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. 2015 Jul;220(4):2355-71.
doi: 10.1007/s00429-014-0791-z. Epub 2014 May 29.

Neural networks related to dysfunctional face processing in autism spectrum disorder

Thomas Nickl-Jockschat  1 , Claudia Rottschy, Johanna Thommes, Frank Schneider, Angela R Laird, Peter T Fox, Simon B Eickhoff
Affiliations

Neural networks related to dysfunctional face processing in autism spectrum disorder

Thomas Nickl-Jockschat et al. Brain Struct Funct. 2015 Jul.

Abstract

One of the most consistent neuropsychological findings in autism spectrum disorders (ASD) is a reduced interest in and impaired processing of human faces. We conducted an activation likelihood estimation meta-analysis on 14 functional imaging studies on neural correlates of face processing enrolling a total of 164 ASD patients. Subsequently, normative whole-brain functional connectivity maps for the identified regions of significant convergence were computed for the task-independent (resting-state) and task-dependent (co-activations) state in healthy subjects. Quantitative functional decoding was performed by reference to the BrainMap database. Finally, we examined the overlap of the delineated network with the results of a previous meta-analysis on structural abnormalities in ASD as well as with brain regions involved in human action observation/imitation. We found a single cluster in the left fusiform gyrus showing significantly reduced activation during face processing in ASD across all studies. Both task-dependent and task-independent analyses indicated significant functional connectivity of this region with the temporo-occipital and lateral occipital cortex, the inferior frontal and parietal cortices, the thalamus and the amygdala. Quantitative reverse inference then indicated an association of these regions mainly with face processing, affective processing, and language-related tasks. Moreover, we found that the cortex in the region of right area V5 displaying structural changes in ASD patients showed consistent connectivity with the region showing aberrant responses in the context of face processing. Finally, this network was also implicated in the human action observation/imitation network. In summary, our findings thus suggest a functionally and structurally disturbed network of occipital regions related primarily to face (but potentially also language) processing, which interact with inferior frontal as well as limbic regions and may be the core of aberrant face processing and reduced interest in faces in ASD.

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Figures

Fig. 1
Fig. 1
A single cluster indicating convergent evidence for hypoactivation in ASD patients compared to healthy controls during face processing was located in the left lateral temporal lobe, in particular the fusiform gyrus (−43, −61, −10, k = 172) [p < 0.05 (cluster-level FWE corrected for multiple comparisons, cluster-forming threshold p < 0.001 at voxel level)]. There were no clusters indicating increased activation in ASD patients compared to healthy controls
Fig. 2
Fig. 2
Task-dependent functional connectivity determined by MACM revealed significant co-activations of seed identified in the meta-analysis, i.e., the left fusiform gyrus regions showing consistent hypo-activation in patients with ASD during face processing [p < 0.05 (cluster-level FWE corrected for multiple comparisons, cluster-forming threshold p < 0.001 at voxel level)]
Fig. 3
Fig. 3
Resting-state functional connectivity analysis revealed a distributed network of areas showing correlated BOLD signal changes with the seed identified in the meta-analysis, i.e., the left fusiform gyrus regions showing consistent hypo-activation in patients with ASD during face processing [p < 0.05 (cluster-level FWE corrected for multiple comparisons, cluster-forming threshold p < 0.001 at voxel level)]
Fig. 4
Fig. 4
Based on the two analyses described above, we then delineated regions that showed consensus functional connectivity, i.e., significant resting-state correlations as well as significant task-based co-activations with the seed region in the left fusiform gyrus that was hypo-activated during face processing in ASD
Fig. 5
Fig. 5
Conjunction analysis between the network showing both task-dependent and task-independent functional connectivity with the seed region overlapped with the action observation/imitation network (Caspers et al. 2010)
Fig. 6
Fig. 6
Overlap between the network showing both task-dependent and task-independent functional connectivity to the seed region and regions showing structural anomalies in ASD patients that have been previously identified by a quantitative meta-analysis on VBM studies (Nickl-Jockschat et al. 2012)
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