Differential late-stage face processing in autism: a magnetoencephalographic study of fusiform gyrus activation

Abstract

Background: Autism is associated with alterations of social communication, such as during face-to-face interactions. This study aimed to probe face processing in autistics with normal IQ utilizing magnetoencephalography to examine event-related fields within the fusiform gyrus during face perception.

Methods: A case-control cohort of 22 individuals diagnosed with autism and 20 age-matched controls (all male, age 29.3 ± 6.9 years) underwent magnetoencephalographic scanning during an active task while observing neutral faces, face-like pareidolic objects, and non-face objects. The fusiform face area was identified using a face localizer for each participant, and the cortical activation pattern was normalized onto an average brain for subsequent analysis.

Results: Early post-stimulus activation amplitudes (before 100-200 ms) indicated differentiation between stimuli containing fundamental facial features and non-face objects in both groups. In contrast, later activation (400-550 ms) differentiated real faces from both pareidolic and non-face objects across both groups and faces from objects in controls but not in autistics. There was no effect of autistic-like traits.

Conclusions: The absence of group differences in early activation suggest intact face detection in autistics possessing a normal IQ. Later activation captures a greater degree of the complexity and social information from actual faces. Although both groups distinguished faces from pareidolic and non-face objects, the control group exhibited a slightly heightened differentiation at this latency, indicating a potential disadvantage for autistics in real face processing. The subtle difference in late-stage face processing observed in autistic individuals may reflect specific cognitive mechanisms related to face perception in autism.

Keywords: Autism; Biomarker; Face processing; Fusiform face area; Magnetoencephalography; Pareidolia.

Fig. 1

Examples of stimuli presented for OBJECTS paradigm. From left to right: pareidolic face-like object, non-face object, real face and inverted face

Fig. 2

Across-group results of event-related fields within the right fusiform area. * and ** denote significant and Holm-Bonferroni-corrected significant differences for main effects from mixed analyses of variance

Fig. 3

Within-group results of event-related fields within the right fusiform area. * and ** denote significant (p < .05) and Holm-Bonferroni-corrected significant differences (see Table 2 for p-value thresholds) for main effects from one-way analyses of variance

Fig. 4

Source space activations within the right fusiform face area averaged for each group and stimulus

Fig. 5

Between-group pairwise group comparison for each stimulus type. Cluster-based permutation test for event-related fields with 5000 permutations when comparing autism and control for faces (p = .10), face-like objects (p = .44), and objects (p = .60). From top to bottom, the subplots present, for each time-point, the averaged event-related field (ERF) activation, a stimulus-wise subtraction for the averaged ERFs, and the permutation-based T-values and effect sizes

Fig. 6

Within-group pairwise comparisons between faces and objects. Cluster-based permutation test for event-related fields with 5000 permutations when comparing faces and objects for control (p < .0002) and autism (p = .067). From top to bottom, the subplots present, for each time-point, the averaged event-related field (ERF) activation, a stimulus-wise subtraction for the averaged ERFs, permutation-based T-values and effect sizes, and the proportion of individuals with positive within-subject subtractions

Fig. 7

Within-group pairwise comparisons between face-like objects and objects. Cluster-based permutation test for event-related fields with 5000 permutations when comparing face-like objects and objects for control (p = .027) and autism (p = .053). From top to bottom, the subplots present, for each time-point, the averaged event-related field (ERF) activation, a stimulus-wise subtraction for the averaged ERFs, permutation-based T-values and effect sizes, and the proportion of individuals with positive within-subject subtractions

Fig. 8

Within-group pairwise comparisons between faces and face-like objects. Cluster-based permutation test for event-related fields with 5000 permutations when comparing faces and face-like objects for control (p = .02) and autism (p = .63). From top to bottom, the subplots present, for each time-point, the averaged event-related field (ERF) activation, a stimulus-wise subtraction for the averaged ERFs, permutation-based T-values and effect sizes, and the proportion of individuals with positive within-subject subtractions

Fig. 9

Source space distribution of F-values around 150–170 ms from cluster-based permutation when comparing face-like objects and objects across all participants

Fig. 10

Source space distribution of F-values around 130–150 ms from cluster-based permutation when comparing faces and objects across all participants