Executive function in obesity and anorexia nervosa: Opposite ends of a spectrum of disordered feeding behaviour?
Higher-order executive functions such as decision-making, cognitive flexibility and behavioural control are critical to adaptive success in all aspects of life, including the maintenance of a healthy body weight by regulating food intake. Performance on tasks designed to assess these aspects of cogn...
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description | Higher-order executive functions such as decision-making, cognitive flexibility and behavioural control are critical to adaptive success in all aspects of life, including the maintenance of a healthy body weight by regulating food intake. Performance on tasks designed to assess these aspects of cognition is impaired in individuals with obesity and anorexia nervosa (AN); conditions at either end of a spectrum of body weight disturbance. While the conceptualisation of obesity and AN as mirror images of each other makes some sense from a metabolic point of view, whether or not these conditions also reflect opposing states of executive function is less clear. Here, we review evidence from neurocognitive and neuroimaging studies to compare the direction and extent of executive dysfunction in subjects with obesity and AN and how these are underpinned by changes in structure and function of subregions of the prefrontal cortex (PFC). Both conditions of extreme body weight disturbance are associated with impaired decision-making and cognitive inflexibility, however, impulsive behaviour presents in opposing directions; obesity being associated with reduced behavioural control and AN being associated with elevated control over behaviour with respect to food and feeding. Accordingly, the subregions of the PFC that guide inhibitory control and valuation of action outcomes (dorsolateral prefrontal cortex and orbitofrontal cortex) show opposite patterns of activation in subjects with obesity compared to those with AN, whereas the subregions implicated in cognitive and behavioural flexibility (ventromedial prefrontal cortex and anterior cingulate cortex) show alterations in the same direction in both conditions but with differential extent of dysfunction. We synthesise these findings in the context of the utility of animal models of obesity and AN to interrogate the detail of the neurobiological contributions to cognition in patient populations and the utility of such detail to inform future treatment strategies that specifically target executive dysfunction.
•In many respects and from a metabolic point of view, anorexia nervosa could be conceptualised as the “opposite” of obesity.•Both conditions show disrupted executive function but only deficits in behavioural control occur in opposing directions.•Impairments in cognition align with specific regional changes in prefrontal cortex function in both extremes of body weight.•Translationally relevant animal models provide cr |
doi_str_mv | 10.1016/j.pnpbp.2021.110395 |
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•In many respects and from a metabolic point of view, anorexia nervosa could be conceptualised as the “opposite” of obesity.•Both conditions show disrupted executive function but only deficits in behavioural control occur in opposing directions.•Impairments in cognition align with specific regional changes in prefrontal cortex function in both extremes of body weight.•Translationally relevant animal models provide crucial insights into how cognition contributes to disordered body weight.</description><identifier>ISSN: 0278-5846</identifier><identifier>EISSN: 1878-4216</identifier><identifier>DOI: 10.1016/j.pnpbp.2021.110395</identifier><identifier>PMID: 34217755</identifier><language>eng</language><publisher>England: Elsevier Inc</publisher><subject>Animals ; Anorexia nervosa ; Anorexia Nervosa - physiopathology ; Body Weight - physiology ; Cognition - physiology ; Cognitive flexibility ; Dorsolateral Prefrontal Cortex - physiopathology ; Executive Function - physiology ; Feeding Behavior - physiology ; Feeding behaviour ; Gyrus Cinguli - physiopathology ; Humans ; Impulse control ; Impulsive Behavior ; Neuroimaging ; Obesity ; Obesity - physiopathology ; Prefrontal Cortex - physiopathology ; Reward</subject><ispartof>Progress in neuro-psychopharmacology & biological psychiatry, 2021-12, Vol.111, p.110395-110395, Article 110395</ispartof><rights>2021 Elsevier Inc.</rights><rights>Copyright © 2021 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c359t-3bb7a987a791b5110832658c9555367817ee85523316f04838bb8407a83520303</citedby><cites>FETCH-LOGICAL-c359t-3bb7a987a791b5110832658c9555367817ee85523316f04838bb8407a83520303</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.pnpbp.2021.110395$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34217755$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Foldi, Claire J.</creatorcontrib><creatorcontrib>Morris, Margaret J.</creatorcontrib><creatorcontrib>Oldfield, Brian J.</creatorcontrib><title>Executive function in obesity and anorexia nervosa: Opposite ends of a spectrum of disordered feeding behaviour?</title><title>Progress in neuro-psychopharmacology & biological psychiatry</title><addtitle>Prog Neuropsychopharmacol Biol Psychiatry</addtitle><description>Higher-order executive functions such as decision-making, cognitive flexibility and behavioural control are critical to adaptive success in all aspects of life, including the maintenance of a healthy body weight by regulating food intake. Performance on tasks designed to assess these aspects of cognition is impaired in individuals with obesity and anorexia nervosa (AN); conditions at either end of a spectrum of body weight disturbance. While the conceptualisation of obesity and AN as mirror images of each other makes some sense from a metabolic point of view, whether or not these conditions also reflect opposing states of executive function is less clear. Here, we review evidence from neurocognitive and neuroimaging studies to compare the direction and extent of executive dysfunction in subjects with obesity and AN and how these are underpinned by changes in structure and function of subregions of the prefrontal cortex (PFC). Both conditions of extreme body weight disturbance are associated with impaired decision-making and cognitive inflexibility, however, impulsive behaviour presents in opposing directions; obesity being associated with reduced behavioural control and AN being associated with elevated control over behaviour with respect to food and feeding. Accordingly, the subregions of the PFC that guide inhibitory control and valuation of action outcomes (dorsolateral prefrontal cortex and orbitofrontal cortex) show opposite patterns of activation in subjects with obesity compared to those with AN, whereas the subregions implicated in cognitive and behavioural flexibility (ventromedial prefrontal cortex and anterior cingulate cortex) show alterations in the same direction in both conditions but with differential extent of dysfunction. We synthesise these findings in the context of the utility of animal models of obesity and AN to interrogate the detail of the neurobiological contributions to cognition in patient populations and the utility of such detail to inform future treatment strategies that specifically target executive dysfunction.
•In many respects and from a metabolic point of view, anorexia nervosa could be conceptualised as the “opposite” of obesity.•Both conditions show disrupted executive function but only deficits in behavioural control occur in opposing directions.•Impairments in cognition align with specific regional changes in prefrontal cortex function in both extremes of body weight.•Translationally relevant animal models provide crucial insights into how cognition contributes to disordered body weight.</description><subject>Animals</subject><subject>Anorexia nervosa</subject><subject>Anorexia Nervosa - physiopathology</subject><subject>Body Weight - physiology</subject><subject>Cognition - physiology</subject><subject>Cognitive flexibility</subject><subject>Dorsolateral Prefrontal Cortex - physiopathology</subject><subject>Executive Function - physiology</subject><subject>Feeding Behavior - physiology</subject><subject>Feeding behaviour</subject><subject>Gyrus Cinguli - physiopathology</subject><subject>Humans</subject><subject>Impulse control</subject><subject>Impulsive Behavior</subject><subject>Neuroimaging</subject><subject>Obesity</subject><subject>Obesity - physiopathology</subject><subject>Prefrontal Cortex - physiopathology</subject><subject>Reward</subject><issn>0278-5846</issn><issn>1878-4216</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kF1LHDEUhkNp0a36CwqSS292m0zmTDKCiIj9AMGbeh2SzJk2y24Sk5lF_32zXfWyF-EknOfk8D6EfOFsxRnvvq5XKSSbVg1r-IpzJnr4QBZcSbVsG959JAvW1Duotjsmn0tZM8a4YOKIHIsKSAmwIOnuGd08-R3ScQ5u8jFQH2i0WPz0Qk0Y6okZn72hAfMuFnNJH1KKtY0Uw1BoHKmhJaGb8rzdvwZfYh4w40BHxMGH39TiH7Pzcc7Xp-TTaDYFz17rCXn8dvfr9sfy_uH7z9ub-6UT0E9LYa00vZJG9txCTadE04FyPQCITiouERVAIwTvRtYqoaxVLZNGCWhYTXlCLg7_phyfZiyT3vricLMxAeNcdAOtgl5BBxUVB9TlWErGUafstya_aM70XrVe63-q9V61PqiuU-evC2a7xeF95s1tBa4OANaYO49ZF-cxuGokV1l6iP6_C_4CTWKP0w</recordid><startdate>20211220</startdate><enddate>20211220</enddate><creator>Foldi, Claire J.</creator><creator>Morris, Margaret J.</creator><creator>Oldfield, Brian J.</creator><general>Elsevier Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope></search><sort><creationdate>20211220</creationdate><title>Executive function in obesity and anorexia nervosa: Opposite ends of a spectrum of disordered feeding behaviour?</title><author>Foldi, Claire J. ; Morris, Margaret J. ; Oldfield, Brian J.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c359t-3bb7a987a791b5110832658c9555367817ee85523316f04838bb8407a83520303</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Animals</topic><topic>Anorexia nervosa</topic><topic>Anorexia Nervosa - physiopathology</topic><topic>Body Weight - physiology</topic><topic>Cognition - physiology</topic><topic>Cognitive flexibility</topic><topic>Dorsolateral Prefrontal Cortex - physiopathology</topic><topic>Executive Function - physiology</topic><topic>Feeding Behavior - physiology</topic><topic>Feeding behaviour</topic><topic>Gyrus Cinguli - physiopathology</topic><topic>Humans</topic><topic>Impulse control</topic><topic>Impulsive Behavior</topic><topic>Neuroimaging</topic><topic>Obesity</topic><topic>Obesity - physiopathology</topic><topic>Prefrontal Cortex - physiopathology</topic><topic>Reward</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Foldi, Claire J.</creatorcontrib><creatorcontrib>Morris, Margaret J.</creatorcontrib><creatorcontrib>Oldfield, Brian J.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Progress in neuro-psychopharmacology & biological psychiatry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Foldi, Claire J.</au><au>Morris, Margaret J.</au><au>Oldfield, Brian J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Executive function in obesity and anorexia nervosa: Opposite ends of a spectrum of disordered feeding behaviour?</atitle><jtitle>Progress in neuro-psychopharmacology & biological psychiatry</jtitle><addtitle>Prog Neuropsychopharmacol Biol Psychiatry</addtitle><date>2021-12-20</date><risdate>2021</risdate><volume>111</volume><spage>110395</spage><epage>110395</epage><pages>110395-110395</pages><artnum>110395</artnum><issn>0278-5846</issn><eissn>1878-4216</eissn><abstract>Higher-order executive functions such as decision-making, cognitive flexibility and behavioural control are critical to adaptive success in all aspects of life, including the maintenance of a healthy body weight by regulating food intake. Performance on tasks designed to assess these aspects of cognition is impaired in individuals with obesity and anorexia nervosa (AN); conditions at either end of a spectrum of body weight disturbance. While the conceptualisation of obesity and AN as mirror images of each other makes some sense from a metabolic point of view, whether or not these conditions also reflect opposing states of executive function is less clear. Here, we review evidence from neurocognitive and neuroimaging studies to compare the direction and extent of executive dysfunction in subjects with obesity and AN and how these are underpinned by changes in structure and function of subregions of the prefrontal cortex (PFC). Both conditions of extreme body weight disturbance are associated with impaired decision-making and cognitive inflexibility, however, impulsive behaviour presents in opposing directions; obesity being associated with reduced behavioural control and AN being associated with elevated control over behaviour with respect to food and feeding. Accordingly, the subregions of the PFC that guide inhibitory control and valuation of action outcomes (dorsolateral prefrontal cortex and orbitofrontal cortex) show opposite patterns of activation in subjects with obesity compared to those with AN, whereas the subregions implicated in cognitive and behavioural flexibility (ventromedial prefrontal cortex and anterior cingulate cortex) show alterations in the same direction in both conditions but with differential extent of dysfunction. We synthesise these findings in the context of the utility of animal models of obesity and AN to interrogate the detail of the neurobiological contributions to cognition in patient populations and the utility of such detail to inform future treatment strategies that specifically target executive dysfunction.
•In many respects and from a metabolic point of view, anorexia nervosa could be conceptualised as the “opposite” of obesity.•Both conditions show disrupted executive function but only deficits in behavioural control occur in opposing directions.•Impairments in cognition align with specific regional changes in prefrontal cortex function in both extremes of body weight.•Translationally relevant animal models provide crucial insights into how cognition contributes to disordered body weight.</abstract><cop>England</cop><pub>Elsevier Inc</pub><pmid>34217755</pmid><doi>10.1016/j.pnpbp.2021.110395</doi><tpages>1</tpages></addata></record> |
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subjects | Animals Anorexia nervosa Anorexia Nervosa - physiopathology Body Weight - physiology Cognition - physiology Cognitive flexibility Dorsolateral Prefrontal Cortex - physiopathology Executive Function - physiology Feeding Behavior - physiology Feeding behaviour Gyrus Cinguli - physiopathology Humans Impulse control Impulsive Behavior Neuroimaging Obesity Obesity - physiopathology Prefrontal Cortex - physiopathology Reward |
title | Executive function in obesity and anorexia nervosa: Opposite ends of a spectrum of disordered feeding behaviour? |
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