Parallel but independent reduction of emotional awareness and corpus callosum connectivity in older age

Abstract

Differential functional specialization of the left and right hemispheres for linguistic and emotional functions, respectively, suggest that interhemispheric communication via the corpus callosum is critical for emotional awareness. Accordingly, it has been hypothesized that the age-related decline in callosal connectivity mediates the frequently demonstrated reduction in emotional awareness in older age. The present study tests this hypothesis in a sample of 307 healthy individuals between 20-89 years using combined structural and diffusion-tensor magnetic resonance imaging (MRI) of the corpus callosum. As assumed, inter-hemispheric connectivity (midsagittal callosal area and thickness, as well as fractional anisotropy, FA) and emotional awareness (i.e., increase in externally-oriented thinking, EOT; assessed with the Toronto Alexithymia Scale, TAS-20) were found to be reduced in older (> 60 years) compared to younger participants. Furthermore, relating callosal measures to emotional awareness, FA in the genu of the corpus callosum was found to be negatively correlated with EOT in male participants. Thus, "stronger" structural connectivity (higher FA) was related with higher emotional awareness (lower EOT). However, a formal mediation analysis did not support the notion that age-related decline in emotional awareness is mediated by the corpus callosum. Thus, the observed reduction of emotional awareness and callosal connectivity in older age likely reflects parallel but not inter-dependent processes.

Fig 1. Aging and emotional awareness.

Mean subscale scores for the three age groups, with error bars indicating the 95% confidence limits. A significant age group by subscale interaction (η² = .03) was found whereby a significant Age group effect was only confirmed for the EOT subscale (right side of graph). Marked by asterisks (*) are the significant post-hoc pairwise comparisons for the EOT score. The older age group differed significantly from the two other groups, indicating an increase in externally oriented thinking, that is, a decrease in emotional awareness with advancing age.

Fig 2. Aging and the corpus callosum.

Mean absolute area (A), relative area (i.e., area/tIV^0.667 ratio) (B), and fractional anisotropy, FA, (C) of the corpus callosum for the three age groups (error bars indicate CI_95%). Panel (A) shows the main effect of age group, indicating a decrease in midsagittal area in the oldest compared to the two other groups. The y-axis provides the mean area measures across the three callosal subregions (in mm²*0.111). Panel (B) shows the main effect for relative area (as average across subregions) with again the oldest group differing from the two others. Panel (C) shows the age group FA means for each of the callosal subregions. Comparable to what was found for the two other parameters, also in the FA analysis the main effect of age was significant. However, an also significant age group by subregion interaction together with post-hoc testing revealed the age effect only to be significant in the genu. The sketch to the right of panel (C) illustrates the corpus callosum outline and the location of the three subregions (anterior: left). In all three panels asterisks (*) indicate significant post-hoc comparisons.

Fig 3. Callosal measures and emotional awareness.

Bars represent the F-values for the effects of interest (i.e., main effect of subscale, interaction of subscale with sex and Region, respectively, and the three-way interaction) for the ANCOVAs conducted in the third analysis step. Results are shown separately for the three callosal parameters (panels) and the three TAS subscales (nested plots). Significant effects (p < .05) are indicated by asterisk (*), and trends (p < .10) by a number sign (#). Post-hoc analyses and effect size are reported in text. All effects common to the performed analyses (i.e., main effect of subregion and sex, as well as the subregion × sex interaction) are not depicted, but followed the same pattern as reported in analysis step 2.

Fig 4. Association of EOT and genu FA.

A significant negative correlation (r = -.259, p = .012) between FA in the genu and EOT in the male sample, was found to be the main factor underlying a significant three-way interaction of EOT, subregion, and sex. For no further callosal parameter, subregion, or subscale comparable effects were found. Details are presented in the Results section.

Fig 5. Mediation analysis.

Estimated callosal mediation model for the prediction of EOT by age group and considering genu FA as mediator. Sequential coding was utilized for Age group, resulting in two predictors contrasting the young and the middle age group (X₁) and the middle age with the older age group (X₂), respectively. Parameter a represents the unstandardized regression weight for Age group prediction the mediator variable Genu FA, parameter b represents the regression weight for the mediator predicting the dependent variable EOT, and parameter c’ represent the direct effect of Age group on EOT. Parameter c represents the prediction without considering Genu FA. The indirect effect estimates are noted as a₁b and a₂b, respectively. Subscript numbers 1 and 2 of the path regression weights (a, c, and c’) indicate on which of the two Age group predictors the estimation was based. Significant effects (p < .05) are indicated by asterisk (*), and trends (p < .10) by a number sign (#).