Background

Language delay is a hallmark feature of autism spectrum disorders (ASD). The identification of word boundaries in continuous speech is a critical first step in language acquisition that can be accomplished via statistical learning and reliance on speech cues. Importantly, early word segmentation skills have been shown to predict later language development in typically developing (TD) children.

Methods

Here we investigated the neural correlates of online word segmentation in children with and without ASD with a well-established behavioral paradigm previously validated for functional magnetic resonance imaging. Eighteen high-functioning boys with ASD and 18 age- and IQ-matched TD boys underwent functional magnetic resonance imaging while listening to two artificial languages (containing statistical or statistical + prosodic cues to word boundaries) and a random speech stream.

Results

Consistent with prior findings, in TD control subjects, activity in fronto-temporal-parietal networks decreased as the number of cues to word boundaries increased. The ASD children, however, did not show this facilitatory effect. Furthermore, statistical contrasts modeling changes in activity over time identified significant learning-related signal increases for both artificial languages in basal ganglia and left temporo-parietal cortex only in TD children. Finally, the level of communicative impairment in ASD children was inversely correlated with signal increases in these same regions during exposure to the artificial languages.

Conclusions

This is the first study to demonstrate significant abnormalities in the neural architecture subserving language-related learning in ASD children and to link the communicative impairments observed in this population to decreased sensitivity to the statistical and speech cues available in the language input.

Understanding the intended meaning of a remark beyond what is explicitly stated is an integral part of successful social interactions. Here, we examined the neural circuitry underlying the interpretation of communicative intent in children and adults using irony comprehension as a test case. Participants viewed cartoon drawings while listening to short scenarios ending with a potentially ironic remark and were asked to decide whether the speaker was being sincere or ironic. In both children and adults, instructions to attend to the cues provided by the speaker's facial expression or tone of voice modulated the activity in visual and language cortices, respectively. Overall, children engaged the medial prefrontal cortex and left inferior frontal gyrus more strongly than adults, whereas adults recruited the fusiform gyrus, extrastriate areas and the amygdala more strongly than children. Greater involvement of prefrontal regions in children may subserve the integration of multiple cues to reconcile the discrepancy between the literal and intended meaning of an ironic remark. This developmental shift from a reliance on frontal regions to posterior occipitotemporal regions may reflect the automatization of basic reasoning about mental states. This study is the first to examine developmental changes in the neural circuitry underlying natural language pragmatics.