Decreased left posterior insular activity during auditory language in autism

Abstract

Background and purpose: Individuals with autism spectrum disorders often exhibit atypical language patterns, including delay of speech onset, literal speech interpretation, and poor recognition of social and emotional cues in speech. We acquired functional MR images during an auditory language task to evaluate systematic differences in language-network activation between control and high-functioning autistic populations.

Materials and methods: Forty-one right-handed male subjects (26 high-functioning autistic subjects, 15 controls) were studied by using an auditory phrase-recognition task, and areas of differential activation between groups were identified. Hand preference, verbal intelligence quotient (IQ), age, and language-function testing were included as covariables in the analysis.

Results: Control and autistic subjects showed similar language-activation networks, with 2 notable differences. Control subjects showed significantly increased activation in the left posterior insula compared with autistic subjects (P < .05, false discovery rate), and autistic subjects showed increased bilaterality of receptive language compared with control subjects. Higher receptive-language scores on standardized testing were associated with greater activation of the posterior aspect of the left Wernicke area. A higher verbal IQ was associated with greater activation of the bilateral Broca area and involvement of the prefrontal cortex and lateral premotor cortex.

Conclusions: Control subjects showed greater activation of the posterior insula during receptive language, which may correlate with impaired emotive processing of language in autism. Subjects with autism showed greater bilateral activation of receptive-language areas, which was out of proportion to the differences in hand preference in autism and control populations.

Fig 1.

Group-level activation maps for an auditory phrase-recognition task for 15 control subjects (A) and for 26 high-functioning autistic subjects (B). Results for each group represent P < .05, false discovery rate (FDR), and color bars represent values for t-scores. Arrows show left posterior insular, right lateral premotor, and right Wernicke homolog areas where differences in activity are observed.

Fig 2.

Group-level activation maps for 15 control subjects for auditory > visual tasks (blue) and auditory tasks (red) after masking the auditory > visual tasks. Both results show P < .05, FDR.

Fig 3.

Areas of greater activation for control than autism subjects for auditory language tasks. A, Control > autism activation for P < .05, FDR. Color bar shows t-scores. B, Blood oxygen level–dependent time series data for clusters are shown above for the entire auditory language task in autism and control populations, averaged across subjects for each group. Thin traces show standard error of the mean across subjects for each group.

Fig 4.

Hand preference and language laterality for autism and control subjects. Histograms show the number of subjects exhibiting scores between −100 and 100 (Edinburgh Handedness Inventory) or between −1 and 1 (functional MR imaging [fMRI] laterality index), in which 100 represents strong right-handedness and 1 represents strong left-hemispheric language dominance.

Fig 5.

Associations between auditory language activation and covariables for all subjects. A, Activity associated with higher receptive-language (Clinical Evaluation of Language Fundamentals, 3rd ed) scores (red, P < .05, FDR) and higher verbal intelligence quotients (blue, P < .001, uncorrected). B, Activity associated with younger age (P < .05, FDR).