Developmental changes in the neural basis of interpreting communicative intent

Abstract

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.

Fig. 1

Example scenario. The setup (top panel) is shared by both the sincere and ironic versions of the scenario. The sincere ending is shown in the bottom left panel and the ironic ending is displayed in the bottom right panel. The text below the drawings represents the accompanying auditory stimuli. Participants first view the setup, then either the sincere or ironic version of a scenario followed by a blank screen and the question, ‘Did Dina mean what she said?’

Fig. 2

Brain activity averaged across all irony conditions compared with rest in children (A) and adults. (B) Figures are thresholded at t > 1.80, corrected for multiple comparisons at the cluster level, P < 0.05.

Fig. 3

Brain regions differentially activated in children and adults across all irony tasks. (A). Children showed significantly greater activity than adults in the MPFC (x = −8, y = 58, z = 20; P < 0.05), the left inferior frontal gyrus (x = −48, y = 16, z = 14; P = 0.05) and the right posterior STS (x = 42, y = −44, z = 16; P < 0.05). (B) Adults showed reliably greater activity than children in posterior temporal-occipital regions, including the left amygdala (x = −22, y = −2, z = −12; P < 0.05, SVC), bilateral FG (L: x = −28, y = −64, z = −8; R: x = 30, y = −66, z = −14; P < 0.05) and left STG (x = −36, y = −26, z = 8; P < 0.05). All regions shown survive a threshold of t > 1.80 and whole-volume correction for multiple comparisons at the cluster level, P < 0.05, or small volume correction (SVC) where noted.

Fig. 4

Age-related brain activity in children across all irony tasks. (A) Increasing chronological age was reliably associated with increased activation of the right FG (x = 24, y = −58, z = −14; P < 0.05). (B) Decreased activation of the MPFC (peak in dorsal MPFC, x = −2, y = 44, z = 32; P < 0.05) was reliably associated with increasing age. Activity in the left IFG (x = −58, y = 20, z = 10; P < 0.05, SVC), left STG (x = −46, −22, 6; P < 0.05) and right MTG (x = 44, y = −36, z = 4; P < 0.05) also decreased as a function of age (not shown). All regions survive a threshold of t > 1.80 and whole-volume correction for multiple comparisons at the cluster level, P < 0.05, or small volume correction (SVC) where noted.