Neural development of networks for audiovisual speech comprehension

Abstract

Everyday conversation is both an auditory and a visual phenomenon. While visual speech information enhances comprehension for the listener, evidence suggests that the ability to benefit from this information improves with development. A number of brain regions have been implicated in audiovisual speech comprehension, but the extent to which the neurobiological substrate in the child compares to the adult is unknown. In particular, developmental differences in the network for audiovisual speech comprehension could manifest through the incorporation of additional brain regions, or through different patterns of effective connectivity. In the present study we used functional magnetic resonance imaging and structural equation modeling (SEM) to characterize the developmental changes in network interactions for audiovisual speech comprehension. The brain response was recorded while children 8- to 11-years-old and adults passively listened to stories under audiovisual (AV) and auditory-only (A) conditions. Results showed that in children and adults, AV comprehension activated the same fronto-temporo-parietal network of regions known for their contribution to speech production and perception. However, the SEM network analysis revealed age-related differences in the functional interactions among these regions. In particular, the influence of the posterior inferior frontal gyrus/ventral premotor cortex on supramarginal gyrus differed across age groups during AV, but not A speech. This functional pathway might be important for relating motor and sensory information used by the listener to identify speech sounds. Further, its development might reflect changes in the mechanisms that relate visual speech information to articulatory speech representations through experience producing and perceiving speech.

Figure 1

Whole-brain analysis results for each condition compared to Baseline for both adults and children. The individual per-vertex threshold was p < .01 (corrected FWE p < .05).

Figure 2

Base theoretical network models for each condition and for each age group. Path coefficients represent standardized values. For the auditory-only networks, path coefficients connecting visual and fusiform nodes to the rest of the network were set to zero. IFGTr = Inferior frontal gyrus (pars triangularis); IFGOp/PMv = Inferior frontal gyrus (pars opercularis)/ventral premotor; SMG = Supramarginal gyrus; STp = Posterior superior temporal (posterior superior temporal gyrus and planum temporale); Aud = Auditory (transverse temporal gyrus and sulcus); STa = Anterior superior temporal (anterior superior temporal gyrus and planum polare); STSp = Posterior superior temporal sulcus; MTGp = Posterior middle temporal gyrus; Fus = Fusiform gyrus; Vis = Visual (striate and extrastriate cortex).

Figure 3

Analysis of age and condition differences within the sub-network of interest. Red nodes were identified as important for connecting auditory and visual information during speech comprehension. Clear nodes comprised the remaining nodes of the theoretical network. Green arrows indicate a significant difference for that pathway for the comparison of interest. Grey arrows indicate pathways that were assessed for significance for the comparison of interest, but indicated no significant differences. IFGTr = Inferior frontal gyrus (pars triangularis); IFGOp/PMv = Inferior frontal gyrus (pars opercularis)/ventral premotor; SMG = Supramarginal gyrus; STp = Posterior superior temporal (posterior superior temporal gyrus and planum temporale); Aud = Auditory (transverse temporal gyrus and sulcus); STa = Anterior superior temporal (anterior superior temporal gyrus and planum polare); STSp = Posterior superior temporal sulcus; MTGp = Posterior middle temporal gyrus; Fus = Fusiform gyrus; Vis = Visual (striate and extrastriate cortex).