Exposure to gestational diabetes mellitus in utero impacts hippocampal functional connectivity in response to food cues in children.

Journal

International journal of obesity (2005)
ISSN: 1476-5497
Titre abrégé: Int J Obes (Lond)
Pays: England
ID NLM: 101256108

Informations de publication

Date de publication:
28 Aug 2024
Historique:
received: 13 02 2024
accepted: 08 08 2024
revised: 30 07 2024
medline: 31 8 2024
pubmed: 31 8 2024
entrez: 28 8 2024
Statut: aheadofprint

Résumé

Intrauterine exposure to gestational diabetes mellitus (GDM) increases the risk of obesity in the offspring, but little is known about the underlying neural mechanisms. The hippocampus is crucial for food intake regulation and is vulnerable to the effects of obesity. The purpose of the study was to investigate whether GDM exposure affects hippocampal functional connectivity during exposure to food cues using functional magnetic resonance imaging (fMRI). Participants were 90 children age 7-11 years (53 females) who underwent an fMRI-based visual food cue task in the fasted state. Hippocampal functional connectivity (FC) was examined using generalized psychophysiological interaction in response to food versus non-food cues. Hippocampal FC was compared between children with and without GDM exposure, while controlling for possible confounding effects of age, sex and waist-to-hip ratio. In addition, the influence of childhood and maternal obesity were investigated using multiple regression models. While viewing high caloric food cues compared to non-food cure, children with GDM exposure exhibited higher hippocampal FC to the insula and striatum (i.e., putamen, pallidum and nucleus accumbens) compared to unexposed children. With increasing BMI, children with GDM exposure had lower hippocampal FC to the somatosensory cortex (i.e., postcentral gyrus). Intrauterine exposure to GDM was associated with higher food-cue induced hippocampal FC especially to reward processing regions. Future studies with longitudinal measurements are needed to clarify whether altered hippocampal FC may raise the risk of the development of metabolic diseases later in life.

Identifiants

DOI: 10.1038/s41366-024-01608-1 PMID: 39198584
pubmed: 39198584
doi: 10.1038/s41366-024-01608-1
pii: 10.1038/s41366-024-01608-1
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s).

Références

American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes care. 2013;36:S67–74.
Damm P, Houshmand-Oeregaard A, Kelstrup L, Lauenborg J, Mathiesen ER, Clausen TD. Gestational diabetes mellitus and long-term consequences for mother and offspring: a view from Denmark. Diabetologia. 2016;59:1396–9.
pubmed: 27174368 doi: 10.1007/s00125-016-3985-5
Money KM, Barke TL, Serezani A, Gannon M, Garbett KA, Aronoff DM, et al. Gestational diabetes exacerbates maternal immune activation effects in the developing brain. Mol Psychiatry. 2018;23:1920–8.
pubmed: 28948973 doi: 10.1038/mp.2017.191
Vuong B, Odero G, Rozbacher S, Stevenson M, Kereliuk SM, Pereira TJ, et al. Exposure to gestational diabetes mellitus induces neuroinflammation, derangement of hippocampal neurons, and cognitive changes in rat offspring. J Neuroinflammation. 2017;14:80.
pubmed: 28388927 pmcid: 5384149 doi: 10.1186/s12974-017-0859-9
Devoto F, Zapparoli L, Bonandrini R, Berlingeri M, Ferrulli A, Luzi L, et al. Hungry brains: a meta-analytical review of brain activation imaging studies on food perception and appetite in obese individuals. Neurosci Biobehav Rev. 2018;94:271–85.
pubmed: 30071209 doi: 10.1016/j.neubiorev.2018.07.017
Stice E, Figlewicz DP, Gosnell BA, Levine AS, Pratt WE. The contribution of brain reward circuits to the obesity epidemic. Neurosci Biobehav Rev. 2013;37:2047–58.
pubmed: 23237885 doi: 10.1016/j.neubiorev.2012.12.001
Boswell RG, Kober H. Food cue reactivity and craving predict eating and weight gain: a meta-analytic review. Obes Rev Off J Int Assoc Study Obes. 2016;17:159–77.
doi: 10.1111/obr.12354
Stice E, Yokum S, Burger KS, Epstein LH, Small DM. Youth at risk for obesity show greater activation of striatal and somatosensory regions to food. J Neurosci Off J Soc Neurosci. 2011;31:4360–6.
doi: 10.1523/JNEUROSCI.6604-10.2011
Luo S, Angelo BC, Chow T, Monterosso JR, Thompson PM, Xiang AH, et al. Associations between exposure to gestational diabetes mellitus in utero and daily energy intake, brain responses to food cues, and adiposity in children. Diabetes Care. 2021;44:1185–93.
pubmed: 33827804 doi: 10.2337/dc20-3006
Page KA, Luo S, Wang X, Chow T, Alves J, Buchanan TA, et al. Children exposed to maternal obesity or gestational diabetes mellitus during early fetal development have hypothalamic alterations that predict future weight gain. Diabetes Care. 2019;42:1473–80.
pubmed: 31332028 pmcid: 6647040 doi: 10.2337/dc18-2581
Chandrasekaran S, Melhorn S, Olerich KLW, Angelo B, Chow T, Xiang A, et al. Exposure to gestational diabetes mellitus prior to 26 weeks is related to the presence of mediobasal hypothalamic gliosis in children. Diabetes. 2022;71:2552–6.
pubmed: 36095276 pmcid: 9750940 doi: 10.2337/db22-0448
Lotfi N, Hami J, Hosseini M, Haghir D, Haghir H. Diabetes during pregnancy enhanced neuronal death in the hippocampus of rat offspring. Int J Develop Neurosci Off J Int Soc Develop Neurosci. 2016;51:28–35.
doi: 10.1016/j.ijdevneu.2016.04.009
Golalipour MJ, Kafshgiri SK, Ghafari S. Gestational diabetes induced neuronal loss in CA1 and CA3 subfields of rat hippocampus in early postnatal life. Folia Morphologica. 2012;71:71–7.
pubmed: 22648583
Lynch KM, Alves JM, Chow T, Clark KA, Luo S, Toga AW, et al. Selective morphological and volumetric alterations in the hippocampus of children exposed in utero to gestational diabetes mellitus. Hum Brain Mapp. 2021;42:2583–92.
pubmed: 33764653 pmcid: 8090774 doi: 10.1002/hbm.25390
Alves JM, Luo S, Chow T, Herting M, Xiang AH, Page KA. Sex differences in the association between prenatal exposure to maternal obesity and hippocampal volume in children. Brain Behav. 2020;10:e01522.
pubmed: 31903710 pmcid: 7010582 doi: 10.1002/brb3.1522
Kanoski SE, Grill HJ. Hippocampus contributions to food intake control: mnemonic, neuroanatomical, and endocrine mechanisms. Biol Psychiatry. 2017;81:748–56.
pubmed: 26555354 doi: 10.1016/j.biopsych.2015.09.011
Stevenson RJ, Francis HM, Attuquayefio T, Gupta D, Yeomans MR, Oaten MJ, et al. Hippocampal-dependent appetitive control is impaired by experimental exposure to a Western-style diet. R Soc Open Sci. 2020;7:191338.
pubmed: 32257311 pmcid: 7062097 doi: 10.1098/rsos.191338
Winocur G, Greenwood CE. Studies of the effects of high fat diets on cognitive function in a rat model. Neurobiol Aging. 2005;26:46–9.
pubmed: 16219391 doi: 10.1016/j.neurobiolaging.2005.09.003
Higgs S, Williamson AC, Attwood AS. Recall of recent lunch and its effect on subsequent snack intake. Physiol Behav. 2008;94:454–62.
pubmed: 18420236 doi: 10.1016/j.physbeh.2008.02.011
Higgs S, Woodward M. Television watching during lunch increases afternoon snack intake of young women. Appetite. 2009;52:39–43.
pubmed: 18692103 doi: 10.1016/j.appet.2008.07.007
Hebben N, Corkin S, Eichenbaum H, Shedlack K. Diminished ability to interpret and report internal states after bilateral medial temporal resection: case H.M. Behav Neurosci. 1985;99:1031–9.
pubmed: 3843537 doi: 10.1037/0735-7044.99.6.1031
Kullmann S, Kleinridders A, Small DM, Fritsche A, Häring HU, Preissl H, et al. Central nervous pathways of insulin action in the control of metabolism and food intake. Lancet Diabetes Endocrinol. 2020;8:524–34.
pubmed: 32445739 doi: 10.1016/S2213-8587(20)30113-3
Jones S, Luo S, Dorton HM, Angelo B, Yunker AG, Monterosso JR, et al. Evidence of a role for the hippocampus in food-cue processing and the association with body weight and dietary added sugar. Obes. 2021;29:370–8.
doi: 10.1002/oby.23085
Parent MB, Higgs S, Cheke LG, Kanoski SE. Memory and eating: a bidirectional relationship implicated in obesity. Neurosci Biobehav Rev. 2022;132:110–29.
pubmed: 34813827 doi: 10.1016/j.neubiorev.2021.10.051
Luo S, Alves J, Hardy K, Wang X, Monterosso J, Xiang AH, et al. Neural processing of food cues in pre-pubertal children. Pediatr Obes. 2019;14:e12435.
pubmed: 30019454 doi: 10.1111/ijpo.12435
Pujol J, Blanco-Hinojo L, Martínez-Vilavella G, Deus J, Pérez-Sola V, Sunyer J. Dysfunctional brain reward system in child obesity. Cereb Cortex. 2021;31:4376–85.
pubmed: 33861860 doi: 10.1093/cercor/bhab092
Borowitz MA, Yokum S, Duval ER, Gearhardt AN. Weight-related differences in salience, default mode, and executive function network connectivity in adolescents. Obes. 2020;28:1438–46.
doi: 10.1002/oby.22853
Zhang P, Wu GW, Yu FX, Liu Y, Li MY, Wang Z, et al. Abnormal regional neural activity and reorganized neural network in obesity: evidence from resting-state fMRI. Obes. 2020;28:1283–91.
doi: 10.1002/oby.22839
Zhao J, Manza P, Gu J, Song H, Zhuang P, Shi F, et al. Contrasting dorsal caudate functional connectivity patterns between frontal and temporal cortex with BMI increase: link to cognitive flexibility. Int J Obes. 2021;45:2608–16.
doi: 10.1038/s41366-021-00929-9
Parsons N, Steward T, Clohesy R, Almgren H, Duehlmeyer L. A systematic review of resting-state functional connectivity in obesity: refining current neurobiological frameworks and methodological considerations moving forward. Rev Endocr Metab Disord. 2022;23:861–79.
pubmed: 34159504 doi: 10.1007/s11154-021-09665-x
Donofry SD, Jakicic JM, Rogers RJ, Watt JC, Roecklein KA, Erickson KI. Comparison of food cue-evoked and resting-state functional connectivity in obesity. Psychosom Med. 2020;82:261–71.
pubmed: 32267660 pmcid: 8057093 doi: 10.1097/PSY.0000000000000769
Devoto F, Ferrulli A, Banfi G, Luzi L, Zapparoli L, Paulesu E. How images of food become cravingly salient in obesity. Obes. 2023;31:2294–303.
doi: 10.1002/oby.23834
American Diabetes Association. Gestational diabetes mellitus. Diabetes care. 2004;27:S88–90.
Kuczmarski RJ, Ogden CL, Guo SS, Grummer-Strawn LM, Flegal KM, Mei Z, et al. CDC Growth Charts for the United States: methods and development. Vital and health statistics Series 11. Data Natl Health Surv. 2000;2002:1–190.
Bohon C. Brain response to taste in overweight children: a pilot feasibility study. PloS One. 2017;12:e0172604.
pubmed: 28235080 pmcid: 5325294 doi: 10.1371/journal.pone.0172604
Boutelle KN, Wierenga CE, Bischoff-Grethe A, Melrose AJ, Grenesko-Stevens E, Paulus MP, et al. Increased brain response to appetitive tastes in the insula and amygdala in obese compared with healthy weight children when sated. Int J Obes. 2015;39:620–8.
doi: 10.1038/ijo.2014.206
Kasper L, Bollmann S, Diaconescu AO, Hutton C, Heinzle J, Iglesias S, et al. The PhysIO toolbox for modeling physiological noise in fMRI data. J Neurosci Methods. 2017;276:56–72.
pubmed: 27832957 doi: 10.1016/j.jneumeth.2016.10.019
Blankenship SL, Redcay E, Dougherty LR, Riggins T. Development of hippocampal functional connectivity during childhood. Hum Brain Mapp. 2017;38:182–201.
pubmed: 27585371 doi: 10.1002/hbm.23353
Wallner-Liebmann S, Koschutnig K, Reishofer G, Sorantin E, Blaschitz B, Kruschitz R, et al. Insulin and hippocampus activation in response to images of high-calorie food in normal weight and obese adolescents. Obes. 2010;18:1552–7.
doi: 10.1038/oby.2010.26
Jastreboff AM, Lacadie C, Seo D, Kubat J, Van Name MA, Giannini C, et al. Leptin is associated with exaggerated brain reward and emotion responses to food images in adolescent obesity. Diabetes Care. 2014;37:3061–8.
pubmed: 25139883 pmcid: 4207200 doi: 10.2337/dc14-0525
Roth CL, Melhorn SJ, Elfers CT, Scholz K, De Leon MRB, Rowland M, et al. Central nervous system and peripheral hormone responses to a meal in children. J Clin Endocrinol Metab. 2019;104:1471–83.
pubmed: 30418574 doi: 10.1210/jc.2018-01525
Volkow ND, Wang GJ, Baler RD. Reward, dopamine and the control of food intake: implications for obesity. Trends Cogn Sci. 2011;15:37–46.
pubmed: 21109477 doi: 10.1016/j.tics.2010.11.001
van Meer F, van der Laan LN, Charbonnier L, Viergever MA, Adan RA, Smeets PA. Developmental differences in the brain response to unhealthy food cues: an fMRI study of children and adults. Am J Clin Nutr. 2016;104:1515–22.
pubmed: 27806979 doi: 10.3945/ajcn.116.137240
Tomasi D, Volkow ND. Striatocortical pathway dysfunction in addiction and obesity: differences and similarities. Crit Rev Biochem Mol Biol. 2013;48:1–19.
pubmed: 23173916 doi: 10.3109/10409238.2012.735642
Carnell S, Thapaliya G, Jansen E, Chen L. Biobehavioral susceptibility for obesity in childhood: behavioral, genetic and neuroimaging studies of appetite. Physiol Behav. 2023;271:114313.
pubmed: 37544571 doi: 10.1016/j.physbeh.2023.114313
Shapiro ALB, Johnson SL, Sutton B, Legget KT, Dabelea D, Tregellas JR. Eating in the absence of hunger in young children is related to brain reward network hyperactivity and reduced functional connectivity in executive control networks. Pediatr Obes. 2019;14:e12502.
pubmed: 30659756 pmcid: 6684353 doi: 10.1111/ijpo.12502
Assari S, Boyce S. Resting-state functional connectivity between putamen and salience network and childhood body mass index. Neurol Int. 2021;13:85–101.
pubmed: 33806587 pmcid: 8006001 doi: 10.3390/neurolint13010009
Contreras-Rodríguez O, Martín-Pérez C, Vilar-López R, Verdejo-Garcia A. Ventral and dorsal striatum networks in obesity: link to food craving and weight gain. Biol Psychiatry. 2017;81:789–96.
pubmed: 26809248 doi: 10.1016/j.biopsych.2015.11.020
Nakamura Y, Koike S. Association of disinhibited eating and trait of impulsivity with insula and amygdala responses to palatable liquid consumption. Front Syst Neurosci. 2021;15:647143.
pubmed: 34012386 pmcid: 8128107 doi: 10.3389/fnsys.2021.647143
Hong Chen WL, Ximei Chen, Qingge Pang, Xiao Gao, Cheng Guo, et al. Altered hippocampal effective connectivity predicts BMI and food approach behavior in children with obesity. 03 May 2024, PREPRINT (Version 1) available at Research Square [ https://doi.org/10.21203/rs.3.rs-4301324/v1 ].
De Araujo IE, Rolls ET. Representation in the human brain of food texture and oral fat. J Neurosci Off J Soc Neurosci. 2004;24:3086–93.
doi: 10.1523/JNEUROSCI.0130-04.2004
Rapuano KM, Huckins JF, Sargent JD, Heatherton TF, Kelley WM. Individual differences in reward and somatosensory-motor brain regions correlate with adiposity in adolescents. Cereb Cortex. 2016;26:2602–11.
pubmed: 25994961 doi: 10.1093/cercor/bhv097
Salbe AD, DelParigi A, Pratley RE, Drewnowski A, Tataranni PA. Taste preferences and body weight changes in an obesity-prone population. Am J Clin Nutr. 2004;79:372–8.
pubmed: 14985209 doi: 10.1093/ajcn/79.3.372
Stice E, Yokum S. Neural vulnerability factors that predict future weight gain. Curr Obes Rep. 2021;10:435–43.
pubmed: 34591256 doi: 10.1007/s13679-021-00455-9
Carnell S, Benson L, Chang KV, Wang Z, Huo Y, Geliebter A, et al. Neural correlates of familial obesity risk and overweight in adolescence. NeuroImage. 2017;159:236–47.
pubmed: 28754348 doi: 10.1016/j.neuroimage.2017.07.052
Moreno-Lopez L, Contreras-Rodriguez O, Soriano-Mas C, Stamatakis EA, Verdejo-Garcia A. Disrupted functional connectivity in adolescent obesity. NeuroImage Clin. 2016;12:262–8.
pubmed: 27504261 pmcid: 4969269 doi: 10.1016/j.nicl.2016.07.005

Auteurs

Sixiu Zhao (S)

Institute for Diabetes Research and Metabolic Diseases of the Helmholtz Center Munich at the University of Tübingen, Tübingen, Germany.
German Center for Diabetes Research (DZD), Tübingen, Germany.

Lorenzo Semeia (L)

Institute for Diabetes Research and Metabolic Diseases of the Helmholtz Center Munich at the University of Tübingen, Tübingen, Germany.
German Center for Diabetes Research (DZD), Tübingen, Germany.
ORCID: 0000-0002-2079-7147

Ralf Veit (R)

Institute for Diabetes Research and Metabolic Diseases of the Helmholtz Center Munich at the University of Tübingen, Tübingen, Germany.
German Center for Diabetes Research (DZD), Tübingen, Germany.
ORCID: 0000-0001-9860-642X

Shan Luo (S)

Division of Endocrinology, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
Diabetes and Obesity Research Institute, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
Department of Psychology, University of Southern California, Los Angeles, CA, USA.
Imaging Genetics Center, Mark and Mary Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.

Brendan C Angelo (BC)

Division of Endocrinology, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
Diabetes and Obesity Research Institute, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
ORCID: 0000-0003-3558-2840

Ting Chow (T)

Department of Research and Evaluation, Kaiser Permanente Southern California, Pasadena, CA, USA.

Andreas L Birkenfeld (AL)

Institute for Diabetes Research and Metabolic Diseases of the Helmholtz Center Munich at the University of Tübingen, Tübingen, Germany.
German Center for Diabetes Research (DZD), Tübingen, Germany.
Department of Internal Medicine, Division of Diabetology, Endocrinology and Nephrology, Eberhard Karls University Tübingen, Tübingen, Germany.
ORCID: 0000-0003-1407-9023

Hubert Preissl (H)

Institute for Diabetes Research and Metabolic Diseases of the Helmholtz Center Munich at the University of Tübingen, Tübingen, Germany.
German Center for Diabetes Research (DZD), Tübingen, Germany.
Department of Internal Medicine, Division of Diabetology, Endocrinology and Nephrology, Eberhard Karls University Tübingen, Tübingen, Germany.
Department of Pharmacy and Biochemistry, Eberhard Karls University Tübingen, Tübingen, Germany.
ORCID: 0000-0002-8859-4661

Anny H Xiang (AH)

Department of Research and Evaluation, Kaiser Permanente Southern California, Pasadena, CA, USA.

Kathleen A Page (KA)

Division of Endocrinology, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
Diabetes and Obesity Research Institute, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
Neuroscience Graduate Program, University of Southern California, Los Angeles, CA, USA.

Stephanie Kullmann (S)

Institute for Diabetes Research and Metabolic Diseases of the Helmholtz Center Munich at the University of Tübingen, Tübingen, Germany. Stephanie.Kullmann@med.uni-tuebingen.de.
German Center for Diabetes Research (DZD), Tübingen, Germany. Stephanie.Kullmann@med.uni-tuebingen.de.
Department of Internal Medicine, Division of Diabetology, Endocrinology and Nephrology, Eberhard Karls University Tübingen, Tübingen, Germany. Stephanie.Kullmann@med.uni-tuebingen.de.
ORCID: 0000-0001-9951-923X

Classifications MeSH