Multimodal investigations of structural and functional brain alterations in anorexia and bulimia nervosa and their relationships to psychopathology

IMAGEN, STRATIFY and ESTRA Consortia; Xinyang Yu; Lauren Robinson; Marina Bobou; Zuo Zhang; Tobias Banaschewski; Gareth J. Barker; Arun L.W. Bokde; Herta Flor; Antoine Grigis; Hugh Garavan; Penny Gowland; Andreas Heinz; Rüdiger Brühl; Jean-Luc Martinot; Marie-Laure Paillère Martinot; Eric Artiges; Frauke Nees; Dimitri Papadopoulos Orfanos; Hervé Lemaître; Luise Poustka; Sarah Hohmann; Nathalie Holz; Christian Bäuchl; Michael N. Smolka; Argyris Stringaris; Henrik Walter; Robert Whelan; Julia Sinclair; Gunter Schumann; Ulrike Schmidt; Sylvane Desrivières

doi:10.1016/j.biopsych.2024.11.008

Multimodal investigations of structural and functional brain alterations in anorexia and bulimia nervosa and their relationships to psychopathology

IMAGEN, STRATIFY and ESTRA Consortia
, Xinyang Yu
, Lauren Robinson
, Marina Bobou
, Zuo Zhang
, Tobias Banaschewski
, Gareth J. Barker
, Arun L.W. Bokde
, Herta Flor
, Antoine Grigis
, Hugh Garavan
, Penny Gowland
, Andreas Heinz
, Rüdiger Brühl
, Jean-Luc Martinot
, Marie-Laure Paillère Martinot
, Eric Artiges
, Frauke Nees
, Dimitri Papadopoulos Orfanos
, Hervé Lemaître

Luise Poustka, Sarah Hohmann, Nathalie Holz, Christian Bäuchl, Michael N. Smolka, Argyris Stringaris, Henrik Walter, Robert Whelan, Julia Sinclair, Gunter Schumann, Ulrike Schmidt, Sylvane Desrivières^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

Abstract

BACKGROUND: Neurobiological understanding of eating disorders (EDs) is limited. This study presents the first comparative multi-modal magnetic resonance imaging (MRI) assessments of anorexia nervosa (AN) and bulimia nervosa (BN), uncovering neurobiological differences associated with these disorders.

METHODS: This female case-control study included 57 healthy controls (HC) and 130 participants with EDs (BN and AN subtypes). Structural and functional MRI assessed gray matter volume (GMV), cortical thickness (CT), and task-based activities related to reward processing, social-emotional functioning, and response inhibition. Whole-brain group differences were correlated to ED psychopathology.

RESULTS: Significant structural differences were observed in the ED group compared to HCs, including reduced GMV in the left lateral orbitofrontal cortex and lower CT in the left rostral middle frontal gyrus and precuneus, after adjusting for BMI. Specific structural alterations were only evident in AN subgroups. GMV reductions in the orbitofrontal cortex were linked to impulsivity, while lower CT in the frontal gyrus correlated with cognitive restraint in eating, suggesting these regions may play key roles in ED psychopathology. Functional MRI also revealed notable differences. During reward anticipation, participants with EDs exhibited deactivations in the cerebellum and right superior frontal gyrus, alongside reduced activation in the left lingual gyrus. These functional changes were associated with heightened neuroticism. Mediation analyses suggested that starvation-related GMV reductions in EDs disrupt reward-related brain function, increase neuroticism, and reinforce cognitive restraint, likely contributing to the persistence of ED symptoms.

CONCLUSIONS: These findings illuminate key neurobehavioral mechanisms underlying EDs, pointing to potential brain-based targets for developing specialized treatment.

Original language	English
Journal	Biological Psychiatry
Early online date	23 Nov 2024
DOIs	https://doi.org/10.1016/j.biopsych.2024.11.008
Publication status	E-pub ahead of print - 23 Nov 2024
Externally published	Yes

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being

Keywords

Eating disorder
anorexia nervosa
bulimia nervosa
magnetic resonance imaging
cognitive restraint
reward processing

ASJC Scopus subject areas

Biological Psychiatry
Psychiatry and Mental health

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10.1016/j.biopsych.2024.11.008Licence: Creative Commons: Attribution (CC BY)

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IMAGEN, STRATIFY and ESTRA Consortia, Yu, X., Robinson, L., Bobou, M., Zhang, Z., Banaschewski, T., Barker, G. J., Bokde, A. L. W., Flor, H., Grigis, A., Garavan, H., Gowland, P., Heinz, A., Brühl, R., Martinot, J.-L., Paillère Martinot, M.-L., Artiges, E., Nees, F., Orfanos, D. P., ... Desrivières, S. (2024). Multimodal investigations of structural and functional brain alterations in anorexia and bulimia nervosa and their relationships to psychopathology. Biological Psychiatry. Advance online publication. https://doi.org/10.1016/j.biopsych.2024.11.008

@article{108699c92280491d9477383d1f91eeeb,

title = "Multimodal investigations of structural and functional brain alterations in anorexia and bulimia nervosa and their relationships to psychopathology",

abstract = "BACKGROUND: Neurobiological understanding of eating disorders (EDs) is limited. This study presents the first comparative multi-modal magnetic resonance imaging (MRI) assessments of anorexia nervosa (AN) and bulimia nervosa (BN), uncovering neurobiological differences associated with these disorders.METHODS: This female case-control study included 57 healthy controls (HC) and 130 participants with EDs (BN and AN subtypes). Structural and functional MRI assessed gray matter volume (GMV), cortical thickness (CT), and task-based activities related to reward processing, social-emotional functioning, and response inhibition. Whole-brain group differences were correlated to ED psychopathology.RESULTS: Significant structural differences were observed in the ED group compared to HCs, including reduced GMV in the left lateral orbitofrontal cortex and lower CT in the left rostral middle frontal gyrus and precuneus, after adjusting for BMI. Specific structural alterations were only evident in AN subgroups. GMV reductions in the orbitofrontal cortex were linked to impulsivity, while lower CT in the frontal gyrus correlated with cognitive restraint in eating, suggesting these regions may play key roles in ED psychopathology. Functional MRI also revealed notable differences. During reward anticipation, participants with EDs exhibited deactivations in the cerebellum and right superior frontal gyrus, alongside reduced activation in the left lingual gyrus. These functional changes were associated with heightened neuroticism. Mediation analyses suggested that starvation-related GMV reductions in EDs disrupt reward-related brain function, increase neuroticism, and reinforce cognitive restraint, likely contributing to the persistence of ED symptoms.CONCLUSIONS: These findings illuminate key neurobehavioral mechanisms underlying EDs, pointing to potential brain-based targets for developing specialized treatment.",

keywords = "Eating disorder, anorexia nervosa, bulimia nervosa, magnetic resonance imaging, cognitive restraint, reward processing",

author = "\{IMAGEN, STRATIFY and ESTRA Consortia\} and Xinyang Yu and Lauren Robinson and Marina Bobou and Zuo Zhang and Tobias Banaschewski and Barker, \{Gareth J.\} and Bokde, \{Arun L.W.\} and Herta Flor and Antoine Grigis and Hugh Garavan and Penny Gowland and Andreas Heinz and R{\"u}diger Br{\"u}hl and Jean-Luc Martinot and \{Paill{\`e}re Martinot\}, Marie-Laure and Eric Artiges and Frauke Nees and Orfanos, \{Dimitri Papadopoulos\} and Herv{\'e} Lema{\^i}tre and Luise Poustka and Sarah Hohmann and Nathalie Holz and Christian B{\"a}uchl and Smolka, \{Michael N.\} and Argyris Stringaris and Henrik Walter and Robert Whelan and Julia Sinclair and Gunter Schumann and Ulrike Schmidt and Sylvane Desrivi{\`e}res",

year = "2024",

month = nov,

day = "23",

doi = "10.1016/j.biopsych.2024.11.008",

language = "English",

journal = "Biological Psychiatry",

issn = "0006-3223",

publisher = "Elsevier",

}

IMAGEN, STRATIFY and ESTRA Consortia, Yu, X, Robinson, L, Bobou, M, Zhang, Z, Banaschewski, T, Barker, GJ, Bokde, ALW, Flor, H, Grigis, A, Garavan, H, Gowland, P, Heinz, A, Brühl, R, Martinot, J-L, Paillère Martinot, M-L, Artiges, E, Nees, F, Orfanos, DP, Lemaître, H, Poustka, L, Hohmann, S, Holz, N, Bäuchl, C, Smolka, MN, Stringaris, A, Walter, H, Whelan, R, Sinclair, J, Schumann, G, Schmidt, U & Desrivières, S 2024, 'Multimodal investigations of structural and functional brain alterations in anorexia and bulimia nervosa and their relationships to psychopathology', Biological Psychiatry. https://doi.org/10.1016/j.biopsych.2024.11.008

TY - JOUR

T1 - Multimodal investigations of structural and functional brain alterations in anorexia and bulimia nervosa and their relationships to psychopathology

AU - IMAGEN, STRATIFY and ESTRA Consortia

AU - Yu, Xinyang

AU - Robinson, Lauren

AU - Bobou, Marina

AU - Zhang, Zuo

AU - Banaschewski, Tobias

AU - Barker, Gareth J.

AU - Bokde, Arun L.W.

AU - Flor, Herta

AU - Grigis, Antoine

AU - Garavan, Hugh

AU - Gowland, Penny

AU - Heinz, Andreas

AU - Brühl, Rüdiger

AU - Martinot, Jean-Luc

AU - Paillère Martinot, Marie-Laure

AU - Artiges, Eric

AU - Nees, Frauke

AU - Orfanos, Dimitri Papadopoulos

AU - Lemaître, Hervé

AU - Poustka, Luise

AU - Hohmann, Sarah

AU - Holz, Nathalie

AU - Bäuchl, Christian

AU - Smolka, Michael N.

AU - Stringaris, Argyris

AU - Walter, Henrik

AU - Whelan, Robert

AU - Sinclair, Julia

AU - Schumann, Gunter

AU - Schmidt, Ulrike

AU - Desrivières, Sylvane

PY - 2024/11/23

Y1 - 2024/11/23

N2 - BACKGROUND: Neurobiological understanding of eating disorders (EDs) is limited. This study presents the first comparative multi-modal magnetic resonance imaging (MRI) assessments of anorexia nervosa (AN) and bulimia nervosa (BN), uncovering neurobiological differences associated with these disorders.METHODS: This female case-control study included 57 healthy controls (HC) and 130 participants with EDs (BN and AN subtypes). Structural and functional MRI assessed gray matter volume (GMV), cortical thickness (CT), and task-based activities related to reward processing, social-emotional functioning, and response inhibition. Whole-brain group differences were correlated to ED psychopathology.RESULTS: Significant structural differences were observed in the ED group compared to HCs, including reduced GMV in the left lateral orbitofrontal cortex and lower CT in the left rostral middle frontal gyrus and precuneus, after adjusting for BMI. Specific structural alterations were only evident in AN subgroups. GMV reductions in the orbitofrontal cortex were linked to impulsivity, while lower CT in the frontal gyrus correlated with cognitive restraint in eating, suggesting these regions may play key roles in ED psychopathology. Functional MRI also revealed notable differences. During reward anticipation, participants with EDs exhibited deactivations in the cerebellum and right superior frontal gyrus, alongside reduced activation in the left lingual gyrus. These functional changes were associated with heightened neuroticism. Mediation analyses suggested that starvation-related GMV reductions in EDs disrupt reward-related brain function, increase neuroticism, and reinforce cognitive restraint, likely contributing to the persistence of ED symptoms.CONCLUSIONS: These findings illuminate key neurobehavioral mechanisms underlying EDs, pointing to potential brain-based targets for developing specialized treatment.

AB - BACKGROUND: Neurobiological understanding of eating disorders (EDs) is limited. This study presents the first comparative multi-modal magnetic resonance imaging (MRI) assessments of anorexia nervosa (AN) and bulimia nervosa (BN), uncovering neurobiological differences associated with these disorders.METHODS: This female case-control study included 57 healthy controls (HC) and 130 participants with EDs (BN and AN subtypes). Structural and functional MRI assessed gray matter volume (GMV), cortical thickness (CT), and task-based activities related to reward processing, social-emotional functioning, and response inhibition. Whole-brain group differences were correlated to ED psychopathology.RESULTS: Significant structural differences were observed in the ED group compared to HCs, including reduced GMV in the left lateral orbitofrontal cortex and lower CT in the left rostral middle frontal gyrus and precuneus, after adjusting for BMI. Specific structural alterations were only evident in AN subgroups. GMV reductions in the orbitofrontal cortex were linked to impulsivity, while lower CT in the frontal gyrus correlated with cognitive restraint in eating, suggesting these regions may play key roles in ED psychopathology. Functional MRI also revealed notable differences. During reward anticipation, participants with EDs exhibited deactivations in the cerebellum and right superior frontal gyrus, alongside reduced activation in the left lingual gyrus. These functional changes were associated with heightened neuroticism. Mediation analyses suggested that starvation-related GMV reductions in EDs disrupt reward-related brain function, increase neuroticism, and reinforce cognitive restraint, likely contributing to the persistence of ED symptoms.CONCLUSIONS: These findings illuminate key neurobehavioral mechanisms underlying EDs, pointing to potential brain-based targets for developing specialized treatment.

KW - Eating disorder

KW - anorexia nervosa

KW - bulimia nervosa

KW - magnetic resonance imaging

KW - cognitive restraint

KW - reward processing

U2 - 10.1016/j.biopsych.2024.11.008

DO - 10.1016/j.biopsych.2024.11.008

M3 - Article

C2 - 39581292

SN - 0006-3223

JO - Biological Psychiatry

JF - Biological Psychiatry

ER -

Multimodal investigations of structural and functional brain alterations in anorexia and bulimia nervosa and their relationships to psychopathology

Abstract

UN SDGs

Keywords

ASJC Scopus subject areas

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