The influence of insulin on anticipation and consummatory reward to food intake: A functional imaging study on healthy normal weight and overweight subjects employing intranasal insulin delivery
Aberrant responses within homeostatic, hedonic and cognitive systems contribute to poor appetite control in those with an overweight phenotype. The hedonic system incorporates limbic and meso‐limbic regions involved in learning and reward processing, as well as cortical regions involved in motivatio...
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Published in | Human brain mapping Vol. 43; no. 18; pp. 5432 - 5451 |
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Main Authors | , , , , , , , |
Format | Journal Article |
Language | English |
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Hoboken, USA
John Wiley & Sons, Inc
15.12.2022
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Abstract | Aberrant responses within homeostatic, hedonic and cognitive systems contribute to poor appetite control in those with an overweight phenotype. The hedonic system incorporates limbic and meso‐limbic regions involved in learning and reward processing, as well as cortical regions involved in motivation, decision making and gustatory processing. Equally important within this complex, multifaceted framework are the cognitive systems involved in inhibitory control and valuation of food choices. Regions within these systems display insulin receptors and pharmacologically increasing central insulin concentrations using intranasal administration (IN‐INS) has been shown to significantly reduce appealing food cue responsiveness and also food intake. In this work we describe a placebo‐controlled crossover pharmacological functional magnetic resonance imaging (fMRI) study that looks at how IN‐INS (160 IU) affects anticipatory and consummatory responses to sweet stimuli and importantly how these responses differ between healthy normal weight and overweight male individuals. This work shows that age matched normal weight and overweight (not obese) individuals respond similarly to both the anticipation and receipt of sweet stimuli under placebo conditions. However, increased central insulin concentrations produce marked differences between groups when anticipating sweet stimuli within the prefrontal cortex and midbrain as well as observed differences in the amygdala during consummatory responses.
This study probes anticipatory and consummatory responses to sweet solution using a fMRI paradigm which delivers liquid stimuli. This work shows that when brain insulin concentration is increased, using intranasal insulin administration, differences in these responses can be identified between lean and overweight individuals. |
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AbstractList | Aberrant responses within homeostatic, hedonic and cognitive systems contribute to poor appetite control in those with an overweight phenotype. The hedonic system incorporates limbic and meso-limbic regions involved in learning and reward processing, as well as cortical regions involved in motivation, decision making and gustatory processing. Equally important within this complex, multifaceted framework are the cognitive systems involved in inhibitory control and valuation of food choices. Regions within these systems display insulin receptors and pharmacologically increasing central insulin concentrations using intranasal administration (IN-INS) has been shown to significantly reduce appealing food cue responsiveness and also food intake. In this work we describe a placebo-controlled crossover pharmacological functional magnetic resonance imaging (fMRI) study that looks at how IN-INS (160 IU) affects anticipatory and consummatory responses to sweet stimuli and importantly how these responses differ between healthy normal weight and overweight male individuals. This work shows that age matched normal weight and overweight (not obese) individuals respond similarly to both the anticipation and receipt of sweet stimuli under placebo conditions. However, increased central insulin concentrations produce marked differences between groups when anticipating sweet stimuli within the prefrontal cortex and midbrain as well as observed differences in the amygdala during consummatory responses. Aberrant responses within homeostatic, hedonic and cognitive systems contribute to poor appetite control in those with an overweight phenotype. The hedonic system incorporates limbic and meso‐limbic regions involved in learning and reward processing, as well as cortical regions involved in motivation, decision making and gustatory processing. Equally important within this complex, multifaceted framework are the cognitive systems involved in inhibitory control and valuation of food choices. Regions within these systems display insulin receptors and pharmacologically increasing central insulin concentrations using intranasal administration (IN‐INS) has been shown to significantly reduce appealing food cue responsiveness and also food intake. In this work we describe a placebo‐controlled crossover pharmacological functional magnetic resonance imaging (fMRI) study that looks at how IN‐INS (160 IU) affects anticipatory and consummatory responses to sweet stimuli and importantly how these responses differ between healthy normal weight and overweight male individuals. This work shows that age matched normal weight and overweight (not obese) individuals respond similarly to both the anticipation and receipt of sweet stimuli under placebo conditions. However, increased central insulin concentrations produce marked differences between groups when anticipating sweet stimuli within the prefrontal cortex and midbrain as well as observed differences in the amygdala during consummatory responses. This study probes anticipatory and consummatory responses to sweet solution using a fMRI paradigm which delivers liquid stimuli. This work shows that when brain insulin concentration is increased, using intranasal insulin administration, differences in these responses can be identified between lean and overweight individuals. Aberrant responses within homeostatic, hedonic and cognitive systems contribute to poor appetite control in those with an overweight phenotype. The hedonic system incorporates limbic and meso-limbic regions involved in learning and reward processing, as well as cortical regions involved in motivation, decision making and gustatory processing. Equally important within this complex, multifaceted framework are the cognitive systems involved in inhibitory control and valuation of food choices. Regions within these systems display insulin receptors and pharmacologically increasing central insulin concentrations using intranasal administration (IN-INS) has been shown to significantly reduce appealing food cue responsiveness and also food intake. In this work we describe a placebo-controlled crossover pharmacological functional magnetic resonance imaging (fMRI) study that looks at how IN-INS (160 IU) affects anticipatory and consummatory responses to sweet stimuli and importantly how these responses differ between healthy normal weight and overweight male individuals. This work shows that age matched normal weight and overweight (not obese) individuals respond similarly to both the anticipation and receipt of sweet stimuli under placebo conditions. However, increased central insulin concentrations produce marked differences between groups when anticipating sweet stimuli within the prefrontal cortex and midbrain as well as observed differences in the amygdala during consummatory responses.Aberrant responses within homeostatic, hedonic and cognitive systems contribute to poor appetite control in those with an overweight phenotype. The hedonic system incorporates limbic and meso-limbic regions involved in learning and reward processing, as well as cortical regions involved in motivation, decision making and gustatory processing. Equally important within this complex, multifaceted framework are the cognitive systems involved in inhibitory control and valuation of food choices. Regions within these systems display insulin receptors and pharmacologically increasing central insulin concentrations using intranasal administration (IN-INS) has been shown to significantly reduce appealing food cue responsiveness and also food intake. In this work we describe a placebo-controlled crossover pharmacological functional magnetic resonance imaging (fMRI) study that looks at how IN-INS (160 IU) affects anticipatory and consummatory responses to sweet stimuli and importantly how these responses differ between healthy normal weight and overweight male individuals. This work shows that age matched normal weight and overweight (not obese) individuals respond similarly to both the anticipation and receipt of sweet stimuli under placebo conditions. However, increased central insulin concentrations produce marked differences between groups when anticipating sweet stimuli within the prefrontal cortex and midbrain as well as observed differences in the amygdala during consummatory responses. |
Author | De Lara Rubio, Alfonso Zelaya, Fernando Wingrove, Jed Forbes, Ben Swedroska, Magda Amiel, Stephanie Hill, Simon O'Daly, Owen |
AuthorAffiliation | 2 Centre for Obesity Research, Department of Medicine University College London London UK 1 Department of Neuroimaging, Institute of Psychiatry Psychology and Neuroscience King's College London London UK 4 Diabetes Research Group, Weston Education Centre King's College London London UK 3 Institute of Pharmaceutical Sciences, Pharmaceutical Sciences King's College London London UK |
AuthorAffiliation_xml | – name: 3 Institute of Pharmaceutical Sciences, Pharmaceutical Sciences King's College London London UK – name: 4 Diabetes Research Group, Weston Education Centre King's College London London UK – name: 2 Centre for Obesity Research, Department of Medicine University College London London UK – name: 1 Department of Neuroimaging, Institute of Psychiatry Psychology and Neuroscience King's College London London UK |
Author_xml | – sequence: 1 givenname: Jed orcidid: 0000-0002-0454-1299 surname: Wingrove fullname: Wingrove, Jed email: jed.wingrove@kcl.ac.uk organization: University College London – sequence: 2 givenname: Owen surname: O'Daly fullname: O'Daly, Owen organization: Psychology and Neuroscience King's College London – sequence: 3 givenname: Alfonso surname: De Lara Rubio fullname: De Lara Rubio, Alfonso organization: Psychology and Neuroscience King's College London – sequence: 4 givenname: Simon surname: Hill fullname: Hill, Simon organization: Psychology and Neuroscience King's College London – sequence: 5 givenname: Magda surname: Swedroska fullname: Swedroska, Magda organization: King's College London – sequence: 6 givenname: Ben surname: Forbes fullname: Forbes, Ben organization: King's College London – sequence: 7 givenname: Stephanie surname: Amiel fullname: Amiel, Stephanie organization: King's College London – sequence: 8 givenname: Fernando surname: Zelaya fullname: Zelaya, Fernando organization: Psychology and Neuroscience King's College London |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/35860945$$D View this record in MEDLINE/PubMed |
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CitedBy_id | crossref_primary_10_1016_j_yfrne_2025_101187 crossref_primary_10_1016_j_bionps_2025_100125 crossref_primary_10_1016_j_physbeh_2024_114622 crossref_primary_10_1016_j_neubiorev_2024_105907 |
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Keywords | consummatory functional imaging intranasal insulin overweight anticipation |
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Notes | Funding information Engineering and Physical Sciences Research Council, Grant/Award Number: EP/L015226/1; Unilever 2019 The content of this article has been published [IN PART] as part of the thesis of Jed Wingrove . ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 ObjectType-Article-2 ObjectType-Feature-1 content type line 23 The content of this article has been published [IN PART] as part of the thesis of Jed Wingrove (2019). Funding information Engineering and Physical Sciences Research Council, Grant/Award Number: EP/L015226/1; Unilever |
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Snippet | Aberrant responses within homeostatic, hedonic and cognitive systems contribute to poor appetite control in those with an overweight phenotype. The hedonic... |
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SubjectTerms | Administration, Intranasal Amygdala anticipation Anticipation, Psychological - physiology Appetite Appetite loss Body mass index Body weight Brain research Cognitive ability consummatory Control systems Cross-Over Studies Decision making Diabetes Eating Food Food intake functional imaging Functional magnetic resonance imaging Glucose Hedonic response Humans Information processing Insulin Insulin receptors Insulin resistance Intranasal administration intranasal insulin Magnetic resonance imaging Magnetic Resonance Imaging - methods Male Males Mesencephalon Metabolism Motivation Neuroimaging Obesity Overweight Overweight - diagnostic imaging Overweight - drug therapy Pharmacology Phenotypes Placebos Prefrontal cortex Reinforcement Reward Stimuli Sucrose Weight control |
Title | The influence of insulin on anticipation and consummatory reward to food intake: A functional imaging study on healthy normal weight and overweight subjects employing intranasal insulin delivery |
URI | https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fhbm.26019 https://www.ncbi.nlm.nih.gov/pubmed/35860945 https://www.proquest.com/docview/2740535842 https://www.proquest.com/docview/2692755702 https://pubmed.ncbi.nlm.nih.gov/PMC9704782 |
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