Neural activation of regions involved in food reward and cognitive control in young females with anorexia nervosa and atypical anorexia nervosa versus healthy controls

Abstract Anorexia nervosa (AN) and atypical AN (AtypAN) are complex neurobiological illnesses that typically onset in adolescence with an often treatment-refractory and chronic illness trajectory. Aberrant eating behaviors in this population have been linked to abnormalities in food reward and cogni...

Full description

Bibliographic Details
Main Authors: Kamryn T. Eddy, Franziska Plessow, Lauren Breithaupt, Kendra R. Becker, Meghan Slattery, Christopher J. Mancuso, Alyssa M. Izquierdo, Avery L. Van De Water, Danielle L. Kahn, Melissa J. Dreier, Seda Ebrahimi, Thilo Deckersbach, Jennifer J. Thomas, Laura M. Holsen, Madhusmita Misra, Elizabeth A. Lawson
Format: Article
Language:English
Published: Nature Publishing Group 2023-06-01
Series:Translational Psychiatry
Online Access:https://doi.org/10.1038/s41398-023-02494-3
_version_ 1827916711401095168
author Kamryn T. Eddy
Franziska Plessow
Lauren Breithaupt
Kendra R. Becker
Meghan Slattery
Christopher J. Mancuso
Alyssa M. Izquierdo
Avery L. Van De Water
Danielle L. Kahn
Melissa J. Dreier
Seda Ebrahimi
Thilo Deckersbach
Jennifer J. Thomas
Laura M. Holsen
Madhusmita Misra
Elizabeth A. Lawson
author_facet Kamryn T. Eddy
Franziska Plessow
Lauren Breithaupt
Kendra R. Becker
Meghan Slattery
Christopher J. Mancuso
Alyssa M. Izquierdo
Avery L. Van De Water
Danielle L. Kahn
Melissa J. Dreier
Seda Ebrahimi
Thilo Deckersbach
Jennifer J. Thomas
Laura M. Holsen
Madhusmita Misra
Elizabeth A. Lawson
author_sort Kamryn T. Eddy
collection DOAJ
description Abstract Anorexia nervosa (AN) and atypical AN (AtypAN) are complex neurobiological illnesses that typically onset in adolescence with an often treatment-refractory and chronic illness trajectory. Aberrant eating behaviors in this population have been linked to abnormalities in food reward and cognitive control, but prior studies have not examined respective contributions of clinical characteristics and metabolic state. Research is needed to identify specific disruptions and inform novel intervention targets to improve outcomes. Fifty-nine females with AN (n = 34) or AtypAN (n = 25), ages 10–22 years, all ≤90% expected body weight, and 34 age-matched healthy controls (HC) completed a well-established neuroimaging food cue paradigm fasting and after a standardized meal, and we used ANCOVA models to investigate main and interaction effects of Group and Appetitive State on blood oxygenation level-dependent (BOLD) activation for the contrast of exposure to high-calorie food images minus objects. We found main effects of Group with greater BOLD activation in the dorsal anterior cingulate cortex (dACC), dorsolateral prefrontal cortex (DLPFC), hippocampus, caudate, and putamen for AN/AtypAN versus HC groups, and in the three-group model including AN, AtypAN, and HC (sub-)groups, where differences were primarily driven by greater activation in the AtypAN subgroup versus HC group. We found a main effect of Appetitive State with increased premeal BOLD activation in the hypothalamus, amygdala, nucleus accumbens, and caudate for models that included AN/AtypAN and HC groups, and in BOLD activation in the nucleus accumbens for the model that included AN, AtypAN, and HC (sub-)groups. There were no interaction effects of Group with Appetitive State for any of the models. Our findings demonstrate robust feeding-state independent group effects reflecting greater neural activation of specific regions typically associated with reward and cognitive control processing across AN and AtypAN relative to healthy individuals in this food cue paradigm. Differential activation of specific brain regions in response to the passive viewing of high-calorie food images may underlie restrictive eating behavior in this clinical population.
first_indexed 2024-03-13T03:19:08Z
format Article
id doaj.art-687dfa51fe654ab4af007bf3f19aded3
institution Directory Open Access Journal
issn 2158-3188
language English
last_indexed 2024-03-13T03:19:08Z
publishDate 2023-06-01
publisher Nature Publishing Group
record_format Article
series Translational Psychiatry
spelling doaj.art-687dfa51fe654ab4af007bf3f19aded32023-06-25T11:29:57ZengNature Publishing GroupTranslational Psychiatry2158-31882023-06-0113111010.1038/s41398-023-02494-3Neural activation of regions involved in food reward and cognitive control in young females with anorexia nervosa and atypical anorexia nervosa versus healthy controlsKamryn T. Eddy0Franziska Plessow1Lauren Breithaupt2Kendra R. Becker3Meghan Slattery4Christopher J. Mancuso5Alyssa M. Izquierdo6Avery L. Van De Water7Danielle L. Kahn8Melissa J. Dreier9Seda Ebrahimi10Thilo Deckersbach11Jennifer J. Thomas12Laura M. Holsen13Madhusmita Misra14Elizabeth A. Lawson15Eating Disorders Clinical and Research Program, Massachusetts General HospitalNeuroendocrine Unit, Massachusetts General HospitalEating Disorders Clinical and Research Program, Massachusetts General HospitalEating Disorders Clinical and Research Program, Massachusetts General HospitalNeuroendocrine Unit, Massachusetts General HospitalNeuroendocrine Unit, Massachusetts General HospitalNeuroendocrine Unit, Massachusetts General HospitalNeuroendocrine Unit, Massachusetts General HospitalNeuroendocrine Unit, Massachusetts General HospitalEating Disorders Clinical and Research Program, Massachusetts General HospitalCambridge Eating Disorders CenterDepartment of Psychiatry, Harvard Medical SchoolEating Disorders Clinical and Research Program, Massachusetts General HospitalDepartment of Psychiatry, Harvard Medical SchoolNeuroendocrine Unit, Massachusetts General HospitalNeuroendocrine Unit, Massachusetts General HospitalAbstract Anorexia nervosa (AN) and atypical AN (AtypAN) are complex neurobiological illnesses that typically onset in adolescence with an often treatment-refractory and chronic illness trajectory. Aberrant eating behaviors in this population have been linked to abnormalities in food reward and cognitive control, but prior studies have not examined respective contributions of clinical characteristics and metabolic state. Research is needed to identify specific disruptions and inform novel intervention targets to improve outcomes. Fifty-nine females with AN (n = 34) or AtypAN (n = 25), ages 10–22 years, all ≤90% expected body weight, and 34 age-matched healthy controls (HC) completed a well-established neuroimaging food cue paradigm fasting and after a standardized meal, and we used ANCOVA models to investigate main and interaction effects of Group and Appetitive State on blood oxygenation level-dependent (BOLD) activation for the contrast of exposure to high-calorie food images minus objects. We found main effects of Group with greater BOLD activation in the dorsal anterior cingulate cortex (dACC), dorsolateral prefrontal cortex (DLPFC), hippocampus, caudate, and putamen for AN/AtypAN versus HC groups, and in the three-group model including AN, AtypAN, and HC (sub-)groups, where differences were primarily driven by greater activation in the AtypAN subgroup versus HC group. We found a main effect of Appetitive State with increased premeal BOLD activation in the hypothalamus, amygdala, nucleus accumbens, and caudate for models that included AN/AtypAN and HC groups, and in BOLD activation in the nucleus accumbens for the model that included AN, AtypAN, and HC (sub-)groups. There were no interaction effects of Group with Appetitive State for any of the models. Our findings demonstrate robust feeding-state independent group effects reflecting greater neural activation of specific regions typically associated with reward and cognitive control processing across AN and AtypAN relative to healthy individuals in this food cue paradigm. Differential activation of specific brain regions in response to the passive viewing of high-calorie food images may underlie restrictive eating behavior in this clinical population.https://doi.org/10.1038/s41398-023-02494-3
spellingShingle Kamryn T. Eddy
Franziska Plessow
Lauren Breithaupt
Kendra R. Becker
Meghan Slattery
Christopher J. Mancuso
Alyssa M. Izquierdo
Avery L. Van De Water
Danielle L. Kahn
Melissa J. Dreier
Seda Ebrahimi
Thilo Deckersbach
Jennifer J. Thomas
Laura M. Holsen
Madhusmita Misra
Elizabeth A. Lawson
Neural activation of regions involved in food reward and cognitive control in young females with anorexia nervosa and atypical anorexia nervosa versus healthy controls
Translational Psychiatry
title Neural activation of regions involved in food reward and cognitive control in young females with anorexia nervosa and atypical anorexia nervosa versus healthy controls
title_full Neural activation of regions involved in food reward and cognitive control in young females with anorexia nervosa and atypical anorexia nervosa versus healthy controls
title_fullStr Neural activation of regions involved in food reward and cognitive control in young females with anorexia nervosa and atypical anorexia nervosa versus healthy controls
title_full_unstemmed Neural activation of regions involved in food reward and cognitive control in young females with anorexia nervosa and atypical anorexia nervosa versus healthy controls
title_short Neural activation of regions involved in food reward and cognitive control in young females with anorexia nervosa and atypical anorexia nervosa versus healthy controls
title_sort neural activation of regions involved in food reward and cognitive control in young females with anorexia nervosa and atypical anorexia nervosa versus healthy controls
url https://doi.org/10.1038/s41398-023-02494-3
work_keys_str_mv AT kamrynteddy neuralactivationofregionsinvolvedinfoodrewardandcognitivecontrolinyoungfemaleswithanorexianervosaandatypicalanorexianervosaversushealthycontrols
AT franziskaplessow neuralactivationofregionsinvolvedinfoodrewardandcognitivecontrolinyoungfemaleswithanorexianervosaandatypicalanorexianervosaversushealthycontrols
AT laurenbreithaupt neuralactivationofregionsinvolvedinfoodrewardandcognitivecontrolinyoungfemaleswithanorexianervosaandatypicalanorexianervosaversushealthycontrols
AT kendrarbecker neuralactivationofregionsinvolvedinfoodrewardandcognitivecontrolinyoungfemaleswithanorexianervosaandatypicalanorexianervosaversushealthycontrols
AT meghanslattery neuralactivationofregionsinvolvedinfoodrewardandcognitivecontrolinyoungfemaleswithanorexianervosaandatypicalanorexianervosaversushealthycontrols
AT christopherjmancuso neuralactivationofregionsinvolvedinfoodrewardandcognitivecontrolinyoungfemaleswithanorexianervosaandatypicalanorexianervosaversushealthycontrols
AT alyssamizquierdo neuralactivationofregionsinvolvedinfoodrewardandcognitivecontrolinyoungfemaleswithanorexianervosaandatypicalanorexianervosaversushealthycontrols
AT averylvandewater neuralactivationofregionsinvolvedinfoodrewardandcognitivecontrolinyoungfemaleswithanorexianervosaandatypicalanorexianervosaversushealthycontrols
AT daniellelkahn neuralactivationofregionsinvolvedinfoodrewardandcognitivecontrolinyoungfemaleswithanorexianervosaandatypicalanorexianervosaversushealthycontrols
AT melissajdreier neuralactivationofregionsinvolvedinfoodrewardandcognitivecontrolinyoungfemaleswithanorexianervosaandatypicalanorexianervosaversushealthycontrols
AT sedaebrahimi neuralactivationofregionsinvolvedinfoodrewardandcognitivecontrolinyoungfemaleswithanorexianervosaandatypicalanorexianervosaversushealthycontrols
AT thilodeckersbach neuralactivationofregionsinvolvedinfoodrewardandcognitivecontrolinyoungfemaleswithanorexianervosaandatypicalanorexianervosaversushealthycontrols
AT jenniferjthomas neuralactivationofregionsinvolvedinfoodrewardandcognitivecontrolinyoungfemaleswithanorexianervosaandatypicalanorexianervosaversushealthycontrols
AT lauramholsen neuralactivationofregionsinvolvedinfoodrewardandcognitivecontrolinyoungfemaleswithanorexianervosaandatypicalanorexianervosaversushealthycontrols
AT madhusmitamisra neuralactivationofregionsinvolvedinfoodrewardandcognitivecontrolinyoungfemaleswithanorexianervosaandatypicalanorexianervosaversushealthycontrols
AT elizabethalawson neuralactivationofregionsinvolvedinfoodrewardandcognitivecontrolinyoungfemaleswithanorexianervosaandatypicalanorexianervosaversushealthycontrols