Elsevier

Cortex

Volume 48, Issue 6, June 2012, Pages 701-717
Cortex

Research report
High-frequency oscillatory response to illusory contour in typically developing boys and boys with autism spectrum disorders

https://doi.org/10.1016/j.cortex.2011.02.016Get rights and content

Abstract

Illusory contour (IC) perception, a fruitful model for studying the automatic contextual integration of local image features, can be used to investigate the putative impairment of such integration in children with autism spectrum disorders (ASD). We used the illusory Kanizsa square to test how the phase-locked (PL) gamma and beta electroencephalogram (EEG) responses of typically developing (TD) children aged 3–7 years and those with ASD were modulated by the presence of IC in the image. The PL beta and gamma activity strongly differentiated between IC and control figures in both groups of children (IC effect). However, the timing, topography, and direction of the IC effect differed in TD and ASD children. Between 40 msec and 120 msec after stimulus onset, both groups demonstrated lower power of gamma oscillations at occipital areas in response to IC than in response to the control figure. In TD children, this relative gamma suppression was followed by relatively higher parieto-occipital gamma and beta responses to IC within 120–270 msec after stimulus onset. This second stage of IC processing was absent in children with ASD. Instead, their response to IC was characterized by protracted (40–270 msec) relative reduction of gamma and beta oscillations at occipital areas. We hypothesize that children with ASD rely more heavily on lower-order processing in the primary visual areas and have atypical later stage related to higher-order processes of contour integration.

Introduction

Autism is a developmental disorder of neurological origin that is currently defined by behavioral criteria, which include impairments in social interaction, impairments in verbal and nonverbal communication, and restricted interests and activities. Although not included in the formal diagnostic criteria for autism or autism spectrum disorders (ASD), abnormalities of sensory perception are observed in the great majority of children with ASD and may significantly contribute to the development of the autistic phenotype (Gerrard and Rugg, 2009).

Sensory abnormalities in ASD have been most intensively investigated in the visual modality. People with ASD often have an uneven profile of visual abilities with both peaks and troughs in performance. They show deficit in tasks requiring Gestalt perception (Brosnan et al., 2004, Grinter et al., 2010) but demonstrate superior performance in a number of tasks relying on processing of local features, such as the embedded figures task (Jolliffe and Baron-Cohen, 1997), the block design subtest (Caron et al., 2006), visual search (Baldassi et al., 2009, Joseph et al., 2009) and first-order grating discrimination (Bertone et al., 2005).

The mechanisms underlying these perceptual atypicalities are still debated. Frith (1989) suggested that people with ASD have weak central coherence resulting in the inability to process information in global (gestalt) form. The reduced connectivity in the distributed cortical region was suggested to be the neural basis for the weak central coherence (Just et al., 2007). Updating the theory, Happe and Frith (2006) noted that the weak central coherence may result from local processing bias rather than a genuine inability to attend to global aspects of the stimulation (Happe and Frith, 2006). Mottron et al. (2006) further argued that the local processing bias in ASD stems from over-functioning of brain areas typically involved in primary perceptual functions without any additional deficits (Caron et al., 2006, Mottron et al., 2006). Indeed, functional magnetic resonance imaging (fMRI) studies reveal atypically strong activation in visual areas during performance of various tasks requiring visual processing (Ring et al., 1999, Sahyoun et al., 2010, Soulieres et al., 2009). There is also limited evidence of the role of underconnectivity in autistic visual perception (Belmonte et al., 2009).

The electroencephalographic studies have also suggested atypical neural correlates of visual perception in individuals with ASD. Vandenbroucke et al. (2008) found in adults with ASD abnormal early brain evoked responses related to visual boundary detection and contour segregation (Vandenbroucke et al., 2008). Several studies have revealed atypical modulation of the event-related potentials (ERP) by spatial frequency of visual stimulation in adults and children with ASD (Jemel et al., 2010, Milne et al., 2009, Vlamings et al., 2010). Webb et al. (2006) reported that ERP abnormalities in ASD depended on the social content (face vs object) of the visual stimulation (Webb et al., 2006).

Data on brain response to illusory contours (ICs) could significantly contribute to the existing neurofunctional evidence on atypical visual perception in ASD. ICs, such as the Kanizsa square illusion, are subjectively perceived boundaries without any physical differences at the border (Ramachandran, 1987). They provide a fruitful model for studying automatic perceptual grouping of local image features (Loffler, 2008, Seghier and Vuilleumier, 2006). Investigation of this phenomenon may shed the light on the origin of the atypical Gestalt perception in ASD.

Is perception of the ICs impaired in ASD? Two existing behavioral studies in children with ASD produced contradictory results. One of them reported the impaired perception of illusory figures in children with ASD (Happe, 1996), while the other did not find such a deficit (Milne and Scope, 2008). Even if children with ASD are able to perceive ICs, the underlying neurofunctional mechanisms may differ in ASD. Studies of neural activity related to IC perception may help to reveal putative distortion of perceptual grouping processes in ASD.

The perception of ICs involves activity modulations in multiple stages of the visual hierarchy [for review see (Nieder, 2002, Seghier and Vuilleumier, 2006)]. The findings suggest that processing of real and illusory contours is based on similar cortical mechanisms. Both real and illusory contours activate early stages of the monkey visual pathway (Grosof et al., 1993, Lee and Nguyen, 2001, Peterhans and von der Heydt, 1991, Sheth et al., 1996). In primary visual cortical area V1, the ICs trigger activity that differs from that elicited by the real contours (Ramsden et al., 2001). Psychophysical studies in humans further support the importance of the early areas in IC processing (Pillow and Rubin, 2002). Contrary, the human imaging studies unanimously suggest a wide network of predominantly higher order visual areas (Larsson et al., 1999, Murray et al., 2002). Based on these findings, Seghier and Vuilleumier (Seghier and Vuilleumier, 2006) concluded that processing of illusory figures engages several brain areas at early as well as intermediate and perhaps late stages in the visual hierarchy. Most likely, the perception of ICs involves a multitude of perceptual processes, some of which are instantiated in lower order areas of the visual cortex (e.g., collinearity processing), whereas others rely on higher order visual areas (e.g., amodal perceptual grouping and shape formation).

Recently, the authors of this paper employed the ERP technique to investigate neural correlates of IC processing in young boys with ASD and in typically developing (TD) boys aged 3–6 years (Stroganova et al., 2007). In TD boys, the illusory Kanizsa square, compared to a control stimulus, elicited enhanced negativity of the N1 peak in the evoked response: the IC effect. This IC effect has previously been described in healthy adults and is linked to intermediate perceptual grouping (Herrmann and Bosch, 2001). Boys with ASD demonstrated a significant inverted IC effect, i.e., more positive N1 amplitude to the IC. There is convincing evidence that the effect of enhanced positivity on the evoked response is related to low-order collinearity processing (Khoe et al., 2004). We suggest that TD boys relied upon intermediate perceptual grouping processing, whereas boys with ASD differentiated between the Kanizsa square and the control figure mainly using collinearity processing mechanisms implemented in the neural circuitry of the primary visual cortex (area V1). These findings provide the first tentative neurophysiological evidence for the superior role of early visual areas in processing coherent shapes in ASD and for the possible deficit in higher-level perceptual grouping.

It has been shown that gamma response is also strongly related to IC processing [for review, see (Herrmann et al., 2009)]. Therefore, investigation of gamma oscillations could provide additional information on Gestalt perception in ASD. High-frequency oscillations in the beta/gamma (approx. 15–60 Hz) range are thought to reflect an underlying temporal structure and coordination of neuron population activity. These oscillations play an important role in neural coding by assembly formation and may be associated with the binding of perceptual information [for review, see (Uhlhaas et al., 2009)]. Studies on gamma response to ICs in humans first evidenced the role of so-called induced gamma at the relatively late stage of processing (250–300 msec) (Tallon-Baudry et al., 1996). Tallon-Baudry et al. have shown that both illusory (i.e., Kanizsa) and real triangles are accompanied by an increase in non-[phase-locked (PL)] (i.e., induced) gamma activity compared to stimulus configurations with no triangle. The findings have led to the conclusion that the feature binding of an illusory figure is associated with an induced gamma response.

Pulvermuller et al., however, argued that perceptual processes occur much earlier and that the induced gamma response is related to cognitive associative learning rather than to perceptual processes per se (Pulvermuller et al., 1999). Indeed, analogous increases in induced gamma power accompanied awareness of visual stimuli independent of whether they were correctly discriminated (Summerfield et al., 2002). In a study similar to that of Tallon-Baudry et al., Herrmann et al. reported that the gamma response was mainly related to the illusory triangle being close in shape to a target in a discrimination task rather than to the presence/absence of the illusory triangle (Herrmann et al., 1999). Moreover, Yuval-Greenberg et al. argued that the late broadband transient-induced gamma band response recorded by scalp electroencephalography reflects properties of miniature saccade dynamics rather than neuronal oscillations (Yuval-Greenberg et al., 2008). Thus, the nature of the processes modulating the induced gamma power during Gestalt perception is still a question of debate. Currently, there is a growing body of evidence showing a relationship between short latency PL beta–gamma response and visual perception of coherent objects in the human brain (Spencer et al., 2004, Wu and Zhang, 2009).

The phase-locked gamma band response (plGBR) appears early (with latency of approx. 40–90 msec) after stimulus onset with high phase synchrony across the trials; its source is located near early sensory areas (Herrmann et al., 2010). The strong dependency of this response on the size or spatial frequency of the visual stimulus (Busch et al., 2004) implies that the plGBR is generated during an early processing stage, which is strongly affected by physical properties of the stimulation. On the other hand, the plGBR is modulated by attention (Stefanics et al., 2004) and familiarity (Herrmann et al., 2004), suggesting involvement of top–down influences.

This dual nature of plGBR makes it an ideal candidate for studying the putative imbalance in lower- and higher-level processing stages during Gestalt perception in ASD. Early PL sensory-evoked oscillations are most reliably found among the gamma oscillatory responses that make them especially suitable for searching putative abnormalities in clinical populations. Interestingly, in schizophrenia, a disorder associated with perceptual abnormalities similar to ASD, plGBR is strongly reduced and does not exhibit the normal enhancement during Gestalt perception (Spencer et al., 2004).

Converging evidence suggests that properties of high-frequency gamma and beta oscillations are altered in ASD and related to aberrant brain development in this disorder. The excess of gamma band oscillations during sustained visual attention in children with ASD is directly related to the degree of developmental delay (Orekhova et al., 2007). The stimulus-induced gamma oscillations in ASD are reduced (Grice et al., 2001) or abnormally modulated by the spatial frequency of simple visual stimuli (Milne et al., 2009). These considerations suggest possible alteration of the PL gamma response to ICs in ASD as well.

In this study, we analyzed PL gamma and beta responses to the IC in children with ASD and in TD children. Although the Kanizsa illusion effect on induced gamma response is already present in infants (Csibra et al., 2000), the PL high-frequency response related to IC processing was not investigated in pediatric samples. Therefore, we had two specific aims: (1) to explore PL gamma and beta responses to the Kanizsa square in TD children and (2) to look for their possible abnormalities in ASD children.

We used an experimental procedure similar to that described by Spencer et al. (Spencer et al., 2004) but with the two alterations. First, stimuli spanned a visual angle of 9° instead of approx. 7.5°. As the magnitude of plGBR is directly related to stimulus size (Busch et al., 2004), the larger stimuli may result in more reliable plGBR. Moreover, taking into consideration the relative disadvantage in processing low spatial frequencies in autism (Grinter et al., 2010), the putative gamma abnormalities could be more readily detected in ASD using large-size stimuli.

Second, in Spencer et al.’s study, subjects were asked to respond by pressing a button according to presence of the illusory square (Spencer et al., 2004); in contrast, we used a passive viewing task. The children’s attention toward the stimulus display was maintained by short animation movies interspersed with stimuli presentation. This design allows us to analyze the IC effect even in young and developmentally delayed children with ASD and to avoid the potentially confounding influence of decision-making processes on gamma response.

Section snippets

Participants

Two groups of children participated in this study: 23 boys with ASD aged 3–7 years [mean age = 60.4 months, standard deviation (SD) = 13.9] and 23 age-matched TD boys (mean age = 61.4 months, SD = 14.7). Of these 46 subjects, 18 boys with ASD and 16 TD boys were involved in a previous N1 study (Stroganova et al., 2007). Boys with ASD were recruited from local developmental disabilities departments and from psychiatry clinics. The control group comprised boys attending regular schools or daycare

The plGBR in TD boys

Time courses of plGBR to Kanizsa and control stimuli in TD children are shown in Figs. Fig. 2, Fig. 3. Repeated measures ANOVA showed highly significant effects of Time [F(9,198) = 14.91; ε = .35; p < .0001] and Area [F(1,22) = 22.25; p < .0001]. For both stimulus types, a plGBR was found within 270 msec after the stimulus onset with a strong peak at about 100 msec post-stimulus and response maximum at the occipital electrodes. ANOVA also yielded significant Stimulus X Time interaction [F(9, 198) = 2.77; ε = 

Discussion

This study investigates how IC processing is reflected in PL gamma and beta oscillations in TD children and children with ASD. We found that PL beta and gamma-band activity differentiated between IC and non-illusory stimuli in both ASD and TD boys. The high-frequency responses to IC were qualitatively different in the two groups. In TD boys, two distinct phases of PL high frequency response to IC were observed approximately corresponding to 40–120 msec and 120–270 msec after stimulus onset.

Funding

This work was supported by the Russian Fund for Basic Researches (grant 09-06-12042-ofi_m), the Ministry of Education and Science of the Russian Federation (project GK 02.740.11.0376), and the Swedish Research Council (project K2010-62X-2140-01-2).

Acknowledgments

We warmly thank all children and their parents for their participation.

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