Sucrose consumption alters steroid and dopamine signalling in the female rat brain

in Journal of Endocrinology
Authors:
Daniel J Tobiansky Department of Psychology, The University of British Columbia
Djavad Mowafaghian Centre for Brain Health, The University of British Columbia, Vancouver, British Columbia, Canada

Search for other papers by Daniel J Tobiansky in
Current site
Google Scholar
PubMed
Close
https://orcid.org/0000-0001-6381-3453
,
George V Kachkovski Department of Psychology, The University of British Columbia

Search for other papers by George V Kachkovski in
Current site
Google Scholar
PubMed
Close
https://orcid.org/0000-0003-3593-7912
,
Reilly T Enos Department of Pathology, Microbiology, and Immunology, School of Medicine, University of South Carolina, Columbia, South Carolina, USA

Search for other papers by Reilly T Enos in
Current site
Google Scholar
PubMed
Close
,
Kim L Schmidt Department of Psychology, The University of British Columbia

Search for other papers by Kim L Schmidt in
Current site
Google Scholar
PubMed
Close
,
E Angela Murphy Department of Pathology, Microbiology, and Immunology, School of Medicine, University of South Carolina, Columbia, South Carolina, USA

Search for other papers by E Angela Murphy in
Current site
Google Scholar
PubMed
Close
, and
Kiran K Soma Department of Psychology, The University of British Columbia
Djavad Mowafaghian Centre for Brain Health, The University of British Columbia, Vancouver, British Columbia, Canada
Department of Zoology, The University of British Columbia, Vancouver, British Columbia, Canada

Search for other papers by Kiran K Soma in
Current site
Google Scholar
PubMed
Close

Correspondence should be addressed to K K Soma: ksoma@psych.ubc.ca

(D J Tobiansky is now at Department of Ecology and Evolutionary Biology, Brown University, Providence, Rhode Island, USA)

Restricted access
Rent on DeepDyve

Sign up for journal news

Sucrose consumption is associated with type 2 diabetes, cardiovascular disease, and cognitive deficits. Sucrose intake during pregnancy might have particularly prominent effects on metabolic, endocrine, and neural physiology. It remains unclear how consumption of sucrose affects parous females, especially in brain circuits that mediate food consumption and reward processing. Here, we examine whether a human-relevant level of sucrose before, during, and after pregnancy (17–18 weeks total) influences metabolic and neuroendocrine physiology in female rats. Females were fed either a control diet or a macronutrient-matched, isocaloric sucrose diet (25% of kcal from sucrose). Metabolically, sucrose impairs glucose tolerance, increases liver lipids, and increases a marker of adipose inflammation, but has no effect on body weight or overall visceral adiposity. Sucrose also decreases corticosterone levels in serum but not in the brain. Sucrose increases progesterone levels in serum and in the brain and increases the brain:serum ratio of progesterone in the mesocorticolimbic system and hypothalamus. These data suggest a dysregulation of systemic and local steroid signalling. Moreover, sucrose decreases tyrosine hydroxylase (TH), a catecholamine-synthetic enzyme, in the medial prefrontal cortex. Finally, sucrose consumption alters the expression pattern of FOSB, a marker of phasic dopamine signalling, in the nucleus accumbens. Overall, chronic consumption of sucrose at a human-relevant level alters metabolism, steroid levels, and brain dopamine signalling in a female rat model.

Supplementary Materials

    • Supplementary Table 1
    • Supplementary Table 2
    • Supplementary Table 3
    • SupplementalFigure1.Bilateralmicrodissectedpunchlocationstakenfromfreshfrozentissuesectionsslicedat300μm.Puncheswererandomlyextractedfromtherightorlefthemisphere,hencethebilateraldistributionofpunchholes.AllpuncheswereusedforsteroidanalysisviaLC-MS/MS.PunchplacementwasverifiedattheendofthestudybyaNisslcounterstain.Rostraltocaudal.

 

  • Collapse
  • Expand
  • Ahmed S, Kashem MA, Sarker R, Ahmed EU, Hargreaves GA & McGregor IS 2014 Neuroadaptations in the striatal proteome of the rat following prolonged excessive sucrose intake. Neurochemical Research 39 815824. (https://doi.org/10.1007/s11064-014-1274-6)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Arbogast LA & Voogt JL 1994 Progesterone suppresses tyrosine hydroxylase messenger ribonucleic acid levels in the arcuate nucleus on proestrus. Endocrinology 135 343350. (https://doi.org/10.1210/endo.135.1.7912184)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Arbogast LA & Voogt JL 2002 Progesterone induces dephosphorylation and inactivation of tyrosine hydroxylase in rat hypothalamic dopaminergic neurons. Neuroendocrinology 75 273281. (https://doi.org/10.1159/000057336)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Asghar ZA, Thompson A, Chi M, Cusumano A, Scheaffer S, Al-Hammadi N, Saben JL & Moley KH 2016 Maternal fructose drives placental uric acid production leading to adverse fetal outcomes. Scientific Reports 6 25091. (https://doi.org/10.1038/srep25091)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Avena NM, Rada P & Hoebel BG 2008 Evidence for sugar addiction: behavioral and neurochemical effects of intermittent, excessive sugar intake. Neuroscience and Biobehavioral Reviews 32 2039. (https://doi.org/10.1016/j.neubiorev.2007.04.019)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Beilharz JE, Maniam J & Morris MJ 2016 Short-term exposure to a diet high in fat and sugar, or liquid sugar, selectively impairs hippocampal-dependent memory, with differential impacts on inflammation. Behavioural Brain Research 306 17. (https://doi.org/10.1016/j.bbr.2016.03.018)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Bray GA 1997 Obesity and reproduction. Human Reproduction 12 (Supplement 1) 2632. (https://doi.org/10.1093/humrep/12.suppl_1.26)

  • Bray GA 2010 Fructose: pure, white, and deadly? Fructose, by any other name, is a health hazard. Journal of Diabetes Science and Technology 4 10031007. (https://doi.org/10.1177/193229681000400432)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Brown CM, Dulloo AG & Montani JP 2008 Sugary drinks in the pathogenesis of obesity and cardiovascular diseases. International Journal of Obesity 32 (Supplement 6) S28S34. (https://doi.org/10.1038/ijo.2008.204)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Bruce-Keller AJ, Keller JN & Morrison CD 2009 Obesity and vulnerability of the CNS. Biochimica et Biophysica Acta 1792 395400. (https://doi.org/10.1016/j.bbadis.2008.10.004)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Bursać BN, Djordjevic AD, Vasiljević AD, Milutinović DDV, Veličković NA, Nestorović NM & Matić GM 2013 Fructose consumption enhances glucocorticoid action in rat visceral adipose tissue. Journal of Nutritional Biochemistry 24 11661172. (https://doi.org/10.1016/j.jnutbio.2012.09.002)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Bursać BN, Vasiljević AD, Nestorović NM, Veličković NA, Vojnović Milutinović DD, Matić GM & Djordjevic AD 2014 High-fructose diet leads to visceral adiposity and hypothalamic leptin resistance in male rats – do glucocorticoids play a role? Journal of Nutritional Biochemistry 25 446455. (https://doi.org/10.1016/j.jnutbio.2013.12.005)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Buyukata C, Vukalo M, Xu TJ, Khore MA & Reichelt AC 2018 Impact of high sucrose diets on the discrimination of spatial and object memories with overlapping features. Physiology and Behavior 192 127133. (https://doi.org/10.1016/j.physbeh.2018.02.027)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Cacciapaglia F, Wightman RM & Carelli RM 2011 Rapid dopamine signaling differentially modulates distinct microcircuits within the nucleus accumbens during sucrose-directed behavior. Journal of Neuroscience 31 1386013869. (https://doi.org/10.1523/JNEUROSCI.1340-11.2011)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Chen L, Xie YM, Pei JH, Kuang J, Chen HM, Chen Z, Li ZW, Fu XY, Wang L, Lai SQ, et al.2018 Sugar-sweetened beverage intake and serum testosterone levels in adult males 20–39 years old in the United States. Reproductive Biology and Endocrinology 16 61. (https://doi.org/10.1186/s12958-018-0378-2)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Choi JY, Park MN, Kim CS, Lee YK, Choi EY, Chun WY & Shin DM 2017 Long-term consumption of sugar-sweetened beverage during the growth period promotes social aggression in adult mice with proinflammatory responses in the brain. Scientific Reports 7 45693. (https://doi.org/10.1038/srep45693)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Corona-Pérez A, Díaz-Muñoz M, Cuevas-Romero E, Luna-Moreno D, Valente-Godínez H, Vázquez-Martínez O, Martínez-Gómez M, Rodríguez-Antolín J & Nicolás-Toledo L 2017 Interactive effects of chronic stress and a high-sucrose diet on nonalcoholic fatty liver in young adult male rats. Stress 20 608617. (https://doi.org/10.1080/10253890.2017.1381840)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Dahm CH, Minagawa J & Jellinek M 1977 Effects of progesterone on some enzymes of fat and carbohydrate metabolism in rat liver. American Journal of Obstetrics and Gynecology 129 130132. (https://doi.org/10.1016/0002-9378(77)90732-3)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ducharme N, Banks WA, Morley JE, Robinson SM, Niehoff ML, Mattern C & Farr SA 2010 Brain distribution and behavioral effects of progesterone and pregnenolone after intranasal or intravenous administration. European Journal of Pharmacology 641 128134. (https://doi.org/10.1016/j.ejphar.2010.05.033)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Enos RT, Velázquez KT & Murphy EA 2014 Insight into the impact of dietary saturated fat on tissue-specific cellular processes underlying obesity-related diseases. Journal of Nutritional Biochemistry 25 600612. (https://doi.org/10.1016/j.jnutbio.2014.01.011)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Enos RT, Velázquez KT, McClellan JL, Cranford TL, Walla MD & Murphy EA 2015 Lowering the dietary omega-6: omega-3 does not hinder nonalcoholic fatty-liver disease development in a murine model. Nutrition Research 35 449459. (https://doi.org/10.1016/j.nutres.2015.04.003)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Enos RT, Velázquez KT, Carson MS, McClellan JL, Nagarkatti P, Nagarkatti M, Davis JM & Murphy EA 2016 A low dose of dietary quercetin fails to protect against the development of an obese phenotype in mice. PLoS ONE 11 e0167979. (https://doi.org/10.1371/journal.pone.0167979)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Floresco SB 2013 Prefrontal dopamine and behavioral flexibility: shifting from an ‘inverted-U’ toward a family of functions. Frontiers in Neuroscience 7 62. (https://doi.org/10.3389/fnins.2013.00062)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Floresco SB, Tse MTL & Ghods-Sharifi S 2008 Dopaminergic and glutamatergic regulation of effort- and delay-based decision making. Neuropsychopharmacology 33 19661979. (https://doi.org/10.1038/sj.npp.1301565)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Friberg E, Wallin A & Wolk A 2011 Sucrose, high-sugar foods, and risk of endometrial cancer – a population-based cohort study. Cancer Epidemiology, Biomarkers and Prevention 20 18311837. (https://doi.org/10.1158/1055-9965.EPI-11-0402)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Gaysinskaya VA, Karatayev O, Shuluk J & Leibowitz SF 2011 Hyperphagia induced by sucrose: relation to circulating and CSF glucose and corticosterone and orexigenic peptides in the arcuate nucleus. Pharmacology, Biochemistry, and Behavior 97 521530. (https://doi.org/10.1016/j.pbb.2010.10.008)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Hart RP, Coover GD, Shnerson A & Smotherman WP 1980 Plasma corticosterone elevations in rats in response to consumption of concentrated sugar solutions. Journal of Comparative and Physiological Psychology 94 337345. (https://doi.org/10.1037/h0077662)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Heimovics SA, Prior NH, Maddison CJ & Soma KK 2012 Rapid and widespread effects of 17β-estradiol on intracellular signaling in the male songbird brain: a seasonal comparison. Endocrinology 153 13641376. (https://doi.org/10.1210/en.2011-1525)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Hojo Y, Higo S, Ishii H, Ooishi Y, Mukai H, Murakami G, Kominami T, Kimoto T, Honma S, Poirier D, et al.2009 Comparison between hippocampus-synthesized and circulation-derived sex steroids in the hippocampus. Endocrinology 150 51065112. (https://doi.org/10.1210/en.2009-0305)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ikemoto S 2007 Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Research Reviews 56 2778. (https://doi.org/10.1016/j.brainresrev.2007.05.004)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Johnson RJ, Perez-Pozo SE, Sautin YY, Manitius J, Sanchez-Lozada LG, Feig DI, Shafiu M, Segal M, Glassock RJ, Shimada M, et al.2009 Hypothesis: could excessive fructose intake and uric acid cause type 2 diabetes? Endocrine Reviews 30 96116. (https://doi.org/10.1210/er.2008-0033)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Keer SE & Stern JM 1999 Dopamine receptor blockade in the nucleus accumbens inhibits maternal retrieval and licking, but enhances nursing behavior in lactating rats. Physiology and Behavior 67 659669. (https://doi.org/10.1016/S0031-9384(99)00116-X)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kendig MD, Rooney KB, Corbit LH & Boakes RA 2014 Persisting adiposity following chronic consumption of 10% sucrose solution: strain differences and behavioural effects. Physiology and Behavior 130 5465. (https://doi.org/10.1016/j.physbeh.2014.03.021)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kimoto T, Ishii H, Higo S, Hojo Y & Kawato S 2010 Semicomprehensive analysis of the postnatal age-related changes in the mRNA expression of sex steroidogenic enzymes and sex steroid receptors in the male rat hippocampus. Endocrinology 151 57955806. (https://doi.org/10.1210/en.2010-0581)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kjaergaard M, Nilsson C, Rosendal A, Nielsen MO & Raun K 2014 Maternal chocolate and sucrose soft drink intake induces hepatic steatosis in rat offspring associated with altered lipid gene expression profile. Acta Physiologica 210 142153. (https://doi.org/10.1111/apha.12138)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kleiner DE, Brunt EM, Van Natta M, Behling C, Contos MJ, Cummings OW, Ferrell LD, Liu YC, Torbenson MS, Unalp-Arida A, et al.2005 Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 41 13131321. (https://doi.org/10.1002/hep.20701)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kovacs CS 2016 Maternal mineral and bone metabolism during pregnancy, lactation, and post-weaning recovery. Physiological Reviews 96 449547. (https://doi.org/10.1152/physrev.00027.2015)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kuo T, McQueen A, Chen TC & Wang JC 2015 Regulation of glucose homeostasis by glucocorticoids. Advances in Experimental Medicine and Biology 872 99126. (https://doi.org/10.1007/978-1-4939-2895-8_5)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • la Fleur SE 2006 The effects of glucocorticoids on feeding behavior in rats. Physiology and Behavior 89 110114. (https://doi.org/10.1016/j.physbeh.2006.01.028)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Lesser EN, Arroyo-Ramirez A, Mi SJ & Robinson MJF 2017 The impact of a junk-food diet during development on ‘wanting’ and ‘liking’. Behavioural Brain Research 317 163178. (https://doi.org/10.1016/j.bbr.2016.09.041)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Lomba A, Milagro FI, García-Díaz DF, Campión J, Marzo F & Martínez JA 2009 A high-sucrose isocaloric pair-fed model induces obesity and impairs NDUFB6 gene function in rat adipose tissue. Journal of Nutrigenetics and Nutrigenomics 2 267272. (https://doi.org/10.1159/000308465)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Maniam J, Antoniadis CP, Youngson NA, Sinha JK & Morris MJ 2015 Sugar consumption produces effects similar to early life stress exposure on hippocampal markers of neurogenesis and stress response. Frontiers in Molecular Neuroscience 8 86. (https://doi.org/10.3389/fnmol.2015.00086)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Matkowskyj KA, Schonfeld D & Benya RV 2000 Quantitative immunohistochemistry by measuring cumulative signal strength using commercially available software Photoshop and MATLAB. Journal of Histochemistry and Cytochemistry 48 303312. (https://doi.org/10.1177/002215540004800216)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • McMahon M, Gerich J & Rizza R 1988 Effects of glucocorticoids on carbohydrate metabolism. Diabetes/Metabolism Reviews 4 1730. (https://doi.org/10.1002/dmr.5610040105)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Mermelstein PG & Becker JB 1995 Increased extracellular dopamine in the nucleus accumbens and striatum of the female rat during paced copulatory behavior. Behavioral Neuroscience 109 354365. (https://doi.org/10.1037//0735-7044.109.2.354)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Michelotti GA, Machado MV & Diehl AM 2013 NAFLD, NASH and liver cancer. Nature Reviews: Gastroenterology and Hepatology 10 656665. (https://doi.org/10.1038/nrgastro.2013.183)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Mizuno G, Munetsuna E, Yamada H, Ando Y, Yamazaki M, Murase Y, Kondo K, Ishikawa H, Teradaira R, Suzuki K, et al.2017 Fructose intake during gestation and lactation differentially affects the expression of hippocampal neurosteroidogenic enzymes in rat offspring. Endocrine Research 42 7177. (https://doi.org/10.1080/07435800.2016.1182186)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Mohr MA, Wong AM, Tomm RJ, Soma KK & Micevych PE 2019 Pubertal development of estradiol-induced hypothalamic progesterone synthesis. Hormones and Behavior 111 110113. (https://doi.org/10.1016/j.yhbeh.2018.12.007)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Mosedale DE, Metcalfe JC & Grainger DJ 1996 Optimization of immunofluorescence methods by quantitative image analysis. Journal of Histochemistry and Cytochemistry 44 10431050. (https://doi.org/10.1177/44.9.8773570)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Muschamp JW, Nemeth CL, Robison AJ, Nestler EJ & Carlezon WA 2012 ΔFosB enhances the rewarding effects of cocaine while reducing the pro-depressive effects of the kappa-opioid receptor agonist U50488. Biological Psychiatry 71 4450. (https://doi.org/10.1016/j.biopsych.2011.08.011)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Newens KJ & Walton J 2016 A review of sugar consumption from nationally representative dietary surveys across the world. Journal of Human Nutrition and Dietetics 29 225240. (https://doi.org/10.1111/jhn.12338)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ohashi K, Ando Y, Munetsuna E, Yamada H, Yamazaki M, Nagura A, Taromaru N, Ishikawa H, Suzuki K & Teradaira R 2015 Maternal fructose consumption alters messenger RNA expression of hippocampal StAR, PBR, P450(11β), 11β-HSD, and 17β-HSD in rat offspring. Nutrition Research 35 259264. (https://doi.org/10.1016/j.nutres.2014.11.001)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Oliveira LSC, Santos DA, Barbosa-da-Silva S, Mandarim-de-Lacerda CA & Aguila MB 2014 The inflammatory profile and liver damage of a sucrose-rich diet in mice. Journal of Nutritional Biochemistry 25 193200. (https://doi.org/10.1016/j.jnutbio.2013.10.006)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Paxinos G & Watson C 2007 The rat brain in stereotaxic coordinates. 6th edn. Cambridge, MA, USA: Academic Press.

  • Pecoraro N, Reyes F, Gomez F, Bhargava A & Dallman MF 2004 Chronic stress promotes palatable feeding, which reduces signs of stress: feedforward and feedback effects of chronic stress. Endocrinology 145 37543762. (https://doi.org/10.1210/en.2004-0305)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Pinheiro J, Bates D, Debroy S, Sarkar D & R Core Team 2019 nlme: linear and nonlinear mixed effects models. R package version 3.1-141. (available at: https://CRAN.R-project.org/package=nlme)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Rada P, Avena NM & Hoebel BG 2005 Daily bingeing on sugar repeatedly releases dopamine in the accumbens shell. Neuroscience 134 737744. (https://doi.org/10.1016/j.neuroscience.2005.04.043)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Rafacho A, Ortsäter H, Nadal A & Quesada I 2014 Glucocorticoid treatment and endocrine pancreas function: implications for glucose homeostasis, insulin resistance and diabetes. Journal of Endocrinology 223 R49R62. (https://doi.org/10.1530/JOE-14-0373)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Reichelt AC, Abbott KN, Fred Westbrook RF & Morris MJ 2016 Differential motivational profiles following adolescent sucrose access in male and female rats. Physiology and Behavior 157 1319. (https://doi.org/10.1016/j.physbeh.2016.01.038)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Robison AJ & Nestler EJ 2011 Transcriptional and epigenetic mechanisms of addiction. Nature Reviews: Neuroscience 12 623637. (https://doi.org/10.1038/nrn3111)

  • Ruff JS, Suchy AK, Hugentobler SA, Sosa MM, Schwartz BL, Morrison LC, Gieng SH, Shigenaga MK & Potts WK 2013 Human-relevant levels of added sugar consumption increase female mortality and lower male fitness in mice. Nature Communications 4 2245. (https://doi.org/10.1038/ncomms3245)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Saben JL, Asghar ZA, Rhee JS, Drury A, Scheaffer S & Moley KH 2016 Excess maternal fructose consumption increases fetal loss and impairs endometrial decidualization in mice. Endocrinology 157 956968. (https://doi.org/10.1210/en.2015-1618)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, et al.2012 Fiji: an open-source platform for biological-image analysis. Nature Methods 9 676682. (https://doi.org/10.1038/nmeth.2019)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Schmidt KL & Soma KK 2008 Cortisol and corticosterone in the songbird immune and nervous systems: local vs. systemic levels during development. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology 295 R103R110. (https://doi.org/10.1152/ajpregu.00002.2008)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Sharpe MJ, Clemens KJ, Morris MJ & Westbrook RF 2016 Daily exposure to sucrose impairs subsequent learning about food cues: a role for alterations in ghrelin signalling and dopamine D2 receptors. Neuropsychopharmacology 41 13571365. (https://doi.org/10.1038/npp.2015.287)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Stafeev IS, Vorotnikov AV, Ratner EI, Menshikov MY & Parfyonova YV 2017 Latent inflammation and insulin resistance in adipose tissue. International Journal of Endocrinology 2017 5076732. (https://doi.org/10.1155/2017/5076732)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Steingrimsdottir L, Greenwood MRC & Brasel JA 1980 Effect of pregnancy, lactation and a high-fat diet on adipose tissue in Osborne-Mendel Rats. Journal of Nutrition 110 600609. (https://doi.org/10.1093/jn/110.4.600)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Tappy L & KA 2010 Metabolic effects of fructose and the worldwide increase in obesity. Physiological Reviews 90 2346. (https://doi.org/10.1152/physrev.00019.2009)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Taves MD, Ma C, Heimovics SA, Saldanha CJ & Soma KK 2011 Measurement of steroid concentrations in brain tissue: methodological considerations. Frontiers in Endocrinology 2 39. (https://doi.org/10.3389/fendo.2011.00039)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Taves MD, Hamden JE & Soma KK 2017 Local glucocorticoid production in lymphoid organs of mice and birds: functions in lymphocyte development. Hormones and Behavior 88 414. (https://doi.org/10.1016/j.yhbeh.2016.10.022)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Tirosh A, Garg R & Adler GK 2010 Mineralocorticoid receptor antagonists and the metabolic syndrome. Current Hypertension Reports 12 252257. (https://doi.org/10.1007/s11906-010-0126-2)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Tobiansky DJ, Roma PG, Hattori T, Will RG, Nutsch VL & Dominguez JM 2013 The medial preoptic area modulates cocaine-induced activity in female rats. Behavioral Neuroscience 127 293302. (https://doi.org/10.1037/a0031949)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Tobiansky DJ, Will RG, Lominac KD, Turner JM, Hattori T, Krishnan K, Martz JR, Nutsch VL & Dominguez JM 2016 Estradiol in the preoptic area regulates the dopaminergic response to cocaine in the nucleus accumbens. Neuropsychopharmacology 41 18971906. (https://doi.org/10.1038/npp.2015.360)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Tobiansky DJ, Wallin-Miller KG, Floresco SB, Wood RI & Soma KK 2018a Androgen regulation of the mesocorticolimbic system and executive function. Frontiers in Endocrinology 9 279. (https://doi.org/10.3389/fendo.2018.00279)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Tobiansky DJ, Korol AM, Ma C, Hamden JE, Jalabert C, Tomm RJ & Soma KK 2018b Testosterone and corticosterone in the mesocorticolimbic system of male rats: effects of gonadectomy and caloric restriction. Endocrinology 159 450464. (https://doi.org/10.1210/en.2017-00704)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Tomm RJ, Tse MT, Tobiansky DJ, Schweitzer HR, Soma KK & Floresco SB 2018 Effects of aging on executive functioning and mesocorticolimbic dopamine markers in male Fischer 344 × brown Norway rats. Neurobiology of Aging 72 134146. (https://doi.org/10.1016/j.neurobiolaging.2018.08.020)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Vasiljević A, Bursać B, Djordjevic A, Milutinović DV, Nikolić M, Matić G & Veličković N 2014 Hepatic inflammation induced by high-fructose diet is associated with altered 11βHSD1 expression in the liver of Wistar rats. European Journal of Nutrition 53 13931402. (https://doi.org/10.1007/s00394-013-0641-4)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Wei R, Wang J, Su M, Jia E, Chen S, Chen T & Ni Y 2018 Missing value imputation approach for mass spectrometry-based metabolomics data. Scientific Reports 8 663. (https://doi.org/10.1038/s41598-017-19120-0)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Welsh JA, Sharma AJ, Grellinger L & Vos MB 2011 Consumption of added sugars is decreasing in the United States. American Journal of Clinical Nutrition 94 726734. (https://doi.org/10.3945/ajcn.111.018366)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Wild P, Rupp N, Buhmann J, Schüffler P, Fuchs T & Ong C 2013 TMARKER: a free software toolkit for histopathological cell counting and staining estimation. Journal of Pathology Informatics 4 2. (https://doi.org/10.4103/2153-3539.109804)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • World Health Organization 2015 Guideline: Sugars intake for adults and children. Geneva, Switzerland: World Health Organisation . (available at: https://www.who.int/nutrition/publications/guidelines/sugars_intake/en/)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Zhang Y, Crofton EJ, Li D, Lobo MK, Fan X, Nestler EJ & Green TA 2014 Overexpression of DeltaFosB in nucleus accumbens mimics the protective addiction phenotype, but not the protective depression phenotype of environmental enrichment. Frontiers in Behavioral Neuroscience 8 297. (https://doi.org/10.3389/fnbeh.2014.00297)

    • PubMed
    • Search Google Scholar
    • Export Citation