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

Abstract

IntroductionBehavioural variant frontotemporal dementia (bvFTD) is a neurodegenerative disorder characterized by progressive dysfunction in social behaviour typically beginning in midlife (50s-60s). A hallmark of bvFTD is the loss of empathy for others, a symptom thought to be partially accounted for by a reduction in emotion recognition.1 Facial expressions are one way in which we communicate emotional information critical for successful social behaviour.2,3 Deficient facial expression recognition, particularly for negative expressions, such as fear and anger, is associated with inappropriate social behaviours. 4,5 Previous studies have demonstrated that patients with bvFTD with frontally or temporally predominant atrophy show deficits in facial expression recognition, while general face processing abilities, such as facial identity and gender discrimination are preserved. [6][7][8] Whereas a growing body of research has associated regions of atrophy with bvFTD clinical symptoms, to our knowledge, the 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.

Impaired recognition of body expressions in the behavioral variant of frontotemporal dementia

“…It cannot be ruled out that the cooperative and motivational demands of the study resulted in an inclusion bias favoring temporal dominant variants (Whitwell et al, 2009). In fact, 6 patients were invited and agreed to participate in the study, but could not be included because of insufficient cooperation or agitation, similar to a previous study (Virani, Jesso, Kertesz, Mitchell, & Finger, 2013). In addition to comparisons with other neurodegenerative disorders, it would be informative to compare emotion recognition in bvFTD as a function of neuro-anatomic phenotype.…”

Amygdala atrophy affects emotion-related activity in face-responsive regions in frontotemporal degeneration

“…Additionally, even though face and emotion processing have been considered to be right-lateralized, recent evidence suggests that perception of dynamic faces shows no clear lateralization in FFA (De Winter et al, 2015). In addition a recent study investigating emotional face processing in bvFTD (Virani, Jesso, Kertesz, Mitchell, & Finger, 2013) reported reduced functional activity compared to healthy controls in left but not right fusiform cortex.…”

Functional dissociation between anterior temporal lobe and inferior frontal gyrus in the processing of dynamic body expressions: Insights from behavioral variant frontotemporal dementia

“…They are components of various intrinsic brain networks such as the salience network [Seeley et al, 2007], comprising anterior cingulate cortex and anterior insula, the default or mentalizing network [Buckner et al, 2008], including precuneus, temporo-parietal junction, medial prefrontal cortex, and the temporal poles, the action observation network [Grafton, 2009], including occipito-temporal, parietal and premotor areas, and the limbic network [Yeo et al, 2011]. Furthermore, numerous behavioral studies have shown impaired emotion recognition in bvFTD patients, using faces [Baez et al, 2014;Bediou et al, 2009;Bertoux et al, 2015;Couto et al, 2013;Diehl-Schmid et al, 2007;Fernandez-Duque and Black, 2005;Keane et al, 2002;Kumfor et al, 2011;Lavenu et al, 1999;Lough et al, 2006;Miller et al, 2012;Rosen et al, 2002;Snowden et al, 2008;Virani et al, 2013], bodies [Van den Stock et al, 2015] and music [Downey et al, 2013;Omar et al, 2011] as test stimuli. To gain insights into the specific functions that individual brain regions perform during emotion perception, we investigated emotion processing in patients diagnosed with the behavioral variant of frontotemporal dementia (bvFTD).…”

“…Because task-based functional imaging in bvFTD patients has proved difficult, given their behavioral symptoms [but see Virani et al, 2013], we opted for a combination of behavioral testing with structural and resting-state imaging in patients and age-matched controls, together with task-based functional imaging in young, healthy volunteers. Starting with the prediction that bvFTD patients would be impaired in emotion detection as well as emotion categorization, we intended to answer four specific questions: (1) Does an individual's impairment correlate with gray matter atrophy in distinct regions involved in emotion processing?…”