Expressive Prosody in Patients With Focal Anterior Temporal Neurodegeneration

Abstract

Background and objectives: Progressive focal anterior temporal lobe (ATL) neurodegeneration has been historically called semantic dementia. More recently, semantic variant primary progressive aphasia (svPPA) and semantic behavioral variant frontotemporal dementia (sbvFTD) have been linked with predominant left and right ATL neurodegeneration, respectively. Nonetheless, clinical tools for an accurate diagnosis of sbvFTD are still lacking. Expressive prosody refers to the modulation of pitch, loudness, tempo, and quality of voice used to convey emotional and linguistic information and has been linked to bilateral but right-predominant frontotemporal functioning. Changes in expressive prosody can be detected with semiautomated methods and could represent a useful diagnostic marker of socioemotional functioning in sbvFTD.

Methods: Participants underwent a comprehensive neuropsychological and language evaluation and a 3T MRI at the University of California San Francisco. Each participant provided a verbal description of the picnic scene from the Western Aphasia Battery. The fundamental frequency (f0) range, an acoustic measure of pitch variability, was extracted for each participant. We compared the f0 range between groups and investigated associations with an informant-rated measure of empathy, a facial emotion labeling task, and gray matter (GM) volumes using voxel-based morphometry.

Results: Twenty-eight patients with svPPA, 18 with sbvFTD, and 18 healthy controls (HCs) were included. f0 range was significantly different across groups: patients with sbvFTD showed reduced f0 range in comparison with both patients with svPPA (mean difference of -1.4 ± 2.4 semitones; 95% CI -2.4 to -0.4]; p < 0.005) and HCs (mean difference of -1.9 ± 3.0 semitones; 95% CI -3.0 to -0.7]; p < 0.001). A higher f0 range was correlated with a greater informant-rated empathy (r = 0.355; p ≤ 0.05), but not facial emotion labeling. Finally, the lower f0 range was correlated with lower GM volume in the right superior temporal gyrus, encompassing anterior and posterior portions (p < 0.05 FWE cluster corrected).

Discussion: Expressive prosody may be a useful clinical marker of sbvFTD. Reduced empathy is a core symptom in sbvFTD; the present results extend this to prosody, a core component of social interaction, at the intersection of speech and emotion. They also inform the long-standing debate on the lateralization of expressive prosody in the brain, highlighting the critical role of the right superior temporal lobe.

Figure 1. Atrophy Profiles Comparison Between the 3 Participant Groups (p < 0.05 FWE Corrected)

Light green represents areas where patients with sbvFTD have more atrophy than HCs and svPPA and dark green those where patients with svPPA have more atrophy than HCs and patients with sbvFTD.

Figure 2. Fundamental Frequency (f0) Range in Each Group of Participants

f0 = fundamental frequency; * indicating p < 0.005; ** indicating p < 0.001.

Figure 3. Correlations Between Socioemotional Measures and f0 Range in Patients With svPPA and sbvFTD

(A) Correlation between f0 range and informant-rated empathy assessed by RSMS; (B) Correlation between f0 range and facial emotion labelling measured by the CATS. CATS = Comprehensive Affect Testing System; f0 = fundamental frequency, RSMS = Revised Self-Monitoring Scale; * indicating p < 0.05.

Figure 4. Gray Matter Correlates of f0 Range in Patients With svPPA and sbvFTD (p < 0.05 FWE Corrected)