Beyond the face: how context modulates emotion processing in frontotemporal dementia subtypes

Abstract

The importance of assessing social cognition to characterize dementia syndromes is increasingly recognized, with lower social cognition capacity associated with reduced functional independence and greater carer burden. Emotion recognition is impaired in both behavioural-variant frontotemporal dementia and semantic dementia, yet the social and behavioural changes observed in these syndromes in everyday situations varies. To date, most studies have investigated isolated, context-free stimuli indexing recognition of facial emotions only. Here, we aimed to investigate how contextual information (i.e. emotional body language) influences emotion recognition, within the framework of the Social Context Network Model. Thirty-one patients with frontotemporal dementia (19 behavioural-variant frontotemporal dementia; 12 semantic dementia) and 20 healthy age- and education-matched controls were assessed on three tasks which varied contextual cues: (i) face alone; (ii) context alone; and (iii) face embedded in context. Voxel-based morphometry was used to identify neural correlates of task performance. Our results demonstrated that both behavioural-variant frontotemporal dementia and semantic dementia patients performed worse than controls in recognizing emotions from face alone and context alone. Importantly, performance differed when faces were presented in context. While both behavioural-variant frontotemporal dementia and semantic dementia patients performed similarly to controls on congruent items (i.e. face emotion and body emotion are the same) (P-values > 0.05), patients with behavioural-variant frontotemporal dementia performed worse than both controls (P < 0.001) and patients with semantic dementia (P = 0.044) for incongruent items (i.e. face emotion and body emotion are different). Neuroimaging analyses revealed that abnormal contextual influence was associated with lower integrity of the right parahippocampal gyrus/amygdala and left precentral gyrus. Together, these results indicate that patients with behavioural-variant frontotemporal dementia are over-reliant on external contextual information. Conversely, in semantic dementia and controls, contextual influence varies, with the degree of contextual influence appearing to be mediated, at least in part, by the facial expression depicted. The profile in behavioural-variant frontotemporal dementia is reminiscent of the 'environmental dependency syndrome' described in frontal lesion patients. It also converges with recent evidence of abnormal face perception in this group. From a theoretical perspective, our findings demonstrate that the capacity to incorporate contextual body language is dependent on the integrity of both contextual association brain regions (i.e. parahippocampal gyrus), as well as regions necessary for processing dynamic body movements. Clinically, these results open new avenues for rehabilitation of social impairments in dementia.

Effect of Acute Physical Exercise on Executive Functions and Emotional Recognition: Analysis of Moderate to High Intensity in Young Adults

“…Studies, which are carried out by magnetic functional resonance (fMRI), have demonstrated that body emotional posture influence in facial expression processing (Poyo-Solanas et al, 2018). Moreover, it has been suggested that the regions that are in charge of processing dynamic body movements are linked to emotional and body recognition (Kumfor et al, 2018). Using tasks of the same kind of our study, emotional recognition patterns in context in teenagers with criminal conduct have been explored (Santamaría-García et al, 2019), and with patients who suffer from frontotemporal dementia (Kumfor et al, 2018).…”

“…In that way, understanding how environmental factors, such as PE, contribute to the performance of emotional recognition in context, and in ecological situations, is a novel area that answers to current questionings of social and cognitive neuroscience (Aviezer et al, 2008;Kumfor et al, 2018). We assumed that acute PE has positive effects on emotional recognition.…”

“…Especially, whenever the aerobic exercise is combined with the demands of coordination seems that it gets more benefits on facial emotion recognition (Brand et al, 2019). In fact, the capacity of information processing, which links body movements with body-face recognition (Kumfor et al, 2018), is associated with brain regions such as motor areas, cerebellum, and fusiform gyrus (Committeri et al, 2007;Yogev-Seligmann et al, 2008), that are connected with the acute PE (Li et al, 2014;Esteban-Cornejo et al, 2019;Won et al, 2019). Recent paradigms on emotional recognition have located body information as contextual keys, taking away attention from facial recognition processing (Aviezer et al, 2008(Aviezer et al, , 2012.…”

Cerebellar atrophy and its contribution to cognition in frontotemporal dementias

“…Structural and functional abnormalities of the cerebellum are present in numerous developmental and acquired neurological conditions, such as developmental dyslexia, autism spectrum disorders, alcohol‐related brain damage, movement disorders (eg, Friedreich ataxia, Parkinson disease, Huntington disease), dementia (eg, Alzheimer disease [AD], dementia with Lewy bodies, frontotemporal dementia), and psychiatric disorders . The contribution of the cerebellum to motor coordination and motor planning is well known, but many studies have downplayed its involvement in other domains despite the mounting evidence over the past 30 years (eg, language, social cognition, interoception).…”

Regional and hemispheric susceptibility of the temporal lobe to FTLD-TDP type C pathology

“…Despite the robust size of this pathology-proven cohort, future studies including more subjects are warranted. Moreover, this retrospective, path confirmed study includes relatively old cases, so the neuropsychological data available do not include more recent measures such as Famous Faces Naming or Emotion Processing tasks (Kumfor et al, 2018). Larger samples, including the more targeted neuropsychological tests now available, will allow more refined investigation of the neural correlates of specific phenotypical characteristics of TDP-43-C driven temporal FTDs.…”