was interviewed with the Autism Diagnostic InterviewRevised (ADIR) (Lord et al., 1994). Table 1 summarizes these behavioural measures. In all eight cases the DSMIV (American Psychiatric Association, 1994) criteria were met according to both the ADIR and the ADOS. All subjects with autism were negative for fragile X, as assayed by cytogenetic analysis. The controls were 12 normal, 273

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4(3) right-handed subjects with no history of neurological or psychiatric disease, ve female and seven male, mean age 22.9 years, standard deviation 4.1 years, range 17.4 to 30.3, recruited from among local college students and hospital employees. (Constraints on resources prevented matching the two samples by sex; however, effects in the normal females were highly similar to those in the normal males both for the SSVEP (F(1,10) = 0.02, p = 0.89) and for background activity (F(1,10) = 0.13, p = 0.73).) Informed consent was obtained from each subject. All subjects were paid for their time. The paradigm was identical to that used in our previous work on attentional shifts in normal subjects (Belmonte, 1998) and consisted essentially of two oddball detection tasks running side by side. Stimuli were coloured squares, 1.8 on each side, centred 3.0 superior and 5.1 lateral to a xation cross. Each square was ashed for 56 ms and was followed by another 56 ms of blank display, producing an SSVEP with a 112 ms cycle (8.9 s1). On detecting a target in the currently attended location, subjects had as rapidly as possible to move a joystick to the opposite side and to shift their attention to that opposite side. Stimuli were presented in 144 trials, and ran continuously within each trial. Each trial contained 32 targets and was about 50 s in duration. Fixation was monitored by electrooculography and by closed-circuit television. Both detection accuracy and response latency were recorded as behavioural measures. Although the latter measure is subject to inuence by delays in motor implementation, the former depends solely on detection and not on the speed of motor implementation. Before EEG recording began, subjects were observed during practice trials until it was clear that they were performing the task as instructed. In addition, the behavioural data serve as an ongoing check for appropriate performance of the task. Owing to the small size of the scalp region of interest, a uniformly sized electrode array was applied to all subjects regardless of variation in head shape. Within such small regions, it has been our experience that errors introduced during the process of electrode placement are comparable to the small errors introduced by variation in head circumference. Ag-AgCl electrodes, 1 cm in diameter, were placed on each hemisphere along three parallel lines 1.5 cm, 3.5 cm, and 5.5 cm superior to the line joining the inion and the preauricular point. On the upper and lower lines, electrodes were placed 4 cm and 8 cm lateral to the midline. On the middle line, electrodes were placed 6 cm lateral to the midline. This scheme produced, over each hemisphere, one central electrode located over occipitoparietal scalp and surrounded by four equally spaced neighbours at a radius of 2.8 cm. EEG was recorded at a sampling rate of 286 s1 (i.e. 32 samples during each 112 ms cycle of the ashing stimulus) using Scan386 digitization
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Table 1 Subjects age, WAISR performance IQ, Childhood Autism Rating Scale score, and subscores from the Autism Diagnostic InterviewRevised for reciprocal social interaction, communication (verbal and non-verbal items), and restricted and repetitive behaviours and interests PIQ CARS ADIR social ADIR communication (verbal) 22 16 20 21 20 22 20 27 21.0 (3.1) 12 8 14 14 14 12 13 13 12.5 (2.0) ADIR communication (non-verbal) ADIR restricted & repetitive 11 7 10 7 6 10 6 12 8.6 (2.4)

Subject

Age

1 2 3 4 5 6 7 8 90.4 (19.9) 36.0 (6.5) 27.6 (7.7)

32 31 19 31 29 31 20 20

93 112 81 80 92 106 108 51

42.5 23.5 35.5 32.5 36.5 36 45 36.5

29 22 45 25 26 21 30 23

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Mean (SD)

26.6 (5.8)

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4(3) software (Neuroscan, El Paso, Texas) and a Scientic Solutions analogueto-digital converter with a Grass Model 12 Neurodata Acquisition System. Half-amplitude cutoffs were 0.1 s1 and 100 s1. Bipolar derivations were transformed off-line into a measure consisting of four times the voltage at the central electrode minus the voltages at each of the four neighbours. This procedure emphasizes sources that underlie the centrally placed electrode and diminishes effects of volume conduction (Hjorth, 1975). EEG intervals in which the range of the median-ltered horizontal electrooculogram exceeded 25 V within 75 ms were rejected. A similar procedure was applied in the case of the vertical electrooculogram with a threshold of 100 V in 300 ms. These rejection parameters were selected based on their reliable identication of horizontal saccades and eyeblinks, respectively, in pilot data. Using the Gnuroscan system (Belmonte, 1997), a set of extensions to the Neuroscan software, artefact-free intervals consisting of the 900 ms epoch following correctly detected targets were averaged into four separate bins depending on the amount of time since the previous correctly detected target: 56728 ms, 8401512 ms, 16242296 ms, and 2408 ms or longer. Since 2296 ms was the longest possible interval between target presentations, the 2408 ms bin contained only responses that followed at least one missed target. For each of the eight successive 112 ms periods within this epoch, SSVEP and background amplitudes were derived from the Fourier transform (Mast and Victor, 1991), and the difference between amplitude in response to left targets and amplitude in response to right targets was computed. Each of the two sets of behavioural measures (latency and accuracy) was subjected to a 2 4 2 analysis of variance (BMDP program 2V) with factors diagnostic group, SOA and target location. Each of the two sets of electrophysiological data (SSVEP and background) was subjected to a 2 4 2 8 analysis of variance with factors diagnostic group, SOA, target location and latency.
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Results
For the SSVEP data, analysis of variance revealed an effect of SOA group (F(3, 54) = 3.06, p = 0.0359). Group effects on background amplitudes were more pronounced than those on the SSVEP itself, owing to less variability in the data: for the background amplitudes there were strong effects of latency group (F(7, 126) = 6.38, p < 0.0001) and of SOA latency group (F(21, 378) = 3.57, p < 0.0001). The complete data set is expressed graphically in Figure 1; for cells that contribute heavily to these statistical effects, means and standard errors are given in the text below. 276

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Since the quantity represented is the difference in amplitude between left targets (which cue rightward shifts) and right targets (which cue leftward shifts), positive values indicate greater response to left targets and negative values indicate greater response to right targets. At short SOAs, people with autism showed much greater SSVEP response to left targets (rightward shifts) than to right targets (leftward shifts), beginning at about 500 ms post-target (Figure 1, column 1, bottom two panels). This heightened response occurred in both hemispheres, but

Figure 1 Difference amplitudes of background EEG and of the phase-locked SSVEP, computed at 112 ms intervals in each hemisphere following the presentation of a successfully detected target. Signal in response to right targets (leftward shifts) is subtracted from signal in response to left targets (rightward shifts). Solid lines and circles, normals. Dotted lines and squares, autism. Averages are plotted for four different ranges of SOA. Error bars represent standard error of the mean. At short SOA, note the similar patterns of activation in left and right hemispheres for autism but not for controls

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4(3) was more consistent in the right hemisphere: for the 56728 ms SOA range, at 600 ms post-target, right-hemisphere mean difference amplitude was 6.8 6.5 V for people with autism versus 1.4 0.8 V for controls, while the left-hemisphere means were 3.3 4.9 V for autism and 0.1 0.4 V for controls. (All ranges are standard error of the mean.) In contrast to this large, bihemispheric effect in autism, the normal pattern of SSVEP modulation consisted of a small leftright difference that increased (i.e. became greater for rightward shifts) in the left hemisphere but decreased (i.e. became greater for leftward shifts) in the right hemisphere. People with autism did not manifest such separate and opposite effects in the two separate hemispheres; instead, the hemispheres behaved similarly to each other, each responding more highly during rightward shifts than during leftward shifts. SSVEP differences at long SOAs (lower right quadrant of Figure 1) were highly variable in the autistic subjects, oscillating between positive and negative signs. For SOA 2408 ms, right-hemisphere mean difference amplitude at 600 ms was 14.0 13.2 V for autism versus 2.4 1.1 V for controls. The corresponding values for the left hemisphere were 6.1 5.7 V and 0.1 0.5 V. These large and disordered amplitudes in the case of autism were utterly dissimilar to the normal pattern in which well dened and oppositely directed modulations in the two hemispheres are evident as early as 300 ms post-target. In the background (non-phase-locked) EEG, at short SOAs people with autism showed strongly decreasing response to left targets (rightward shifts) and increasing response to right targets (leftward shifts) (Figure 1, column 1, top two panels). Again the direction of the effect was the same in both hemispheres. The control subjects, in contrast, manifested a weak, decreasing leftright difference in the left hemisphere but a stronger, increasing trend in the right hemisphere. For the 56728 ms SOA range, by 700 ms post-target the mean leftright difference had fallen to 0.89 0.37 V in autism as compared to 0.32 0.26 V in controls, in the right hemisphere; and to 0.75 0.65 V for autism as compared to 0.03 0.07 V for controls, in the left hemisphere. At longer SOAs, this pattern of bihemispheric decrease in difference amplitude of the background EEG disappeared and, in the case of the right hemisphere, amplitude became high in response to left targets (rightward shifts) throughout the epoch (column 2, panel 2). For the 8401512 ms SOA range, by 300 ms post-target the amplitude in controls was 0.44 0.17 V, whereas in autism it had increased to 0.54 0.40 V. In addition, right-hemisphere background amplitude modulation that was quite pronounced in control subjects in the two longest SOA ranges was utterly absent in autism (columns 3 and 4, panel 2). For SOA 2408 ms,
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Figure 2 Accuracy ratios and response latencies for various SOAs. Solid lines and circles, normals. Dotted lines and squares, autism. Error bars represent standard error of the mean. At short SOAs, note the greater impairment in accuracy yet faster response times for correctly detected targets

difference amplitudes in controls climbed from 0.55 0.22 V at 400 ms post-target to 0.56 0.26 V at 700 ms post-target, whereas for people with autism the amplitudes remained at, from 0.09 0.22 V at 400 ms to 0.0 0.08 V at 700 ms. The behavioural data are displayed in Figure 2. As expected, there were highly signicant effects of SOA on accuracy (F(6, 66) = 43.27, p < 0.0001) and on response latency (F(6, 66) = 3.49, p = 0.0047). The ratio of correct target detections to total number of detection opportunities was lower for the autistic group than for the normal group (0.58 0.04 for autism and 0.77 0.06 for controls, F(1, 18) = 6.48, p = 0.0203), and attained its maximum at a longer SOA (SOA group effect, F(6, 108) = 9.53, p < 0.0001). The response latency also was greater for the autistic group (728 43 ms for autism and 500 20 ms for controls, F(1, 18) = 24.21, p = 0.0001), and decreased more rapidly with increases in SOA (SOA group effect, F(6, 108) = 4.01, p = 0.0012). Interestingly, the response latency was somewhat lower for correctly detected targets in the shortest SOA range than for the next shortest. 279

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Discussion
Because the autistic and normal groups involved in this study were not closely matched for age, IQ or gender, the results reported must be considered as tentative at this stage. However, these results indicate that in autism there is an abnormal modulation not only at short SOAs as predicted by the hypothesis of non-specic sensory gating, but also at longer SOAs. This latter nding is remarkable given the relatively intact behavioural performance of persons with autism at these longer SOAs. Physiological abnormality at longer SOAs is consistent, however, with electrophysiological evidence showing lack of frontal negativities and diminished P3b response even where behavioural performance is unimpaired, and suggests that the autistic brain implements attentional processing via a mechanism different than that of the normal brain. When persons with autism had only a short amount of time in which to reorient attention (short SOAs), they performed less accurately by behavioural measures, and electrophysiological measures of SSVEP and background EEG amplitudes indicated a failure of the two hemispheres to operate independently: in both hemispheres the SSVEP was much more responsive to rightward shifts than to leftward shifts, and in both hemispheres the background EEG decreased during rightward shifts and increased during leftward shifts. These electrophysiological results are consistent with other reports of loss of hemispheric specialization in autism (Dawson and Lewy, 1989; Chiron et al., 1995), and suggest that in autism a generalized arousal substitutes for the normal brains more ne-grained, spatiotopically specic pattern of activation. This high level of generalized arousal may account for the autistic subjects combination of low accuracy and especially quick response times at short SOAs: if a person with autism is able to distinguish the target from the rest of the ood of sensory data, the response to that target occurs with a very low threshold. Activation patterns at longer SOAs suggest a lack of functional specificity of attention, in addition to the aforementioned failure of spatial specificity. At longer SOAs persons with autism had more time to reorient, and performed more accurately but still not quite at the level of the controls. The lack of modulation of background EEG and the high variability in the SSVEP under these conditions suggest that irrelevant processing is not appropriately supressed and that relevant stimuli are not reliably selected. It thus becomes difficult for the person with autism to pick out and to act upon task-relevant stimuli. The variability in the SSVEP data is interesting in light of suggestions that autism may be viewed functionally as a sort of dysmetria of thought (Courchesne and Allen, 1997), in which reciprocal connections with subcortical structures fail to tune 280

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cortical excitability appropriately for the current sensory inputs and behavioural set. Group social activities present many simultaneous signals, between which attention must be switched effortlessly and rapidly. In a conversation, information is transferred not only in the text of the dialogue but also in tone of voice (auditory), facial expression (visual), gesture (peripheral visual), and reference to third parties or to external objects or events (peripheral auditory and visual). Without the ability to integrate rapidly stimuli in separate modalities and spatial locations, the everyday task of constructing a coherent mental narrative of the external world becomes nearly impossible. Many persons with autism have reported episodes of sensory overload that prevent their processing any inputs at all. Sounds can become painfully intense, and visual stimuli can become whited out. The electrophysiological ndings reported here reveal that the autistic brain attempts to compensate for impaired attention by applying a much coarser, ersatz mechanism of sensory gating: instead of the normal spatially and functionally specic enhancement of sensory processing, there is a generalized, non-specic arousal that heightens response to all stimuli. It is quite remarkable that persons with autism are able most of the time to sort through the resulting cacophony. When such generalized hyper-arousal is uncontrolled, sensory overload may be the result. The use of steady-state potentials to quantify attentional modulation of sensory input is a technique previously untried in clinical populations, and its application in this study was restricted to a narrowly dened, largely high-functioning group of adult men with autism. Moreover, the autistic and control groups differed in terms of gender ratio and, because of constraints and resources, it was not possible to make them on the basis of age and IQ. This study should therefore be regarded as a preliminary report, and general conclusions should be approached with caution. Although there were no detectable differences in attentional processing between male and female controls, the same is not necessarily true of people with autism: autistic males as a group are more severely impaired in early social development than are autistic females (McLennan et al., 1993), and this behavioural distinction may reect a quantitative or even qualitative difference in the process of attentional control. A similar distinction may exist between the high-functioning subjects studied here and persons whose autism is complicated by severe mental retardation. Furthermore, even within our diagnostically homogeneous group of high-functioning male subjects, physiological subgroups may exist, and the presence of such subgroups may have been masked by high variability in the data combined with a small sample size. 281

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4(3) Although this study sheds light on the physiological basis of attention in adults with autism, it does not address the developmental processes of which this adult physiology is the end result. It is known that the neurochemistry of the child with autism changes during development (Chugani et al., 1999). As corresponding differences in neurophysiology are to be expected, the extension of this electrophysiological work to children with autism would be of interest. In light of physiological studies, the autistic obsession with replicable, patterned sensory stimulation becomes explicable as a consequence of attentional dysfunction: any human being confronted with such a profound difculty in integrating the many separate elements of a complex stimulus will naturally gravitate to simple stimuli that can be repeated or replayed over and over again. It is only by imposing such limits that persons with profound impairments in the shifting of attention can make sense of the world. Thus, many autistic behaviours can be understood as the products of a normal human mind confronted with a highly abnormal sensory experience. Historically in the eld of autism, biological studies and the development of behavioural interventions have proceeded independently of each other. This has been a loss, since physiology supplies a unique window onto the ways in which persons with autism process information. Educational and social approaches to people with autism must take these biologically based strengths and weaknesses into account. In particular, they must endeavour to avoid rapid presentation of information in disjointed spatial locations or in different sensory modalities, since the integration of such complex sensory stimuli demands a level of attentional control physiologically impossible for people with autism. This study adds a new type of electrophysiological evidence to the growing body of ndings indicating abnormal shifting and distribution of attention in autism. In the future, it will be important to localize these shiftrelated activations and thus to ascertain what anatomical regions and functional networks are responsible for the spatiotopically and functionally non-specic pattern of activation seen in autism. In the long term, this information will inform behavioural and pharmacological interventions, and point the way to an understanding of the abnormal neurological development that leads to autistic perception and behaviour.
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Acknowledgements I thank Eric Courchesne for access to his laboratory, Alan Lincoln for diagnostic data, Brian Egaas and Greg Allen for helpful discussions, Robert Ringrose for computing facilities, and Marissa Westereld for invaluable
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assistance in conducting the experiments. Most importantly, thanks are due to the people with autism who volunteered to participate in this study.

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