Elsevier

Cortex

Volume 133, December 2020, Pages 236-246
Cortex

Behavioural Neurology
Using a second-person approach to identify disease-specific profiles of social behavior in frontotemporal dementia and Alzheimer's disease

https://doi.org/10.1016/j.cortex.2020.09.011Get rights and content

Abstract

Changes in social behavior are recognized as potential symptoms of behavioral-variant frontotemporal dementia (bvFTD) and semantic dementia (SD), yet objective ways to assess these behaviors in natural social situations are lacking. This study takes a truly social (or second-person) approach and examines changes in real-world social behavior in different dementia syndromes, by analyzing non-scripted social interactions in bvFTD patients (n = 20) and SD patients (n = 20), compared to patients with Alzheimer's disease (AD) (n = 20). Video recordings of 10-min conversations between patients and behavioral neurologists were analyzed for the presence of socially engaging (e.g., nodding, smiling, gesturing) and disengaging behavior (e.g., avoiding eye contact, self-grooming, interrupting). Results demonstrated disease-specific profiles, with bvFTD patients showing less nodding and more looking away than AD, and SD patients showing more gesturing than AD. A principal components analysis revealed the presence of four unobserved components, showing atypical disengaging patterns of behavior. Whole-brain voxel-based morphometry analyses revealed distinct neurobiological bases for each of these components, with the brain regions identified previously associated with behavior selection, abstract mentalization and processing of multi-sensory and socially-relevant information, in mediating socially engaging and disengaging behavior. This study demonstrates the utility of systematic behavioral observation of social interactions in the differential diagnosis of dementia.

Introduction

Traditionally, studies investigating social cognition and behavior in dementia have relied on observation paradigms, whereby the participant is required to make judgements about another person's emotions or mental state. For example, in emotion recognition studies, participants are typically exposed to static or dynamic images of emotional faces (e.g., Kumfor et al., 2011; Rosen et al., 2004), while in theory of mind studies, participants are given stories about characters and are required to make judgements on how they feel (Gregory et al., 2002). In such tasks, the participant acts as an observer rather than a participant. Generally, these tasks do not require participants to feel actively involved in a social interaction. This is in stark contrast to day-to-day life, where situations are dependent on interactions with social partners, rather than mere observations. Recently, there has been a call to complement observer-based tests with novel, second-person approaches that assess dynamically unfolding interactions between participants and a social partner (Redcay & Schilbach, 2019; Schilbach, 2016). The overarching claim of this second-person approach is that social cognition is fundamentally different when people are in interaction with others as compared to merely observing them. Second-person paradigms are expected to give a more accurate representation of daily life when studying changes in social behavior, as participants are being observed or examined while they are involved in a face-to-face interaction with an actual person (Schilbach, 2016).

Studies using observation paradigms rather than second-person paradigms have demonstrated that changes in social behavior and difficulties in reading the behavior of others are affected to varying degrees in dementia syndromes. Frontotemporal dementia appears to be uniquely characterized by changes in social behavior and capacity for social interactions. People with the behavioral-variant of frontotemporal dementia (bvFTD) show a gradual loss of empathy (e.g., Baez et al., 2016; Dermody et al., 2016; Eslinger et al., 2011; Oliver et al., 2015), changes in emotional behavior (e.g., Bozeat et al., 2000; Carr et al., 2018; Hua et al., 2018) and deficits in recognizing facial emotional expressions (e.g., Calabria et al., 2009; Kumfor & Piguet, 2012). In particular, bvFTD patients show pervasive deficits in mentalizing skills including theory of mind (Adenzato et al., 2010) and perspective taking (Dermody et al., 2016), associated with atrophy in core regions of the mentalizing network, as well as other fronto-insular regions implicated in executive functions and emotion recognition (Baez et al., 2016). In the semantic variant of primary progressive aphasia (referred to here as semantic dementia, SD), changes in language are the primary symptoms at presentation (Gorno-Tempini, 2011). It is increasingly recognized, however, that changes in social behavior are present and become more apparent with disease progression (Kumfor et al., 2017). In SD, impairment on tests of emotion recognition and theory of mind (Duval et al., 2012; Fittipaldi et al., 2019) has been associated with atrophy in the right anterior temporal lobe (Kumfor et al., 2017) and amygdala, medial prefrontal cortex and precuneus (Bejanin et al., 2017). In contrast, in Alzheimer's disease (AD), initial symptoms typically include decline in episodic memory and visuospatial abilities (McKhann, 2011; Mendez et al., 1998; Swartz et al., 1997). Unlike in bvFTD and SD, social cognitive processes remain relatively intact in AD, and appear to be modulated by progression in global cognitive deficits and left temporo-parietal atrophy (Dermody et al., 2016).

However, the overwhelming reliance on observation paradigms in previous dementia studies provides are limited in ecological validity. Systematic examination of social behaviors following a second-person approach, in which participants are observed or examined while in a face-to-face social interaction is rare, with the notable exception of two studies by Sturm et al. (2011; 2018). One study examined mutual eye gaze between dementia patients and their partner and found that mutual gaze was preserved in AD couples and diminished between people with bvFTD and their partners, while SD couples showed evidence of greater mutual gaze (Sturm et al., 2011). The other study used a helping task to assess prosocial behaviour in bvFTD, AD and controls, and found that bvFTD showed lower empathic concern, greater disengagement and impatience than AD and controls (Sturm et al., 2018). These studies demonstrate the value of employing a second-person approach. Social behavior during other interactions, for example conversations, however, has been remarkably underexplored. In healthy participants, social engagement in conversations is typically expressed by cues including smiling, head nodding, eyebrow raising, gesturing, closing distance from another person and back channeling (Hall et al., 2015). Conversely, social disengagement is typically signaled through cues including self-grooming, object manipulation, yawning, looking away and interrupting (Hall et al., 2015). Neuroimaging studies have highlighted the involvement of the mentalizing (medial prefrontal cortex, inferior frontal gyrus, temporo-parietal junction and posterior superior temporal sulcus) and mirror neuron (premotor cortex and anterior intraparietal sulcus) networks when perceiving socially engaging cues (e.g., eye contact, communicative gestures/intent) from videotaped partners (Ciaramidaro et al., 2013). Of relevance here, the brain regions implicated in processing social cues, overlap with brain regions typically affected in dementia (Kumfor et al., 2017).

This study took a second-person approach and aimed to investigate social behavior in people with bvFTD and SD. People with AD were included as a disease control. We hypothesized that people with bvFTD and SD would show abnormal social behavior compared to AD. As a secondary aim, we explored the neural correlates underpinning social behavior. Here, we hypothesized that behavioral patterns would correspond with integrity of related brain regions within in the mentalizing and mirror neuron networks.

Section snippets

Participants

Video recordings of conversations between 20 bvFTD patients, 20 SD patients, and 20 AD patients and a behavioral neurologist were analyzed. The video recordings were drawn from FRONTIER, the frontotemporal dementia research clinic based in Sydney, Australia. Participants were matched on demographics (age, sex, education, disease duration) at the group level, and had MRIs available. All participants had a good quality baseline video (i.e., wasn't blurry, had good lighting) taken at their first

Demographics and neuropsychological performance

Demographics and ACE-III test results are reported in Table 3. No significant group differences were found for age, sex, years of education or disease duration. Performance on a range of neuropsychological tests illustrated cognitive profiles consistent with what is typically reported for each syndrome. In brief, bvFTD patients showed significantly better performance than SD patients on working memory and episodic memory tasks (p < .001). SD patients showed greater language impairment than

Discussion

This study took a second-person approach to examine social behavior during conversations in bvFTD, SD and AD patients. Importantly, while previous studies have reported changes in capacity for emotion recognition (e.g., Kumfor & Piguet, 2012), empathy (e.g., Oliver et al., 2015) and theory of mind in bvFTD and SD (e.g., Gregory et al., 2002) using observer based approaches, our results revealed for one of the first times, disease-specific changes in social behavior using a second-person

Top guideline statement

The conditions of ethics regulations do not permit public archiving of the behavioral, clinical or MRI data obtained in this study. Readers seeking access to the labelling data should contact the corresponding author (FK). Access will be granted to named individuals in accordance with ethical procedures governing the reuse of sensitive data, including the completion of a formal data sharing agreement. No part of the study procedures or analyses was preregistered in an independent repository

Credit author statement

Mandy Visser, Conceptualization, Data curation, Funding acquisition, Formal analysis, Writing: original draft.

Stephanie Wong2, Conceptualization, Data curation, Formal analysis, Writing: original draft.

Simone Simonetti, Conceptualization, Formal analysis.

Jessica L Hazelton, Conceptualization, Data curation, Project administration.

Emma Devenney, Resources; Investigation.

Rebekah M. Ahmed, Resources; Investigation.

Tim van Langenhove, Resources; Investigation.

Deborah Parker, Conceptualization,

Declarations of interest

None.

Acknowledgements

We are grateful to our participants and families for their support, time and effort. This study was conducted by ForeFront, a large collaborative research group dedicated to the study of neurodegenerative diseases and funded by the National Health and Medical Research Council Program Grant (#1132524) and The ARC Centre of Excellence in Cognition and its Disorders (CE11000102). This study was supported through a Vice Chancellor's Early Career Researcher Grant 2018 for MV, by University of

References (58)

  • S. Noble et al.

    Cluster failure or power failure? Evaluating sensitivity in cluster-level inference

    Neuroimage

    (2020)
  • L.D. Oliver et al.

    Parsing cognitive and emotional empathy deficits for negative and positive stimuli in frontotemporal dementia

    Neuropsychologia

    (2015)
  • F. van Overwalle et al.

    Social cognition and the cerebellum: A meta-analysis of over 350 fMRI studies

    Neuroimage

    (2014)
  • S.M. Smith et al.

    Advances in functional and structural MR image analysis and implementation as FSL

    Neuroimage

    (2004)
  • M. Sollberger et al.

    Neural basis of interpersonal traits in neurodegenerative diseases

    Neuropsychologia

    (2009)
  • V.E. Sturm et al.

    Resting parasympathetic dysfunction predicts prosocial helping deficits in behavioral variant frontotemporal dementia

    Cortex; a Journal Devoted To the Study of the Nervous System and Behavior

    (2018)
  • M.W. Woolrich et al.

    Bayesian analysis of neuroimaging data in FSL

    Neuroimage

    (2009)
  • T.W. Anderson et al.

    Statistical inference in factor analysis

  • J.L. Andersson et al.

    Non-linear registration aka spatial normalisation FMRIB technical report TR07JA2

    (2007)
  • J.P. Barsuglia et al.

    A scale of socioemotional dysfunction in frontotemporal dementia

    Archives of Clinical Neuropsychology

    (2014)
  • A. Bejanin et al.

    Distinct neural substrates of affective and cognitive theory of mind impairment in semantic dementia

    Social Neuroscience

    (2017)
  • S. Bozeat et al.

    Which neuropsychiatric and behavioral features distinguish frontal and temporal variants of frontotemporal dementia from Alzheimer's disease?

    Journal of Neurology, Neurosurgery, and Psychiatry

    (2000)
  • A.R. Carr et al.

    Screening for emotional expression in frontotemporal dementia: A pilot study

    Behavioural Neurology

    (2018)
  • S. Charron et al.

    Divided representation of concurrent goals in the human frontal lobes

    Science

    (2010)
  • A. Ciaramidaro et al.

    Do you mean me? Communicative intentions recruit the mirror and the mentalizing system

    [Social Cognitive and Affective Neuroscience Electronic Resource]

    (2013)
  • H.H. Clark

    Using language

    (1996)
  • J. De Ruiter

    The production of gesture and speech

  • N. Dermody et al.

    Uncovering the neural bases of cognitive and affective empathy deficits in Alzheimer's disease and the behavioral-variant of frontotemporal dementia

    Journal of Alzheimer's Disease

    (2016)
  • C. Duval et al.

    Theory of mind impairments in patients with semantic dementia

    Brain: a Journal of Neurology

    (2012)
  • View full text