Exploration Deficits Under Ecological Conditions as a Marker of Apathy in Frontotemporal Dementia

Apathy is one of the six clinical criteria for the behavioral variant of frontotemporal dementia (bvFTD), and it is almost universal in this disease. Although its consequences in everyday life are debilitating, its underlying mechanisms are poorly known, its assessment is biased by subjectivity and...

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Main Authors: Bénédicte Batrancourt, Karen Lecouturier, Johan Ferrand-Verdejo, Vincent Guillemot, Carole Azuar, David Bendetowicz, Raffaella Migliaccio, Armelle Rametti-Lacroux, Bruno Dubois, Richard Levy
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-08-01
Series:Frontiers in Neurology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fneur.2019.00941/full
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author Bénédicte Batrancourt
Karen Lecouturier
Johan Ferrand-Verdejo
Vincent Guillemot
Carole Azuar
David Bendetowicz
David Bendetowicz
David Bendetowicz
Raffaella Migliaccio
Raffaella Migliaccio
Raffaella Migliaccio
Armelle Rametti-Lacroux
Bruno Dubois
Bruno Dubois
Richard Levy
Richard Levy
Richard Levy
spellingShingle Bénédicte Batrancourt
Karen Lecouturier
Johan Ferrand-Verdejo
Vincent Guillemot
Carole Azuar
David Bendetowicz
David Bendetowicz
David Bendetowicz
Raffaella Migliaccio
Raffaella Migliaccio
Raffaella Migliaccio
Armelle Rametti-Lacroux
Bruno Dubois
Bruno Dubois
Richard Levy
Richard Levy
Richard Levy
Exploration Deficits Under Ecological Conditions as a Marker of Apathy in Frontotemporal Dementia
Frontiers in Neurology
apathy
disinhibition
motivation
frontotemporal lobar degeneration
behavior
neurodegenerative diseases
author_facet Bénédicte Batrancourt
Karen Lecouturier
Johan Ferrand-Verdejo
Vincent Guillemot
Carole Azuar
David Bendetowicz
David Bendetowicz
David Bendetowicz
Raffaella Migliaccio
Raffaella Migliaccio
Raffaella Migliaccio
Armelle Rametti-Lacroux
Bruno Dubois
Bruno Dubois
Richard Levy
Richard Levy
Richard Levy
author_sort Bénédicte Batrancourt
title Exploration Deficits Under Ecological Conditions as a Marker of Apathy in Frontotemporal Dementia
title_short Exploration Deficits Under Ecological Conditions as a Marker of Apathy in Frontotemporal Dementia
title_full Exploration Deficits Under Ecological Conditions as a Marker of Apathy in Frontotemporal Dementia
title_fullStr Exploration Deficits Under Ecological Conditions as a Marker of Apathy in Frontotemporal Dementia
title_full_unstemmed Exploration Deficits Under Ecological Conditions as a Marker of Apathy in Frontotemporal Dementia
title_sort exploration deficits under ecological conditions as a marker of apathy in frontotemporal dementia
publisher Frontiers Media S.A.
series Frontiers in Neurology
issn 1664-2295
publishDate 2019-08-01
description Apathy is one of the six clinical criteria for the behavioral variant of frontotemporal dementia (bvFTD), and it is almost universal in this disease. Although its consequences in everyday life are debilitating, its underlying mechanisms are poorly known, its assessment is biased by subjectivity and its care management is very limited. In this context, we have developed “ECOCAPTURE,” a method aimed at providing quantifiable and objective signature(s) of apathy in order to assess it and identify its precise underlying mechanisms. ECOCAPTURE consists of the observation and recording of the patient's behavior when the participant is being submitted to a multiple-phase scenario reproducing a brief real-life situation. It is performed in a functional exploration platform transformed into a fully furnished waiting room equipped with a video and sensor-based data acquisition system. This multimodal method allowed video-based behavior analyses according to predefined behavioral categories (exploration behavior, sustained activities or inactivity) and actigraphy analyses from a 3D accelerometer. The data obtained were also correlated with behavioral/cognitive tests and scales assessing global cognitive efficiency, apathy, cognitive disinhibition, frontal syndrome, depression and anxiety. Here, bvFTD patients (n = 14) were compared to healthy participants (n = 14) during the very first minutes of the scenario, when the participants discovered the room and were encouraged to explore it. We showed that, in the context of facing a new environment, healthy participants first explored it and then engaged in sustained activities. By contrast, bvFTD patients were mostly inactive and eventually explored this new place, but in a more irregular and less efficient mode than normal subjects. This exploration deficit was correlated with apathy, disinhibition and cognitive and behavioral dysexecutive syndromes. These findings led us to discuss the presumed underlying mechanisms responsible for the exploration deficit (an inability to self-initiate actions, to integrate reward valuation and to inhibit involuntary behavior). Altogether, these results pave the way for simple and objective assessment of behavioral changes that represents a critical step for the evaluation of disease progression and efficacy of treatment in bvFTD.
topic apathy
disinhibition
motivation
frontotemporal lobar degeneration
behavior
neurodegenerative diseases
url https://www.frontiersin.org/article/10.3389/fneur.2019.00941/full
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spelling doaj-8cc0197cde3346329c27587f9f5085ec2020-11-25T01:40:09ZengFrontiers Media S.A.Frontiers in Neurology1664-22952019-08-011010.3389/fneur.2019.00941452586Exploration Deficits Under Ecological Conditions as a Marker of Apathy in Frontotemporal DementiaBénédicte Batrancourt0Karen Lecouturier1Johan Ferrand-Verdejo2Vincent Guillemot3Carole Azuar4David Bendetowicz5David Bendetowicz6David Bendetowicz7Raffaella Migliaccio8Raffaella Migliaccio9Raffaella Migliaccio10Armelle Rametti-Lacroux11Bruno Dubois12Bruno Dubois13Richard Levy14Richard Levy15Richard Levy16Inserm U 1127, CNRS UMR 7225, Sorbonne Universités, UPMC Univ Paris 06, Institut du Cerveau et de la Moelle épiniére (ICM), FRONTlab, Paris, FranceInserm U 1127, CNRS UMR 7225, Sorbonne Universités, UPMC Univ Paris 06, Institut du Cerveau et de la Moelle épiniére (ICM), FRONTlab, Paris, FranceInserm U 1127, CNRS UMR 7225, Sorbonne Universités, UPMC Univ Paris 06, Institut du Cerveau et de la Moelle épiniére (ICM), FRONTlab, Paris, FranceInstitut Pasteur, Centre de Bioinformatique, Biostatistique et Biologie Intégrative (C3BI), Paris, FranceAP-HP, Groupe Hospitalier Pitiè-Salpêtrière, Département de Neurologie, Institut de la Mèmoire et de la Maladie d'Alzheimer (IM2A), Paris, FranceInserm U 1127, CNRS UMR 7225, Sorbonne Universités, UPMC Univ Paris 06, Institut du Cerveau et de la Moelle épiniére (ICM), FRONTlab, Paris, FranceAP-HP, Groupe Hospitalier Pitiè-Salpêtrière, Département de Neurologie, Institut de la Mèmoire et de la Maladie d'Alzheimer (IM2A), Paris, FranceAP-HP, Groupe Hospitalier Pitiè-Salpêtrière, Département de Neurologie, Behavioral Neuropsychiatry Unit, Paris, FranceInserm U 1127, CNRS UMR 7225, Sorbonne Universités, UPMC Univ Paris 06, Institut du Cerveau et de la Moelle épiniére (ICM), FRONTlab, Paris, FranceAP-HP, Groupe Hospitalier Pitiè-Salpêtrière, Département de Neurologie, Institut de la Mèmoire et de la Maladie d'Alzheimer (IM2A), Paris, FranceAP-HP, Groupe Hospitalier Pitiè-Salpêtrière, Département de Neurologie, Behavioral Neuropsychiatry Unit, Paris, FranceInserm U 1127, CNRS UMR 7225, Sorbonne Universités, UPMC Univ Paris 06, Institut du Cerveau et de la Moelle épiniére (ICM), FRONTlab, Paris, FranceInserm U 1127, CNRS UMR 7225, Sorbonne Universités, UPMC Univ Paris 06, Institut du Cerveau et de la Moelle épiniére (ICM), FRONTlab, Paris, FranceAP-HP, Groupe Hospitalier Pitiè-Salpêtrière, Département de Neurologie, Institut de la Mèmoire et de la Maladie d'Alzheimer (IM2A), Paris, FranceInserm U 1127, CNRS UMR 7225, Sorbonne Universités, UPMC Univ Paris 06, Institut du Cerveau et de la Moelle épiniére (ICM), FRONTlab, Paris, FranceAP-HP, Groupe Hospitalier Pitiè-Salpêtrière, Département de Neurologie, Institut de la Mèmoire et de la Maladie d'Alzheimer (IM2A), Paris, FranceAP-HP, Groupe Hospitalier Pitiè-Salpêtrière, Département de Neurologie, Behavioral Neuropsychiatry Unit, Paris, FranceApathy is one of the six clinical criteria for the behavioral variant of frontotemporal dementia (bvFTD), and it is almost universal in this disease. Although its consequences in everyday life are debilitating, its underlying mechanisms are poorly known, its assessment is biased by subjectivity and its care management is very limited. In this context, we have developed “ECOCAPTURE,” a method aimed at providing quantifiable and objective signature(s) of apathy in order to assess it and identify its precise underlying mechanisms. ECOCAPTURE consists of the observation and recording of the patient's behavior when the participant is being submitted to a multiple-phase scenario reproducing a brief real-life situation. It is performed in a functional exploration platform transformed into a fully furnished waiting room equipped with a video and sensor-based data acquisition system. This multimodal method allowed video-based behavior analyses according to predefined behavioral categories (exploration behavior, sustained activities or inactivity) and actigraphy analyses from a 3D accelerometer. The data obtained were also correlated with behavioral/cognitive tests and scales assessing global cognitive efficiency, apathy, cognitive disinhibition, frontal syndrome, depression and anxiety. Here, bvFTD patients (n = 14) were compared to healthy participants (n = 14) during the very first minutes of the scenario, when the participants discovered the room and were encouraged to explore it. We showed that, in the context of facing a new environment, healthy participants first explored it and then engaged in sustained activities. By contrast, bvFTD patients were mostly inactive and eventually explored this new place, but in a more irregular and less efficient mode than normal subjects. This exploration deficit was correlated with apathy, disinhibition and cognitive and behavioral dysexecutive syndromes. These findings led us to discuss the presumed underlying mechanisms responsible for the exploration deficit (an inability to self-initiate actions, to integrate reward valuation and to inhibit involuntary behavior). Altogether, these results pave the way for simple and objective assessment of behavioral changes that represents a critical step for the evaluation of disease progression and efficacy of treatment in bvFTD.https://www.frontiersin.org/article/10.3389/fneur.2019.00941/fullapathydisinhibitionmotivationfrontotemporal lobar degenerationbehaviorneurodegenerative diseases