Reduced neural selectivity for mental states in deaf children with delayed exposure to sign language

Abstract

Language provides a rich source of information about other people's thoughts and feelings. Consequently, delayed access to language may influence conceptual development in Theory of Mind (ToM). We use functional magnetic resonance imaging and behavioral tasks to study ToM development in child (n = 33, 4-12 years old) and adult (n = 36) fluent signers of American Sign Language (ASL), and characterize neural ToM responses during ASL and movie-viewing tasks. Participants include deaf children whose first exposure to ASL was delayed up to 7 years (n = 12). Neural responses to ToM stories (specifically, selectivity of the right temporo-parietal junction) in these children resembles responses previously observed in young children, who have similar linguistic experience, rather than those in age-matched native-signing children, who have similar biological maturation. Early linguistic experience may facilitate ToM development, via the development of a selective brain region for ToM.

Fig. 1. Theory of mind behavior.

a Proportion correct on linguistic (L (ASL); left) and minimally linguistic (ML; right) ToM tasks (y-axis) by age (top row; x-axis) or by Z-scored age of ASL onset (middle row; x-axis). Z scores are used for de-identification of data. Native signers (n = 16, L task; n = 21, ML task) are shown in blue; delayed signers (n = 12 (both tasks)) are shown in orange. For the linguistic task, gray dots show 3–12 year-old hearing participants who completed an analogous task in English in other studies (n = 137). Gray shading (top row) shows the 95% confidence level interval for a linear regression predicting the effect of age on ToM performance, per ASL signing group. Asterisk (middle left) indicates a significant effect of age of ASL onset on linguistic ToM performance (b = −0.54, t = −3.4, 95% CI = [−0.86, −0.21], P = 0.002; linear regression controlling for age). b Standard boxplots of proportion correct on linguistic and minimally linguistic ToM tasks for native (blue; n = 16, L task; n = 21, ML task) and delayed (orange, n = 12, both tasks) signers (y-axis) by question category (x-axis; FB refers to false-belief items). Center line indicates median, box reflects interquartile range, whiskers show first quartile/third quartile −/+ 1.5*IQR, means are shown with black diamonds, and individual data points are shown with blue (NS) and orange (DS) circles. Source data are provided as a Source Data file and at https://osf.io/kyu3f/.

Fig. 2. Theory of mind brain regions preferentially respond to ASL stories that describe mental states.

Brain images show results of whole-brain random effects analyses for all children (n = 24, top row) and adults (n = 36, bottom row) for the Mental > Physical stories contrast (one-sample t tests). Clusters that survive correction for multiple comparisons using permutation analyses (SnPM; P < 0.05) are shown in orange; red clusters show activation where P < 0.001, k = 10, uncorrected for multiple comparisons (children only); see Table 1 for further information about significant clusters. Bar plots show average beta-value estimates per condition + /− SEM (Mental (red), Social (purple), Physical (blue) stories, and Non-Signs (green) in individually defined functional ToM regions of interest (ROIs; averaged across bilateral temporoparietal junction, precuneus, and dorso-, middle-, and ventromedial prefrontal cortex); dots show individual data points per participant. The adult non-sign condition bar refers to the 8-Non-Sign condition (see Methods). Error bars are omitted for Mental and Physical conditions because these conditions were used for individual ROI definition. See Supplementary Fig. 2 for similar plots in group regions of interest. Source data are provided as a Source Data file and at https://osf.io/kyu3f/.

Fig. 3. RTPJ & DMPFC responses to ASL story task.

a Standard boxplots (left) show the distribution of selectivity indices in RTPJ (top row) and DMPFC (bottom row) in native signing (NS; blue; RTPJ: n = 15; DMPFC: n = 12 (out of 16)), delayed signing (DS; orange; RTPJ: n = 8; DMPFC: n = 6 (out of 8)), and age-matched neurotypical hearing (gray; n = 28 6–10-year old) children, who completed an analogous fMRI story task in English. Center line reflects median, box reflects interquartile range (IQR), whiskers show first quartile/third quartile −/+ 1.5*IQR; dots show individual data points per participant; violin outline shows the distribution of data. Selectivity index was calculated as the average beta estimate to (Mental–Social/Mental–Physical)*100. Asterisk indicates that delayed signers had less selective RTPJ responses than native signers (two-sided non-parametric Mann–Whitney U test; W = 97, CI = [4.3, 53.6], P = 0.02). Bar plots (middle) show mean beta estimates by condition + /− SEM (Mental (red), Social (purple), Physical (blue)) in individually defined RTPJ (top) and DMPFC (bottom) ROIs in children; dots show individual data points per participant. The mental and physical conditions were used for individual ROI definition and are shown for visualization purposes only (and therefore do not have error bars). Scatterplots (right) show the selectivity index for RTPJ and DMPFC in NS (RTPJ: n = 15; DMPFC: n = 12) and DS children (RTPJ: n = 8; DMPFC: n = 6) by Z-scored age of ASL onset (x-axis). Asterisk indicates a significant effect of age of ASL onset on RTPJ selectivity among children (b = −0.47, t = −2.3, 95% CI = [−0.90, −0.05], P = 0.03; linear regression controlling for age and motion). b Scatterplots show the selectivity index for RTPJ and DMPFC in adults (RTPJ (top): n = 20 NS (blue), n = 16 DS (orange); DMPFC (bottom): n = 19 NS, n = 16 DS), by Z-scored age of ASL onset (x-axis). Z scores are used on x-axes for de-identification of data. Source data are provided as a Source Data file and at https://osf.io/kyu3f/.