Chapter 20, DTI and Tractography in the Autistic Brain
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Figure 4. Correlations between gyrification and short-range connectivity within the group of patients with ASD. Partial correlations accounting for age, gender and total number of streamlines were conducted between l GI in the cluster of between-group differences and the number of intra-lobar streamlines in the lobe where most of the cluster was located. Significant positive correlations were observed only in the corresponding lobe dashed lines report non-significant relationships.
Results of the exploratory correlations between clinical scores at the ADI and SCQ and all variables that showed between-group differences are presented in Table 1. None of the neuroanatomical variables correlated with the total score obtained on the SCQ. Table 1. Correlations between clinical scores and neuroanatomical variables with between-group differences in participants with ASD.
In this study, we applied neuroimaging techniques using T1-weighted and DTI images in the interest of quantifying morphometric and connectivity differences in a group of children and adolescents with ASD. We used a validated technique with exquisite resolution to measure local cortical gyrification across the hemispheres Schaer et al. However, we believe part of the difference to relate to the way GI was calculated. Indeed, the two studies that reported higher GI in the frontal lobe of subjects with ASD used manual delineation on one single frontal slice.
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Aside from the fact that manual tracing may be less reliable than automated delineation, measuring GI on 2-D sections does not take into account the inherent 3-D nature of the cortical surface. Other studies that partly addressed these concerns did not report any significant differences in GI in patients with ASD compared to controls Casanova et al. Casanova et al. The technique that we use in the present study to measure l GI is automated, unbiased by slice orientation, and allows the quantification of gyrification differences at thousands of points over the reconstructed cortical surface.
As a result, by using l GI, we may have been able to detect gyrification differences in the frontal lobe of patients with ASD that had previously gone undetected. Studies using cortical reconstructions in autism corroborate this idea.
They have detected focal changes to sulcal shape with alterations to the sylvian fissure and inferior frontal sulcus Levitt et al. It is however worth noting that a recent study using the same technique as in the present study observed increased gyrification in different regions of the brain of 39 male adolescents with ASD as compared to 41 controls, namely in bilateral occipital areas as well as in the left superior precuneus Wallace et al.
This discrepancy in the location and direction of gyrification changes using the same technique suggest either that different developmental mechanisms take place in different regions of the brain of affected patients, or that that demographic characteristics such as differences in age, gender, cognitive level, or symptom intensity may have influenced the results. Indeed, it may be the case that the high clinical heterogeneity observed in patients affected with autism may be associated with different neurodevelopmental pathways.
Decreased gyrification, as observed in the present study, is highly suggestive of reduced cortical expansion during early brain development, a process that might differentially affect specific cortical regions. Neuropathological reports have pointed to abnormal cortical development in ASD, including a higher incidence of cortical dysgenesis, heterotopias and migration abnormalities Avino and Hutsler, ; Wegiel et al. Further detailed examination revealed that one cell type affected by migration deficits in young children with ASD is von Economo neurons Santos et al.
The location of the von Economo neurons coincides with the location of cluster 3 in the present study see Figure 2. Functional neuroimaging studies tend to confirm the hypothesis of hypoactivation of the right anterior insula in autism, as pointed out by a meta-analysis based on 24 functional neuroimaging studies examining social processes for a total of patients with ASD and controls Di Martino et al.
Two other clusters, in the right inferior frontal gyrus cluster 2 and in a region extending from the right inferior part of the precentral gyrus to the inferior parietal region cluster 1 , are also located in regions that have received attention in ASD. Indeed, these regions are striking in their correspondence to the location of the fronto-parietal mirror neuron system, implicated in action imitation Rizzolatti and Craighero, Decreased gyrification in the inferior fronto-parietal region thus supports altered development of the mirror system in ASD during in utero life or the first months after birth, pointing to a potential mechanism for early-disrupted abilities to imitate action of others.
The final cluster of reduced gyrification cluster 4 is centered in the occipital lobe, encompassing the cuneus and the pericalcarine sulcus, and further extending to the precuneus. Volumetric reductions have been consistently reported in the precuneus in structural neuroimaging studies of ASD Cauda et al.
Resting state paradigms have received increased recent interest in autism given the crucial role of the DMN in some aspects of social cognition. It is currently unclear to what extent the fronto-parietal mirror system where we observed decreased l GI in clusters 1 and 2 interacts with other regions of the social brain, including regions of the DMN. In an attempt to integrate these different views of the social brain, Uddin et al.
Accordingly, reduced gyrification in the mirror-neuron system may impair physical aspects of the self-other relationship, consequently altering the developmental cascade of the DMN responsible for more sophisticated social skills, such as empathy and theory of mind. The fact that cluster 4 extends into the precuneus may also point to an early defect, on top of which altered cortical maturation subsequently occurs.
Indeed, the currently observed inverse relationship between gyrification and the level of autistic symptoms in the domains of reciprocal social interactions and communication points to the idea that early cortical development may determine the subsequent development of these more sophisticated social skills encoded in the precuneus.
We found reduced gyrification in the absence of differences in cortical thickness or volume. This absence contrasts with numerous studies that have reported altered cortical volume or thickness differences in ASD. Most studies have reported increased cortical volume or thickness in children with ASD Hardan et al. Some studies in adults with ASD have reported mostly decreased cortical thickness Hadjikhani et al. Volumetric studies have more consistently reported increased volume in children and reduced volume in adults, supporting the hypothesis of early brain overgrowth followed by neurodegenerative changes Courchesne, Indeed, using a cross-sectional design with patients aged 1 to 50, the largest study published to date provides evidence for an aberrant trajectory of cortical volume changes with age, with a pattern of early overgrowth during the first years of life, followed by decreased volume around 7 or 8 years old Courchesne et al.
Longitudinal studies confirm this pattern of abnormal cortical development in toddlers with ASD Schumann et al. It should be noted, however, that studies recording abnormal trajectories of cortical features require large sample sizes, a broad age range at inclusion, and preferably, a longitudinal design.
The Neuroscience of Autism Spectrum Disorders
By contrast, our small study sample does not have the power to detect subtle cortical thickness differences that may be further diluted by complex maturational changes. As the largest white matter bundle of the brain, the corpus callosum represents the most essential component of connectivity, and more specifically long-range connectivity. Patients with ASD were also shown to perform poorly on tests of inter-hemispheric transfer for auditory, visual and motor tasks Nyden et al.
More generally, decreased abilities in associative Nikolaenko, a and metaphoric thinking Nikolaenko, b were thought to depend on decreased inter-hemispheric information transfer. Here, we observed decreased volume of the most anterior part of the corpus callosum, reduced inter-hemispheric frontal connections, and decreased FA in the anterior corpus callosum, providing strong multimodal evidence for altered inter-hemispheric frontal connections in ASD.
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Our volumetric finding is consistent with previous studies reporting reduced area of the entire corpus callosum, with greater magnitude of reduction in its anterior region see the meta-analysis by Frazier and Hardan, Reduced FA in the corpus callosum is also consistent with many previous findings reported by others Alexander et al. But, to the best of our knowledge, only one study reported a reduction in the number of inter-hemispheric frontal fibers using tractographic reconstructions in patients with ASD Thomas et al.
Thomas et al. The fact that we replicate this correlation though we focus on a more anterior, but overlapping, region provides strong support for a role for the corpus callosum in repetitive behaviors, across ages and across IQ. In addition to multimodal evidence for altered inter-hemispheric connectivity, we also observed seven clusters of decreased FA in the right hemisphere of patients with ASD compared to controls.
The direction of our results was consistent with most previously published studies, which show decreased FA, although a few studies do report increased FA reviewed in Travers et al. Surprisingly, in our small sample of children and adolescents with ASD, we found reduced FA only in the right hemisphere and did not detect changes to FA in the left hemisphere. Exclusively right-sided alterations to gyrification in the same sample of participants provide initial support for a relationship between white matter connectivity and cortical folding.
However, it was not possible to detect whether the observed FA differences were related to differences in the degree of myelinisation or to differences in the orientation or number of white matter bundles, using voxel-wise measurements of FA. The spatial correspondence of altered gyrification and white matter microstructure in the same hemisphere led us to further examine the relationship between cortical folding and connectivity using more sophisticated tractographic measurements.
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However, three out of the four clusters with decreased gyrification were mostly located in the frontal region, i. The co-occurrence of decreased long-range connections in regions of altered gyrification points to a possible relationship between these two anatomical variables, but the mechanisms governing their association is likely to be more complex than what a linear regression can capture.
We did, however, observe significant positive correlations between l GI and short-range connectivity in patients with ASD, but not in controls. This positive correlation means that higher l GI was observed in patients with higher intra-lobar short-range connectivity. Accordingly, the gyrification alterations observed in the present study may be a compensatory way of coping with altered connectivity in patients with ASD. The main limitation of our study is its small sample size, restricting our ability to identify age-related maturational changes or subtle brain-behavior relationships.
We realize that, in a heterogeneous disorder such as ASD, such small sample size may lead to observation of findings that may not be representative of the variability observed across the spectrum. However, despite the small sample size, we demonstrate the feasibility of multimodal studies in autism, bridging the gap between reports of altered cortical morphometry and findings of abnormal connectivity patterns.
These preliminary results provide initial support for the idea that a higher degree of short-range connectivity alters the shape of the brain in patients with ASD during early neural development, and are an encouraging starting point for exploring this issue in larger samples of children, adolescents or adults with autism. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
We would like to thank the children, adolescents and families who participated in this study. Alexander, A. Diffusion tensor imaging of the corpus callosum in Autism.