The current study aimed at examining the neurocognitive basis of visuospatial vs. linguistic processing differences between high-functioning children with autism and typically developing controls. Our findings revealed that despite similar behavioral performances of the two groups, the underlying structural and functional neuroanatomy were significantly different between HFA and CTRL.
The two groups did not differ in accuracy or response times on the task, supporting the view that HFA have intact visuospatial processing skills (Dakin & Frith, 2005
; Edgin & Pennington, 2005
), and intact pictorial access to semantics (Kamio & Toichi, 2000
). Although non-significant, we noted a qualitatively lower accuracy of the HFA group in the S than in the V and V+S conditions, consistent with a trend for a difference in verbal IQ between the groups. As children with autism typically do worse under language processing conditions (Rapin & Dunn, 2005; Sahyoun et al, 2009
; Tager-Flusberg, Lindgren & Mody, 2008
), this may help in the interpretation of some of the brain activation differences found in our HFA participants.
We found that regardless of the differing linguistic versus visuospatial demands of the task, pictorial reasoning engaged a similar, largely overlapping network of cortical regions in both groups. This core network comprised of areas related to language processing (TPJ, supramarginal gyrus, STS, MTG, IF), visuospatial manipulations (IPS, superior precentral sulcus), and visual processing and picture identification (occipital cortex, ventral temporal stream). Regions known to be involved in visuospatial processing were more active during V and V+S than in S (Ecker et al., 2008
; Klingberg, 2006
; Zacks, 2008
), and language-processing areas were more active and often, more anterior (suggesting more conceptual coding) (Gold & Buckner, 2002
) in S and V+S than in V.
The two groups, however, clearly differed in their activation profiles. Whereas CTRL appeared to engage fronto-temporal areas when verbal mediation was available and/or necessary, as in the V+S and S conditions, HFA relied more on posterior, occipito-temporal and ventral temporal, brain areas, evident in the within-group fMRI comparisons. Compared to the control group, HFA’s poorer frontal activation in S and V+S than in V (), and greater activation of IPS, especially in V+S (), together with its reduced structural connectivity between frontal and ventral temporal areas (), suggest an impaired frontal language system and greater reliance on visual mediation via inferior parietal and ventral temporal areas to do the task. This could account for the absence of significant difference between the groups in behavioral performance, reflecting an intact visually-mediated access to semantics in a pictorial reasoning task like the one used in the present study.
That both CTRL and HFA participants showed greater activation of the occipito-temporal and ventral temporal areas in the S and V+S conditions than in V, implies more of a conceptual than structural coding of pictorial stimuli by both groups; however, the CTRL group also showed greater activation in language areas, STS and IF, for S and V+S than V. A direct contrast between CTRL and HFA in the S condition revealed greater activation in CTRL in the left STS/MTG and right supramarginal gyrus, as well as in right angular gyrus in the V+S condition in keeping with their tendency to use semantic and visuospatial information, when both processing routes are available (Sahyoun et al., 2009
). These results also suggest that control subjects may engage an extended network of language areas, including right hemisphere homologues, during tasks that involve linguistic (semantic and/or verbal
) mediation (Harris et al., 2006
In striking contrast to the increased activation in the CTRL group within the language network in S and V+S, the HFA group showed increased activation in these conditions in left IPS and occipital cortex. This pattern of increased reliance on posterior processing areas has been associated with “structural” coding of information (Kellenbach, Hovius, & Patterson, 2005
) and with a cognitive use of
visual strategies in problem-solving in autism (Manjaly et al., 2007
; Soulières et al., in press
). The HFA group also showed increased activation in all three conditions in the left hemisphere lateral occipito-temporal sulcus, and pre- and post-central sulci, which have been implicated in visuospatial transformations (Ecker et al., 2008
); in contrast, the CTRL group showed greater activation in all conditions in left hemisphere MTG and lingual gyrus which may reflect greater processing of semantic attributes of the stimuli in CTRL. The superior precentral sulcus was also consistently activated in this group. Given its location in what might be functionally defined as the frontal eye field, the activation in the superior precentral sulcus warrants a closer investigation of eye movements and potential differences in visual search strategies between HFA and CTRL.
The results of our tractography analysis provide a window into the structural basis for the activation differences in pictorial reasoning between HFA and CTRL. Connections between the FG and IPS and FG and STS/MTG were intact in both hemispheres in the HFA group (, ), consistent with accounts of a reliance on visuospatial processing abilities and intact pictorial access to language in autism. These results also highlight an important mediating role for the FG in higher-level cognition in autism. The HFA group, however, showed reduced FA compared to CTRL in the IF-FG pathways in both hemispheres (Koshino et al., 2008
; Lee et al., 2007
), consistent with lower functional activation of the IF in semantic processing observed in this group, relative to CTRL, and in keeping with accounts of decreased use of covert speech strategies in autism (Kana et al., 2006
). In addition, HFA participants showed lower FA compared to CTRL in the right hemisphere IF-MTG pathway, consistent with our finding that CTRL but not HFA may engage the right frontal areas as part on an extended language network. Surprisingly, we did not find reduced fronto-parietal connectivity, or left hemisphere IF-STS underconnectivity, seen in some studies (Just et al., 2004
; Kennedy & Courchesnes, 2008
). These studies used functional correlations between activated areas, and assess connectivity using a different (i.e., indirect) approach (Hughes, 2007
), making it difficult to compare results across the studies. Insofar as functional underconnectivity may be associated with altered grey matter, white matter, or both, with little information about potential cytoarchitectural underpinnings (Kleinhans et al., 2008
), recent methods, including DTI, could allow one to examine the potential correspondence between functional and anatomical connectivity (Just et al., 2006). It is worth noting that the present tractography approach averages FA over large pathways, such that some localized differences in white matter integrity may not be detected, as these may lie primarily within the tails of the FA distributions (Ciccarelli et al., 2006
). Further developments in quantitative tractography, such as point-by-point comparisons along pathways (Salat et al., 2008
), may provide better sensitivity to localized differences and help reconcile differences between functional and structural connectivity findings.
In conclusion, the neuroimaging results from the present study on pictorial reasoning suggest that individuals with autism may favor the use of visual mediation strategies in tasks of higher cognition. The HFA recruited posterior brain regions particularly the occipital and ventral temporal areas and the intraparietal sulcus, related to visuospatial processing. The typically developing group, in contrast, relied more on a fronto-temporal language network for reasoning. This pattern was consistent with differences in white matter integrity: HFA showed intact connections between ventral temporal areas and posterior language and visuospatial processing regions, but reduced connectivity with inferior frontal areas.