Motor signatures of emotional reactivity in frontotemporal dementia

Charles R Marshall,Jonathan D Rohrer,James M Kilner,Lucy L Russell,Emilie V Brotherhood,Cath J Mummery,Rebecca L Bond,Jason D Warren,Camilla N Clark,Katrina M Dick,Jonathan M Schott,Chris J D Hardy

doi:10.1038/s41598-018-19528-2

Abstract

Automatic motor mimicry is essential to the normal processing of perceived emotion, and disrupted automatic imitation might underpin socio-emotional deficits in neurodegenerative diseases, particularly the frontotemporal dementias. However, the pathophysiology of emotional reactivity in these diseases has not been elucidated. We studied facial electromyographic responses during emotion identification on viewing videos of dynamic facial expressions in 37 patients representing canonical frontotemporal dementia syndromes versus 21 healthy older individuals. Neuroanatomical associations of emotional expression identification accuracy and facial muscle reactivity were assessed using voxel-based morphometry. Controls showed characteristic profiles of automatic imitation, and this response predicted correct emotion identification. Automatic imitation was reduced in the behavioural and right temporal variant groups, while the normal coupling between imitation and correct identification was lost in the right temporal and semantic variant groups. Grey matter correlates of emotion identification and imitation were delineated within a distributed network including primary visual and motor, prefrontal, insular, anterior temporal and temporo-occipital junctional areas, with common involvement of supplementary motor cortex across syndromes. Impaired emotional mimesis may be a core mechanism of disordered emotional signal understanding and reactivity in frontotemporal dementia, with implications for the development of novel physiological biomarkers of socio-emotional dysfunction in these diseases.

Highlights

Motor mimicry supports the decoding of perceived emotions by the healthy brain[1,2]
We investigated facial motor responses to viewing facial emotional expressions in a cohort of patients representing all major phenotypes of frontotemporal dementias (FTD) relative to healthy older individuals
We predicted that bvFTD and rtvFTD would be associated with reduced EMG responses while semantic variant primary progressive aphasia (svPPA) would be associated with aberrant coupling of muscle reactivity to emotion identification and nonfluent variant primary progressive aphasia (nfvPPA) with a more selective, emotion-specific reactivity profile

Summary

Introduction

Motor mimicry supports the decoding of perceived emotions by the healthy brain[1,2]. Viewing emotional facial expressions rapidly and involuntarily engages the facial muscles of neurologically normal observers[3,4]. Based on previous neuroimaging studies both in the healthy brain and in FTD14,23,26,45,48–50, we further hypothesised that facial emotion identification and EMG reactivity would have partly overlapping neuroanatomical correlates within the extensive cortical circuitry previously implicated in the decoding of visual emotional signals, supplementary motor and insular cortices mediating the integration of somatic representations and antero-medial temporal and prefrontal circuitry involved in the evaluation of emotion Within these distributed networks (given the known neuroanatomical heterogeneity of the target syndromes) we predicted a differential emphasis of grey matter correlates, with more marked involvement of inferior frontal, anterior cingulate and insular cortices in bvFTD and nfvPPA and more extensive, lateralised temporal lobe involvement in svPPA and rtvFTD16–18

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Conclusion