The functional neuroanatomy of emotion processing in frontotemporal dementias

Abstract

Impaired processing of emotional signals is a core feature of frontotemporal dementia syndromes, but the underlying neural mechanisms have proved challenging to characterize and measure. Progress in this field may depend on detecting functional changes in the working brain, and disentangling components of emotion processing that include sensory decoding, emotion categorization and emotional contagion. We addressed this using functional MRI of naturalistic, dynamic facial emotion processing with concurrent indices of autonomic arousal, in a cohort of patients representing all major frontotemporal dementia syndromes relative to healthy age-matched individuals. Seventeen patients with behavioural variant frontotemporal dementia [four female; mean (standard deviation) age 64.8 (6.8) years], 12 with semantic variant primary progressive aphasia [four female; 66.9 (7.0) years], nine with non-fluent variant primary progressive aphasia [five female; 67.4 (8.1) years] and 22 healthy controls [12 female; 68.6 (6.8) years] passively viewed videos of universal facial expressions during functional MRI acquisition, with simultaneous heart rate and pupillometric recordings; emotion identification accuracy was assessed in a post-scan behavioural task. Relative to healthy controls, patient groups showed significant impairments (analysis of variance models, all P < 0.05) of facial emotion identification (all syndromes) and cardiac (all syndromes) and pupillary (non-fluent variant only) reactivity. Group-level functional neuroanatomical changes were assessed using statistical parametric mapping, thresholded at P < 0.05 after correction for multiple comparisons over the whole brain or within pre-specified regions of interest. In response to viewing facial expressions, all participant groups showed comparable activation of primary visual cortex while patient groups showed differential hypo-activation of fusiform and posterior temporo-occipital junctional cortices. Bi-hemispheric, syndrome-specific activations predicting facial emotion identification performance were identified (behavioural variant, anterior insula and caudate; semantic variant, anterior temporal cortex; non-fluent variant, frontal operculum). The semantic and non-fluent variant groups additionally showed complex profiles of central parasympathetic and sympathetic autonomic involvement that overlapped signatures of emotional visual and categorization processing and extended (in the non-fluent group) to brainstem effector pathways. These findings open a window on the functional cerebral mechanisms underpinning complex socio-emotional phenotypes of frontotemporal dementia, with implications for novel physiological biomarker development.

Lesions in the right Rolandic operculum are associated with self-rating affective and apathetic depressive symptoms for post-stroke patients

“…Several studies have reported relationships between the Rolandic operculum and psychology (or emotion) with or without an external factor (disease) and/or intervention (substance abuse). The role of the operculum is also related to emotion processing through music 15 , 16 and facial expression 17 . Mean diffusivity of the Rolandic operculum is positively correlated with indices of empathizing-cooperativeness 18 and depressive symptoms 19 , and hypoactivation in the right parietal and central operculum is associated with impaired emotion processing due to alcohol dependence 20 .…”

rTMS modulates precuneus-hippocampal subregion circuit in subjective cognitive decline

“…The SVM classi er showed that the abnormalities in brain memory networks had a high power to discriminate SCD from CN on an individual subject basis, with an ACC of 86.0%, an AUC of 92.9%, 83.8% sensitivity, and 89.1% speci city, which suggests that this study identi es a HIPsub pathological circuit related to SCD. The HIPe network connectivity in SCD subjects is predominantly abnormal in the brain regions involved in many aspects of emotional processing, including the cerebellum [39,40], anterior insula [39,41], parahippocampa gyrus [39,42], and fusiform gyrus [43]. Indeed, SCD subjects are characterized by self-reported concerns regarding their memory decline [44], which signi cantly increases the risk of AD [5].…”

rTMS modulates precuneus-hippocampal subregion circuit in subjective cognitive decline 

“…The SVM classi er showed that the abnormalities in brain memory networks had a high power to discriminate SCD from CN on an individual subject basis, with an ACC of 86.0%, an AUC of 92.9%, 83.8% sensitivity, and 89.1% speci city, which suggests that this study identi es a HIPsub pathological circuit related to SCD. The HIPe network connectivity in SCD subjects is predominantly abnormal in the brain regions involved in many aspects of emotional processing, including the cerebellum [21,22], anterior insula [21,23], parahippocampa gyrus [21,24], and fusiform gyrus [25]. Indeed, SCD subjects are characterized by self-reported concerns regarding their memory decline [26], which signi cantly increases the risk of AD [5].…”