Cortical underconnectivity coupled with preserved visuospatial cognition in autism: Evidence from an fMRI study of an embedded figures task

Abstract

Individuals with high-functioning autism sometimes exhibit intact or superior performance on visuospatial tasks, in contrast to impaired functioning in other domains such as language comprehension, executive tasks, and social functions. The goal of the current study was to investigate the neural bases of preserved visuospatial processing in high-functioning autism from the perspective of the cortical underconnectivity theory. We used a combination of behavioral, functional magnetic resonance imaging (fMRI), functional connectivity, and corpus callosum morphometric methodological tools. Thirteen participants with high-functioning autism and thirteen controls (age-, IQ-, and gender-matched) were scanned while performing an Embedded Figures Task (EFT). Despite the ability of the autism group to attain behavioral performance comparable to the control group, the brain imaging results revealed several group differences consistent with the cortical underconnectivity account of autism. First, relative to controls, the autism group showed less activation in left dorsolateral prefrontal and inferior parietal areas and more activation in visuospatial (bilateral superior parietal extending to inferior parietal and right occipital) areas. Second, the autism group demonstrated lower functional connectivity between higher-order working memory/executive areas and visuospatial regions (between frontal and parietal-occipital). Third, the size of the corpus callosum (an index of anatomical connectivity) was positively correlated with frontal-posterior (parietal and occipital) functional connectivity in the autism group. Thus, even in the visuospatial domain, where preserved performance among people with autism is observed, the neuroimaging signatures of cortical underconnectivity persist. KeywordsEmbedded figures task; Functional connectivity; Corpus callosum; functional MRI One of the enigmatic aspects of autism is that people with the disorder exhibit preserved or even enhanced performance on visuospatial tasks (Baron-Cohen & Hammer, 1997;Brian & Bryson, 1996;De Jonge et al., 2006;Jolliffe & Baron-Cohen, 1997;Lee et al., 2007;Manjaly et al., 2007;Mottron et al., 1999;Ring et al., 1999;Shah & Frith, Shah and Frith (1983) demonstrated that children with high-functioning autism exhibited superior performance relative to IQ-and age-matched controls on the Embedded Figures Task (EFT), in which individuals are asked to locate a simple figure that is embedded in a more complex configuration.A recently proposed theoretical account of autism, the cortical underconnectivity theory (Just et al., 2004;, provides a neurobiological explanation of the psychological processes underlying the disorder. This theory posits that autism is a neural systems disorder marked by inefficient interregional brain connectivity between frontal and posterior areas resulting in a deficit in integration of information at both psychological and neural levels. The theory predicts that if a task does not require tight integration between frontal and more po...

Impact of IQ Discrepancy on Executive Function in High-Functioning Autism: Insight into Twice Exceptionality

“…There is an ongoing discussion in the literature as to whether weak central coherence is necessarily a deficit . While it has been demonstrated through neuroimaging that frontal language areas are underconnected in autism (Damarla et al 2010;Washington et al 2010;Just et al 2007), this behavioral data converges to an underlying question about the role of language ability in highability HFA and its candidacy as a mechanism of support for EF in high-ability HFA. On the surface, one possible explanation for the emphasis on MI stems from the fact that it has twice as many items as the BRI and thus greater power.…”

Visuo-Spatial Performance in Autism: A Meta-analysis

“…These findings suggest that individuals with ASD did not require as many resources as TD individuals in order to achieve the same level of performance, which supports the idea of superiority of Figure Disembedding in individuals with ASD. Furthermore, the fMRI study conducted by Manjaly et al (2007) utilized a different control task than the previous two studies, and concluded that the ASD group showed enhanced local processing in visual areas, a conclusion supported by Damarla et al (2010). Silk et al (2006) investigated activity levels in frontoparietal networks during Mental Rotation.…”

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“…Three recent studies (Damarla et al 2010;Lee et al 2007;Manjaly et al 2007) made use of functional Magnetic Resonance Imaging (fMRI) during a Figure Disembedding task. While none of these studies found performance differences between ASD and TD groups, differential brain activation was observed.…”

Brain dynamics in ASD during movie‐watching show idiosyncratic functional integration and segregation

“…Accordingly, coordinated processing between separate brain regions, known as functional connectivity (FC), that is, typically quantified by correlational measures of statistical interdependency (Friston, 1994), has been assessed in resting‐state (Di Martino et al, 2014; Gotts et al, 2012; Supekar et al, 2013) and in a variety of tasks probing speech comprehension (Just, Cherkassky, Keller, & Minshew, 2004), visuomotor performance (Mizuno, Villalobos, Davies, Dahl, & Müller, 2006; Turner, Frost, Linsenbardt, McIlroy, & Müller, 2006; Villalobos, Mizuno, Dahl, Kemmotsu, & Müller, 2005), visuospatial abilities (Damarla et al, 2010; Liu, Cherkassky, Minshew, & Just, 2011), face processing (Kleinhans et al, 2008; Rudie et al, 2012), or executive functions (Just, Cherkassky, Keller, Kana, & Minshew, 2007; Kana, Keller, Minshew, & Just, 2007; Koshino et al, 2008). The big picture emerging from those reports is lowered FC between frontal and posterior brain regions (see Vissers, Cohen, & Geurts, 2012 for a review), as formulated in the underconnectivity theory of autism (Just, Keller, Malave, Kana, & Varma, 2012).…”