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Dorsolateral prefrontal cortex and amygdala function during cognitive reappraisal predicts weight restoration and emotion regulation impairment in anorexia nervosa

Published online by Cambridge University Press:  23 July 2020

Trevor Steward Open the ORCID record for Trevor Steward [Opens in a new window] ,
Ignacio Martínez-Zalacaín Open the ORCID record for Ignacio Martínez-Zalacaín [Opens in a new window] ,
Gemma Mestre-Bach Open the ORCID record for Gemma Mestre-Bach [Opens in a new window] ,
Isabel Sánchez Open the ORCID record for Isabel Sánchez [Opens in a new window] ,
Nadine Riesco Open the ORCID record for Nadine Riesco [Opens in a new window] ,
Susana Jiménez-Murcia Open the ORCID record for Susana Jiménez-Murcia [Opens in a new window] ,
Jose A Fernández-Formoso Open the ORCID record for Jose A Fernández-Formoso [Opens in a new window] ,
Misericordia Veciana de las Heras Open the ORCID record for Misericordia Veciana de las Heras [Opens in a new window] ,
Nuria Custal Open the ORCID record for Nuria Custal [Opens in a new window]  and
Jose M Menchón Open the ORCID record for Jose M Menchón [Opens in a new window]
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Trevor Steward
Affiliation:
Melbourne School of Psychological Sciences, Faculty of Medicine, Dentistry and Health Sciences, University of Melbourne, Melbourne, Australia Ciber Fisiopatología Obesidad y Nutrición (CIBEROBN), Instituto Salud Carlos III, Barcelona, Spain Department of Psychiatry, Bellvitge University Hospital -IDIBELL, Barcelona, Spain
Ignacio Martínez-Zalacaín
Affiliation:
Department of Psychiatry, Bellvitge University Hospital -IDIBELL, Barcelona, Spain Department of Clinical Sciences, School of Medicine, University of Barcelona, Barcelona, Spain
Gemma Mestre-Bach
Affiliation:
Ciber Fisiopatología Obesidad y Nutrición (CIBEROBN), Instituto Salud Carlos III, Barcelona, Spain Department of Psychiatry, Bellvitge University Hospital -IDIBELL, Barcelona, Spain Facultad de Ciencias de la Salud, Universidad Internacional de La Rioja, La Rioja, Spain
Isabel Sánchez
Affiliation:
Ciber Fisiopatología Obesidad y Nutrición (CIBEROBN), Instituto Salud Carlos III, Barcelona, Spain Department of Psychiatry, Bellvitge University Hospital -IDIBELL, Barcelona, Spain
Nadine Riesco
Affiliation:
Ciber Fisiopatología Obesidad y Nutrición (CIBEROBN), Instituto Salud Carlos III, Barcelona, Spain Department of Psychiatry, Bellvitge University Hospital -IDIBELL, Barcelona, Spain
Susana Jiménez-Murcia
Affiliation:
Ciber Fisiopatología Obesidad y Nutrición (CIBEROBN), Instituto Salud Carlos III, Barcelona, Spain Department of Psychiatry, Bellvitge University Hospital -IDIBELL, Barcelona, Spain Department of Clinical Sciences, School of Medicine, University of Barcelona, Barcelona, Spain
Jose A Fernández-Formoso
Affiliation:
Ciber Fisiopatología Obesidad y Nutrición (CIBEROBN), Instituto Salud Carlos III, Barcelona, Spain
Misericordia Veciana de las Heras
Affiliation:
Neurology Department, Bellvitge University Hospital-IDIBELL, Barcelona, Spain
Nuria Custal
Affiliation:
Department of Psychiatry, Bellvitge University Hospital -IDIBELL, Barcelona, Spain
Jose M Menchón
Affiliation:
Department of Psychiatry, Bellvitge University Hospital -IDIBELL, Barcelona, Spain Department of Clinical Sciences, School of Medicine, University of Barcelona, Barcelona, Spain Ciber Mental Health (CIBERSAM), Instituto Salud Carlos III, Barcelona, Spain
Carles Soriano-Mas*
Affiliation:
Department of Psychiatry, Bellvitge University Hospital -IDIBELL, Barcelona, Spain Ciber Mental Health (CIBERSAM), Instituto Salud Carlos III, Barcelona, Spain Department of Psychobiology and Methodology, Universitat Autònoma de Barcelona, Barcelona, Spain
Fernando Fernandez-Aranda*
Affiliation:
Ciber Fisiopatología Obesidad y Nutrición (CIBEROBN), Instituto Salud Carlos III, Barcelona, Spain Department of Psychiatry, Bellvitge University Hospital -IDIBELL, Barcelona, Spain Department of Clinical Sciences, School of Medicine, University of Barcelona, Barcelona, Spain
*
Author for correspondence: Fernando Fernández-Aranda, E-mail: [email protected], Carles Soriano-Mas, E-mail: [email protected]
Author for correspondence: Fernando Fernández-Aranda, E-mail: [email protected], Carles Soriano-Mas, E-mail: [email protected]
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Abstract

Background

Although deficits in affective processing are a core component of anorexia nervosa (AN), we lack a detailed characterization of the neurobiological underpinnings of emotion regulation impairment in AN. Moreover, it remains unclear whether these neural correlates scale with clinical outcomes.

Methods

We investigated the neural correlates of negative emotion regulation in a sample of young women receiving day-hospital treatment for AN (n = 21) and healthy controls (n = 21). We aimed to determine whether aberrant brain activation patterns during emotion regulation predicted weight gain following treatment in AN patients and were linked to AN severity. To achieve this, participants completed a cognitive reappraisal paradigm during functional magnetic resonance imaging. Skin conductance response, as well as subjective distress ratings, were recorded to corroborate task engagement.

Results

Compared to controls, patients with AN showed reduced activation in the dorsolateral prefrontal cortex (dlPFC) during cognitive reappraisal [pFWE<0.05, threshold-free cluster enhancement (TFCE) corrected]. Importantly, psycho–physiological interaction analysis revealed reduced functional connectivity between the dlPFC and the amygdala in AN patients during emotion regulation (pFWE<0.05, TFCE corrected), and dlPFC-amygdala uncoupling was associated with emotion regulation deficits (r = −0.511, p = 0.018) and eating disorder severity (r = −0.565, p = .008) in the AN group. Finally, dlPFC activity positively correlated with increases in body mass index (r = 0.471, p = 0.042) and in body fat mass percentage (r = 0.605, p = 0.008) following 12 weeks of treatment.

Conclusions

Taken together, our findings indicate that individuals with AN present altered fronto-amygdalar response during cognitive reappraisal and that this response may serve as a predictor of response to treatment and be linked to clinical severity.

Keywords

Anorexia nervosacognitive reappraisaleating disordersemotion regulationfMRI
Type
Original Article
Information
Psychological Medicine , Volume 52 , Issue 5 , April 2022 , pp. 844 - 852
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Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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Footnotes

*

These authors contributed equally to this work.

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