Functional neural correlates of emotional expression processing deficits in behavioural variant frontotemporal dementia

Abstract

Background: Frontotemporal dementia (FTD) is a neurodegenerative disorder resulting in social-cognitive deficits partially attributed to abnormalities processing social cues, such as facial expressions. However, to our knowledge, the functional neuroanatomy of deficient social cue processing in individuals with FTD has not been examined. The objective of this study was to delineate the functional abnormalities under lying altered facial expression processing in individuals with FTD using functional magnetic resonance imaging (fMRI).

Methods: Patients meeting Neary criteria for behavioural variant FTD (bvFTD) with supportive neuroimaging and 18 age-matched healthy controls completed an implicit facial expression task during fMRI. We conducted volumetric brain morphometry to correct functional imaging data for volume differences.

Results: We included 20 patients with bvFTD and 18 controls in our study. The results demonstrate emotion-specific functional abnormalities in frontal and limbic regions in patients with bvFTD. Patients also showed decreased activity in posterior ventral visual regions, specifically the fusiform cortex, possibly reflecting reduced afferent input from limbic regions. Finally, bvFTD was associated with increased activity in posterior regions, including the inferior parietal cortex.

Limitations: Autopsy validation of frontotemporal dementia is not yet available for this cohort.

Conclusion: Together, these findings suggest that fMRI combined with tasks targeting social-cognitive deficits is a powerful technique to objectively measure neural systems involved in emotion processing in individuals with bvFTD. As viewing emotional expressions is known to engage many of the same neural systems that are active when experiencing the emotion itself, fMRI during expression processing provides a novel window into the emotions of patients with FTD.

Fig. 1

Emotional facial expression functional magnetic resonance imaging task. Trial schematic depicting the time course for 2 consecutive trials. The first face shows a disgusted man at 40% emotional intensity; the second shows a fearful woman at 100% emotional intensity.

Fig. 2

Regions demonstrating significant blood oxygen level–dependent (BOLD) signal differences during emotional facial expressions in patients with behavioural variant frontotemporal dementia (bvFTD) compared with controls. During angry expression processing, patients with bvFTD demonstrate decreased BOLD signal (blue/green) compared with controls in the (A) right ventrolateral pre-frontal cortex and (B) ventral visual stream, specifically the left fusiform gyrus. In contrast, patients with bvFTD showed increased BOLD signal (red/yellow) in the (C) right inferior parietal lobule and left posterior cingulate gyrus. (D) During disgusted expression processing, decreased BOLD signal in the bilateral insula and right middle occipital gyrus is observed in patients with bvFTD compared with controls. (E) During happy expression processing, decreased BOLD signal in the left amygdala is observed in patients with bvFTD compared with controls. Significant clusters are shown at p < 0.005 and at p < 0.05 to illustrate the extent of the activations. Statistical maps are corrected for voxel-wise grey matter differences. All images are displayed in radiological convention.

Fig. 3

Contrast of low-intensity (40%) facial expressions in patients with behavioural variant frontotemporal dementia (bvFTD) compared with controls demonstrating increased blood oxygen level–dependent signal (red/yellow) in patients with bvFTD in dorsal regions, including the bilateral inferior parietal lobule, left posterior cingulate cortex and left precuneus. Significant clusters are shown at p < 0.005 and also at p < 0.05 to illustrate the extent of activation. Statistical maps are corrected for voxel-wise grey matter differences. All images are displayed in radiological convention.