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Emotional Eating in Socially Subordinate Female Rhesus Monkeys

  • Vasiliki MichopoulosEmail author
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Part of the Developments in Primatology: Progress and Prospects book series (DIPR)

Abstract

Prolonged states of energy excess result in obesity and increase risk for an array of other adverse health outcomes. The increase in rates of obesity in the last decade has been linked to emotional eating that arises from the accessibility of highly palatable diets under the conditions of chronic psychosocial stress exposure. Thus, understanding factors that contribute to an obese phenotype is critical for identifying novel interventional targets that alleviate the health burden imposed by obesity and obesity-related adverse health outcomes. One translational animal model that has been leveraged to study the adverse health effects of chronic stressor exposure is that of social subordination in socially housed female macaques. Uncontrollable, unpredictable psychogenic stress exposure in the form of harassment from higher-ranking animals within a social group is associated with increased caloric intake in a dietary environment wherein both a low-calorie diet (LCD) and a calorically dense diet (CDD), high in fat and sugar, are available. This emotional eating phenotype in subordinate monkeys is comorbid with dysregulation of the stress axis and the reward system. More recent studies have shown that pharmacological blockade of corticotropin-releasing hormone (CRH) activity attenuates emotional eating in subordinate females and also increases limbic levels of dopamine D2 receptors (D2R). Together, these data suggest that stress-induced hyperphagia in subordinates is sustained by stress-induced changes in mesolimbic D2R levels. Future investigations studying the effects of social subordination in macaques will focus on delineating the effects of chronic psychosocial stress exposure and access to a CDD throughout development to adversely impact biobehavioral outcomes related to health.

Keywords

Emotional Eating Cortisol Reactivity Dominant Female Obese Phenotype Subordinate Female 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We would like to thank Jennifer Whitley, Angela Tripp, Brandon Hughes, Shannon Bounar, Jodi Godfrey, Christine Marsteller, Jonathon Lowe, Patrick Ulam, Rebecca Herman, Robert Johnston and Gregory Henry for their expert technical assistance in conducting the feeding studies summarized in the current chapter. We also thank Drs. Mark Wilson, Donna Toufexis, Zachary Johnson, and Carla Moore for helping shape our understanding of the relationship between stressor exposure and emotional eating. These studies would not have been possible without the dedication of the animal husbandry staff at the Yerkes National Primate Research Center (YNPRC) and support by NIH grants HD46501, MH081816, RR00165, and F31MH085445. Further support was provided by the Center for Behavioral Neuroscience through the STC Program of the National Science Foundation IBN-9876754. The YNPRC is fully accredited by the Association for Assessment and Accreditation of Laboratory Animal Care International.

References

  1. Adam TC, Epel ES (2007) Stress, eating and the reward system. Physiol Behav 91:449–458PubMedCrossRefGoogle Scholar
  2. Adams MR, Kaplan JR, Koritnik DR (1985) Psychosocial influences on ovarian endocrine and ovulatory function in Macaca fascicularis. Physiol Behav 35:935–940PubMedCrossRefGoogle Scholar
  3. Andrews RC, Walker BR (1999) Glucocorticoids and insulin resistance: old hormones, new targets. Clin Sci (Lond) 96:513–523CrossRefGoogle Scholar
  4. Arce M, Michopoulos V, Shepard KN, Ha QC, Wilson ME (2010) Diet choice, cortisol reactivity, and emotional feeding in socially housed rhesus monkeys. Physiol Behav 101:446–455PubMedPubMedCentralCrossRefGoogle Scholar
  5. Armario A (2006) The hypothalamic-pituitary-adrenal axis: what can it tell us about stressors? CNS Neurol Disord: Drug Targets 5:485–501CrossRefGoogle Scholar
  6. Asarian L, Geary N (2013) Sex differences in the physiology of eating. Am J Physiol 305:R1215–R1267Google Scholar
  7. Auvinen HE, Romijn JA, Biermasz NR, Havekes LM, Smit JW, Rensen PC, Pereira AM (2011) Effects of high fat diet on the basal activity of the hypothalamus-pituitary-adrenal axis in mice: a systematic review. Hormon- und Stoffwechselforschung (Horm Metab Res) 43:899–906CrossRefGoogle Scholar
  8. Bale TL, Vale WW (2004) CRF and CRF receptors: role in stress responsivity and other behaviors. Annu Rev Pharmacol Toxicol 44:525–557PubMedCrossRefGoogle Scholar
  9. Barry D, Pietrzak RH, Petry NM (2008) Gender differences in associations between body mass index and DSM-IV mood and anxiety disorders: results from the National Epidemiologic Survey on Alcohol and Related Conditions. Ann Epidemiol 18:458–466PubMedPubMedCentralCrossRefGoogle Scholar
  10. Behan DP, Grigoriadis DE, Lovenberg T, Chalmers D, Heinrichs S, Liaw C, De Souza EB (1996) Neurobiology of corticotropin releasing factor (CRF) receptors and CRF-binding protein: implications for the treatment of CNS disorders. Molecular psychiatry 1:265–277PubMedGoogle Scholar
  11. Bernstein IS (1976) Dominance, aggression and reproduction in primate societies. J Theor Biol 60:459–472PubMedCrossRefGoogle Scholar
  12. Bernstein IS, Gordon TP (1974) The function of aggression in primate societies. Am Sci 62:304–311PubMedGoogle Scholar
  13. Bernstein IS, Gordon TP, Rose RM (1974) Aggression and social controls in rhesus monkey (Macaca mulatta) groups revealed in group formation studies. Folia Primatol (Basel) 21:81–107CrossRefGoogle Scholar
  14. Bhatnagar S, Dallman M (1998) Neuroanatomical basis for facilitation of hypothalamic-pituitary-adrenal responses to a novel stressor after chronic stress. Neuroscience 84:1025–1039PubMedCrossRefGoogle Scholar
  15. Bhatnagar S, Vining C (2003) Facilitation of hypothalamic-pituitary-adrenal responses to novel stress following repeated social stress using the resident/intruder paradigm. Horm Behav 43:158–165PubMedCrossRefGoogle Scholar
  16. Bhatnagar S, Dallman MF, Roderick RE, Basbaum AI, Taylor BK (1998) The effects of prior chronic stress on cardiovascular responses to acute restraint and formalin injection. Brain Res 797:313–320PubMedCrossRefGoogle Scholar
  17. Bhatnagar S, Vining C, Iyer V, Kinni V (2006) Changes in hypothalamic-pituitary-adrenal function, body temperature, body weight and food intake with repeated social stress exposure in rats. J Neuroendocrinol 18:13–24PubMedCrossRefGoogle Scholar
  18. Bjorntorp P (2001) Do stress reactions cause abdominal obesity and comorbidities? Obes Rev 2:73–86PubMedCrossRefGoogle Scholar
  19. Broadbear JH, Winger G, Rivier JE, Rice KC, Woods JH (2004) Corticotropin-releasing hormone antagonists, astressin B and antalarmin: differing profiles of activity in rhesus monkeys. Neuropsychopharmacology 29:1112–1121PubMedCrossRefGoogle Scholar
  20. Buwalda B, Blom WA, Koolhaas JM, van Dijk G (2001) Behavioral and physiological responses to stress are affected by high-fat feeding in male rats. Physiol Behav 73:371–377PubMedCrossRefGoogle Scholar
  21. Chalmers DT, Lovenberg TW, Grigoriadis DE, Behan DP, De Souza EB (1996) Corticotrophin-releasing factor receptors: from molecular biology to drug design. Trends Pharmacol Sci 17:166–172PubMedCrossRefGoogle Scholar
  22. Chrousos GP, Gold PW (1992) The concepts of stress and stress system disorders. Overview of physical and behavioral homeostasis. JAMA 267:1244–1252PubMedCrossRefGoogle Scholar
  23. Chrousos GP, Kino T (2007) Glucocorticoid action networks and complex psychiatric and/or somatic disorders. Stress 10:213–219Google Scholar
  24. Cohen S (1999) Social status and susceptibility to respiratory infections. Ann NY Acad Sci 896:246–253PubMedCrossRefGoogle Scholar
  25. Collura LA, Hoffman JB, Wilson ME (2009) Administration of human leptin differentially affects parameters of cortisol secretion in socially housed female rhesus monkeys. Endocrine 36:530–537PubMedCrossRefGoogle Scholar
  26. Coryell W, Fiedorowicz J, Zimmerman M, Young E (2008) HPA-axis hyperactivity and mortality in psychotic depressive disorder: preliminary findings. Psychoneuroendocrinology 33:654–658PubMedPubMedCentralCrossRefGoogle Scholar
  27. Dallman MF, Pecoraro NC, la Fleur SE (2005) Chronic stress and comfort foods: self-medication and abdominal obesity. Brain Behav Immun 19:275–280PubMedCrossRefGoogle Scholar
  28. de Kloet ER, Sibug RM, Helmerhorst FM, Schmidt MV (2005) Stress, genes and the mechanism of programming the brain for later life. Neurosci Biobehav Rev 29:271–281PubMedCrossRefGoogle Scholar
  29. Duclos M, Marquez Pereira P, Barat P, Gatta B, Roger P (2005) Increased cortisol bioavailability, abdominal obesity, and the metabolic syndrome in obese women. Obes Res 13:1157–1166PubMedCrossRefGoogle Scholar
  30. Epel ES, McEwen B, Seeman T, Matthews K, Castellazzo G, Brownell KD, Bell J, Ickovics JR (2000) Stress and body shape: stress-induced cortisol secretion is consistently greater among women with central fat. Psychosom Med 62:623–632PubMedCrossRefGoogle Scholar
  31. Epel E, Lapidus R, McEwen B, Brownell K (2001) Stress may add bite to appetite in women: a laboratory study of stress-induced cortisol and eating behavior. Psychoneuroendocrinology 26:37–49PubMedCrossRefGoogle Scholar
  32. Farmer A, Korszun A, Owen MJ, Craddock N, Jones L, Jones I, Gray J, Williamson RJ, McGuffin P (2008) Medical disorders in people with recurrent depression. Br J Psychiatry 192:351–355PubMedCrossRefGoogle Scholar
  33. Flegal KM (2005) Epidemiologic aspects of overweight and obesity in the United States. Physiol Behav 86:599–602PubMedCrossRefGoogle Scholar
  34. Flegal KM, Carroll MD, Ogden CL, Curtin LR (2010) Prevalence and trends in obesity among US adults, 1999-2008. JAMA 303:235–241PubMedCrossRefGoogle Scholar
  35. Fong AK, Kretsch MJ (1993) Changes in dietary intake, urinary nitrogen, and urinary volume across the menstrual cycle. Am J Clin Nutr 57:43–46PubMedGoogle Scholar
  36. Gamaro GD, Manoli LP, Torres IL, Silveira R, Dalmaz C (2003) Effects of chronic variate stress on feeding behavior and on monoamine levels in different rat brain structures. Neurochem Int 42:107–114PubMedCrossRefGoogle Scholar
  37. Geary N (2000) Estradiol and appetite. Appetite 35:273–274PubMedCrossRefGoogle Scholar
  38. Gibson EL (2006) Emotional influences on food choice: sensory, physiological, and psychological pathways. Physiol Behav (in press)Google Scholar
  39. Goldstein JM, Jerram M, Abbs B, Whitfield-Gabrieli S, Makris N (2010) Sex differences in stress response circuitry activation dependent on female hormonal cycle. J Neurosci 30:431–438PubMedPubMedCentralCrossRefGoogle Scholar
  40. Gong EJ, Garrel D, Calloway DH (1989) Menstrual cycle and voluntary food intake. Am J Clin Nutr 49:252–258PubMedGoogle Scholar
  41. Grant KA, Shively CA, Nader MA, Ehrenkaufer RL, Line SW, Morton TE, Gage HD, Mach RH (1998) Effect of social status on striatal dopamine D2 receptor binding characteristics in cynomolgus monkeys assessed with positron emission tomography. Synapse 29:80–83Google Scholar
  42. Grunberg NE, Straub RO (1992) The role of gender and taste class in the effects of stress on eating. Health Psychol 11:97–100PubMedCrossRefGoogle Scholar
  43. Gust DA, Gordon TP, Wilson ME, Ahmed-Ansari A, Brodie AR, McClure HM (1991) Formation of a new social group of unfamiliar female rhesus monkeys affects the immune and pituitary adrenocortical systems. Brain Behav Immun 5:296–307PubMedCrossRefGoogle Scholar
  44. Hall FS, Wilkinson LS, Humby T, Inglis W, Kendall DA, Marsden CA, Robbins TW (1998) Isolation rearing in rats: pre- and postsynaptic changes in striatal dopaminergic systems. Pharmacol Biochem Behav 59:859–872PubMedCrossRefGoogle Scholar
  45. Hill JO (2006) Understanding and addressing the epidemic of obesity: an energy balance perspective. Endocr Rev 27:750–761PubMedCrossRefGoogle Scholar
  46. Holsboer F (2001) Stress, hypercortisolism and corticosteroid receptors in depression: implications for therapy. J Affect Disord 62:77–91PubMedCrossRefGoogle Scholar
  47. Iemolo A, Blasio A, St Cyr SA, Jiang F, Rice KC, Sabino V, Cottone P (2013) CRF-CRF1 receptor system in the central and basolateral nuclei of the amygdala differentially mediates excessive eating of palatable food. Neuropsychopharmacology 38:2456–2466PubMedPubMedCentralCrossRefGoogle Scholar
  48. Izzo E, Sanna PP, Koob GF (2005) Impairment of dopaminergic system function after chronic treatment with corticotropin-releasing factor. Pharmacol Biochem Behav 81:701–708PubMedCrossRefGoogle Scholar
  49. Jaferi A, Bhatnagar S (2006) Corticosterone can act at the posterior paraventricular thalamus to inhibit hypothalamic-pituitary-adrenal activity in animals that habituate to repeated stress. Endocrinology 147:4917–4930PubMedCrossRefGoogle Scholar
  50. Jarrell H, Hoffman JB, Kaplan JR, Berga S, Kinkead B, Wilson ME (2008) Polymorphisms in the serotonin reuptake transporter gene modify the consequences of social status on metabolic health in female rhesus monkeys. Physiol Behav 93:807–819PubMedPubMedCentralCrossRefGoogle Scholar
  51. Jayo JM, Shively CA, Kaplan JR, Manuck SB (1993) Effects of exercise and stress on body fat distribution in male cynomolgus monkeys. Int J Obes Relat Metab Disord 17:597–604PubMedGoogle Scholar
  52. Jochman KA, Newman SM, Kalin NH, Bakshi VP (2005) Corticotropin-releasing factor-1 receptors in the basolateral amygdala mediate stress-induced anorexia. Behav Neurosci 119:1448–1458PubMedCrossRefGoogle Scholar
  53. Johnson PM, Kenny PJ (2010) Dopamine D2 receptors in addiction-like reward dysfunction and compulsive eating in obese rats. Nat Neurosci 13:635–641PubMedPubMedCentralCrossRefGoogle Scholar
  54. Johnson WG, Corrigan SA, Lemmon CR, Bergeron KB, Crusco AH (1994) Energy regulation over the menstrual cycle. Physiol Behav 56:523–527PubMedCrossRefGoogle Scholar
  55. Johnson ZP, Lowe J, Michopoulos V, Moore CJ, Wilson ME, Toufexis D (2013) Oestradiol differentially influences feeding behaviour depending on diet composition in female rhesus monkeys. J Neuroendocrinol 25:729–741PubMedPubMedCentralCrossRefGoogle Scholar
  56. Jokinen J, Nordstrom AL, Nordstrom P (2008) ROC analysis of dexamethasone suppression test threshold in suicide prediction after attempted suicide. J Affect Disord 106:145–152PubMedCrossRefGoogle Scholar
  57. Jones LE, Carney CP (2006) Increased risk for metabolic syndrome in persons seeking care for mental disorders. Ann Clin Psychiatry 18:149–155PubMedCrossRefGoogle Scholar
  58. Kamara K, Eskay R, Castonguay T (1998) High-fat diets and stress responsivity. Physiol Behav 64:1–6PubMedCrossRefGoogle Scholar
  59. Kaplan JR, Adams MR, Clarkson TB, Manuck SB, Shively CA, Williams JK (1996) Psychosocial factors, sex differences, and atherosclerosis: lessons from animal models. Psychosom Med 58:598–611PubMedCrossRefGoogle Scholar
  60. Kaplan JR, Chen H, Appt SE, Lees CJ, Franke AA, Berga SL, Wilson ME, Manuck SB, Clarkson TB (2010) Impairment of ovarian function and associated health-related abnormalities are attributable to low social status in premenopausal monkeys and not mitigated by a high-isoflavone soy diet. Human reproduction (Oxford, England) 25:3083–3094CrossRefGoogle Scholar
  61. Kassirer JP, Angell M (1998) Losing weight—an ill-fated New Year’s resolution. The New England journal of medicine 338:52–54PubMedCrossRefGoogle Scholar
  62. Keck ME, Welt T, Wigger A, Renner U, Engelmann M, Holsboer F, Landgraf R (2001) The anxiolytic effect of the CRH(1) receptor antagonist R121919 depends on innate emotionality in rats. Eur J Neurosci 13:373–380PubMedCrossRefGoogle Scholar
  63. Koob GF, Le Moal M (2001) Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology 24:97–129PubMedCrossRefGoogle Scholar
  64. Leibowitz SF, Akabayashi A, Alexander J, Karatayev O, Chang GQ (2009) Puberty onset in female rats: relationship with fat intake, ovarian steroids and the peptides, galanin and enkephalin, in the paraventricular and medial preoptic nuclei. J Neuroendocrinol 21:538–549PubMedPubMedCentralCrossRefGoogle Scholar
  65. Lissner L, Stevens J, Levitsky DA, Rasmussen KM, Strupp BJ (1988) Variation in energy intake during the menstrual cycle: implications for food-intake research. Am J Clin Nutr 48:956–962PubMedGoogle Scholar
  66. Locke AE, Kahali B, Berndt SI, Justice AE, Pers TH, Day FR, Powell C, Vedantam S, Buchkovich ML, Yang J, Croteau-Chonka DC, Esko T, Fall T, Ferreira T, Gustafsson S, Kutalik Z, Luan J, Magi R, Randall JC, Winkler TW, Wood AR, Workalemahu T, Faul JD, Smith JA, Hua Zhao J, Zhao W, Chen J, Fehrmann R, Hedman AK, Karjalainen J, Schmidt EM, Absher D, Amin N, Anderson D, Beekman M, Bolton JL, Bragg-Gresham JL, Buyske S, Demirkan A, Deng G, Ehret GB, Feenstra B, Feitosa MF, Fischer K, Goel A, Gong J, Jackson AU, Kanoni S, Kleber ME, Kristiansson K, Lim U, Lotay V, Mangino M, Mateo Leach I, Medina-Gomez C, Medland SE, Nalls MA, Palmer CD, Pasko D, Pechlivanis S, Peters MJ, Prokopenko I, Shungin D, Stancakova A, Strawbridge RJ, Ju Sung Y, Tanaka T, Teumer A, Trompet S, van der Laan SW, van Setten J, Van Vliet-Ostaptchouk JV, Wang Z, Yengo L, Zhang W, Isaacs A, Albrecht E, Arnlov J, Arscott GM, Attwood AP, Bandinelli S, Barrett A, Bas IN, Bellis C, Bennett AJ, Berne C, Blagieva R, Bluher M, Bohringer S, Bonnycastle LL, Bottcher Y, Boyd HA, Bruinenberg M, Caspersen IH, Ida Chen YD, Clarke R, Daw EW, de Craen AJ, Delgado G, Dimitriou M, Doney AS, Eklund N, Estrada K, Eury E, Folkersen L, Fraser RM, Garcia ME, Geller F, Giedraitis V, Gigante B, Go AS, Golay A, Goodall AH, Gordon SD, Gorski M, Grabe HJ, Grallert H, Grammer TB, Grassler J, Gronberg H, Groves CJ, Gusto G, Haessler J, Hall P, Haller T, Hallmans G, Hartman CA, Hassinen M, Hayward C, Heard-Costa NL, Helmer Q, Hengstenberg C, Holmen O, Hottenga JJ, James AL, Jeff JM, Johansson A, Jolley J, Juliusdottir T, Kinnunen L, Koenig W, Koskenvuo M, Kratzer W, Laitinen J, Lamina C, Leander K, Lee NR, Lichtner P, Lind L, Lindstrom J, Sin Lo K, Lobbens S, Lorbeer R, Lu Y, Mach F, Magnusson PK, Mahajan A, McArdle WL, McLachlan S, Menni C, Merger S, Mihailov E, Milani L, Moayyeri A, Monda KL, Morken MA, Mulas A, Muller G, Muller-Nurasyid M, Musk AW, Nagaraja R, Nothen MM, Nolte IM, Pilz S, Rayner NW, Renstrom F, Rettig R, Ried JS, Ripke S, Robertson NR, Rose LM, Sanna S, Scharnagl H, Scholtens S, Schumacher FR, Scott WR, Seufferlein T, Shi J, Vernon Smith A, Smolonska J, Stanton AV, Steinthorsdottir V, Stirrups K, Stringham HM, Sundstrom J, Swertz MA, Swift AJ, Syvanen AC, Tan ST, Tayo BO, Thorand B, Thorleifsson G, Tyrer JP, Uh HW, Vandenput L, Verhulst FC, Vermeulen SH, Verweij N, Vonk JM, Waite LL, Warren HR, Waterworth D, Weedon MN, Wilkens LR, Willenborg C, Wilsgaard T, Wojczynski MK, Wong A, Wright AF, Zhang Q, Brennan EP, Choi M, Dastani Z, Drong AW, Eriksson P, Franco-Cereceda A, Gadin JR, Gharavi AG, Goddard ME, Handsaker RE, Huang J, Karpe F, Kathiresan S, Keildson S, Kiryluk K, Kubo M, Lee JY, Liang L, Lifton RP, Ma B, McCarroll SA, McKnight AJ, Min JL, Moffatt MF, Montgomery GW, Murabito JM, Nicholson G, Nyholt DR, Okada Y, Perry JR, Dorajoo R, Reinmaa E, Salem RM, Sandholm N, Scott RA, Stolk L, Takahashi A, Van’t Hooft FM, Vinkhuyzen AA, Westra HJ, Zheng W, Zondervan KT, Heath AC, Arveiler D, Bakker SJ, Beilby J, Bergman RN, Blangero J, Bovet P, Campbell H, Caulfield MJ, Cesana G, Chakravarti A, Chasman DI, Chines PS, Collins FS, Crawford DC, Cupples LA, Cusi D, Danesh J, de Faire U, den Ruijter HM, Dominiczak AF, Erbel R, Erdmann J, Eriksson JG, Farrall M, Felix SB, Ferrannini E, Ferrieres J, Ford I, Forouhi NG, Forrester T, Franco OH, Gansevoort RT, Gejman PV, Gieger C, Gottesman O, Gudnason V, Gyllensten U, Hall AS, Harris TB, Hattersley AT, Hicks AA, Hindorff LA, Hingorani AD, Hofman A, Homuth G, Hovingh GK, Humphries SE, Hunt SC, Hypponen E, Illig T, Jacobs KB, Jarvelin MR, Jockel KH, Johansen B, Jousilahti P, Jukema JW, Jula AM, Kaprio J, Kastelein JJ, Keinanen-Kiukaanniemi SM, Kiemeney LA, Knekt P, Kooner JS, Kooperberg C, Kovacs P, Kraja AT, Kumari M, Kuusisto J, Lakka TA, Langenberg C, Le Marchand L, Lehtimaki T, Lyssenko V, Mannisto S, Marette A, Matise TC, McKenzie CA, McKnight B, Moll FL, Morris AD, Morris AP, Murray JC, Nelis M, Ohlsson C, Oldehinkel AJ, Ong KK, Madden PA, Pasterkamp G, Peden JF, Peters A, Postma DS, Pramstaller PP, Price JF, Qi L, Raitakari OT, Rankinen T, Rao DC, Rice TK, Ridker PM, Rioux JD, Ritchie MD, Rudan I, Salomaa V, Samani NJ, Saramies J, Sarzynski MA, Schunkert H, Schwarz PE, Sever P, Shuldiner AR, Sinisalo J, Stolk RP, Strauch K, Tonjes A, Tregouet DA, Tremblay A, Tremoli E, Virtamo J, Vohl MC, Volker U, Waeber G, Willemsen G, Witteman JC, Zillikens MC, Adair LS, Amouyel P, Asselbergs FW, Assimes TL, Bochud M, Boehm BO, Boerwinkle E, Bornstein SR, Bottinger EP, Bouchard C, Cauchi S, Chambers JC, Chanock SJ, Cooper RS, de Bakker PI, Dedoussis G, Ferrucci L, Franks PW, Froguel P, Groop LC, Haiman CA, Hamsten A, Hui J, Hunter DJ, Hveem K, Kaplan RC, Kivimaki M, Kuh D, Laakso M, Liu Y, Martin NG, Marz W, Melbye M, Metspalu A, Moebus S, Munroe PB, Njolstad I, Oostra BA, Palmer CN, Pedersen NL, Perola M, Perusse L, Peters U, Power C, Quertermous T, Rauramaa R, Rivadeneira F, Saaristo TE, Saleheen D, Sattar N, Schadt EE, Schlessinger D, Slagboom PE, Snieder H, Spector TD, Thorsteinsdottir U, Stumvoll M, Tuomilehto J, Uitterlinden AG, Uusitupa M, van der Harst P, Walker M, Wallaschofski H, Wareham NJ, Watkins H, Weir DR, Wichmann HE, Wilson JF, Zanen P, Borecki IB, Deloukas P, Fox CS, Heid IM, O’Connell JR, Strachan DP, Stefansson K, van Duijn CM, Abecasis GR, Franke L, Frayling TM, McCarthy MI, Visscher PM, Scherag A, Willer CJ, Boehnke M, Mohlke KL, Lindgren CM, Beckmann JS, Barroso I, North KE, Ingelsson E, Hirschhorn JN, Loos RJ, Speliotes EK (2015) Genetic studies of body mass index yield new insights for obesity biology. Nature 518:197–206PubMedPubMedCentralCrossRefGoogle Scholar
  67. Lucas LR, Celen Z, Tamashiro KL, Blanchard RJ, Blanchard DC, Markham C, Sakai RR, McEwen BS (2004) Repeated exposure to social stress has long-term effects on indirect markers of dopaminergic activity in brain regions associated with motivated behavior. Neuroscience 124:449–457PubMedCrossRefGoogle Scholar
  68. Makino S, Smith MA, Gold PW (1995) Increased expression of corticotropin-releasing hormone and vasopressin messenger ribonucleic acid (mRNA) in the hypothalamic paraventricular nucleus during repeated stress: association with reduction in glucocorticoid receptor mRNA levels. Endocrinology 136:3299–3309PubMedGoogle Scholar
  69. Marmot M (2006) Health in an unequal world: social circumstances, biology and disease. Clin Med 6:559–572CrossRefGoogle Scholar
  70. Marti O, Marti J, Armario A (1994) Effects of chronic stress on food intake in rats: influence of stressor intensity and duration of daily exposure. Physiol Behav 55:747–753PubMedCrossRefGoogle Scholar
  71. McEwen BS (1998) Stress, adaptation, and disease. Allostasis and allostatic load. Ann NY Acad Sci 840:33–44PubMedCrossRefGoogle Scholar
  72. McNeilly AD, Stewart CA, Sutherland C, Balfour DJ (2015) High fat feeding is associated with stimulation of the hypothalamic-pituitary-adrenal axis and reduced anxiety in the rat. Psychoneuroendocrinology 52:272–280PubMedCrossRefGoogle Scholar
  73. Michopoulos V, Wilson ME (2011) Body weight decreases induced by estradiol in female rhesus monkeys are dependent upon social status. Physiol Behav 102:382–388PubMedPubMedCentralCrossRefGoogle Scholar
  74. Michopoulos V, Berga SL, Kaplan JR, Wilson ME (2009) Social subordination and polymorphisms in the gene encoding the serotonin transporter enhance estradiol inhibition of luteinizing hormone secretion in female rhesus monkeys. Biol Reprod 81:1154–1163PubMedPubMedCentralCrossRefGoogle Scholar
  75. Michopoulos V, Loucks T, Berga SL, Rivier J, Wilson ME (2010) Increased ghrelin sensitivity and calorie consumption in subordinate monkeys is affected by short-term astressin B administration. Endocrine 38:227–234PubMedPubMedCentralCrossRefGoogle Scholar
  76. Michopoulos V, Higgins M, Toufexis D, Wilson ME (2012a) Social subordination produces distinct stress-related phenotypes in female rhesus monkeys. Psychoneuroendocrinology 37:1071–1085PubMedPubMedCentralCrossRefGoogle Scholar
  77. Michopoulos V, Reding KM, Wilson ME, Toufexis D (2012b) Social subordination impairs hypothalamic-pituitary-adrenal function in female rhesus monkeys. Horm Behav 62:389–399PubMedPubMedCentralCrossRefGoogle Scholar
  78. Michopoulos V, Toufexis D, Wilson ME (2012c) Social stress interacts with diet history to promote emotional feeding in females. Psychoneuroendocrinology 37:1479–1490PubMedPubMedCentralCrossRefGoogle Scholar
  79. Michopoulos V, Perez Diaz M, Moore CJ, Johnson Z, Sanchez M, Toufexis D, Wilson ME (2014) The effects of CRFR1 antagonism on food intake, behavior, and dopamine 2 receptor binding potential in socially subordinate rhesus monkeys. Society for Biological Psychiatry, New York, NYGoogle Scholar
  80. Moore CJ, Lowe J, Michopoulos V, Ulam P, Toufexis D, Wilson ME, Johnson Z (2013) Small changes in meal patterns lead to significant changes in total caloric intake. Effects of diet and social status on food intake in female rhesus monkeys. Appetite 62:60–69PubMedCrossRefGoogle Scholar
  81. Moore CJ, Johnson ZP, Higgins M, Toufexis D, Wilson ME (2015) Antagonism of corticotrophin-releasing factor type 1 receptors attenuates caloric intake of free feeding subordinate female rhesus monkeys in a rich dietary environment. J Neuroendocrinol 27:33–43PubMedPubMedCentralCrossRefGoogle Scholar
  82. Morgan D, Grant KA, Gage HD, Mach RH, Kaplan JR, Prioleau O, Nader SH, Buchheimer N, Ehrenkaufer RL, Nader MA (2002) Social dominance in monkeys: dopamine D2 receptors and cocaine self-administration. Nat Neurosci 5:169–174PubMedCrossRefGoogle Scholar
  83. O’Rahilly S, Farooqi IS (2000) The genetics of obesity in humans. Endotext.org South Dartmouth (MA): MDText.comGoogle Scholar
  84. Paiardini M, Hoffman J, Cervasi B, Ortiz AM, Stroud F, Silvestri G, Wilson ME (2009) T-cell phenotypic and functional changes associated with social subordination and gene polymorphisms in the serotonin reuptake transporter in female rhesus monkeys. Brain Behav Immun 23:286–293PubMedPubMedCentralCrossRefGoogle Scholar
  85. Pasquali R, Ambrosi B, Armanini D, Cavagnini F, Uberti ED, Del Rio G, de Pergola G, Maccario M, Mantero F, Marugo M, Rotella CM, Vettor R (2002) Cortisol and ACTH response to oral dexamethasone in obesity and effects of sex, body fat distribution, and dexamethasone concentrations: a dose-response study. J Clin Endocrinol Metab 87:166–175PubMedCrossRefGoogle Scholar
  86. Paulmyer-Lacroix O, Hery M, Pugeat M, Grino M (1996) The modulatory role of estrogens on corticotropin-releasing factor gene expression in the hypothalamic paraventricular nucleus of ovariectomized rats: role of the adrenal gland. J Neuroendocrinol 8:515–519PubMedCrossRefGoogle Scholar
  87. 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 145:3754–3762PubMedCrossRefGoogle Scholar
  88. Power ML, Schulkin J (2008) Sex differences in fat storage, fat metabolism, and the health risks from obesity: possible evolutionary origins. Br J Nutr 99:931–940PubMedCrossRefGoogle Scholar
  89. Raison CL, Miller AH (2003) When not enough is too much: the role of insufficient glucocorticoid signaling in the pathophysiology of stress-related disorders. Am J Psychiatry 160:1554–1565PubMedCrossRefGoogle Scholar
  90. Riddick NV, Czoty PW, Gage HD, Kaplan JR, Nader SH, Icenhower M, Pierre PJ, Bennett A, Garg PK, Garg S, Nader MA (2009) Behavioral and neurobiological characteristics influencing social hierarchy formation in female cynomolgus monkeys. Neuroscience 158:1257–1265PubMedPubMedCentralCrossRefGoogle Scholar
  91. Rilke O, May T, Oehler J, Wolffgramm J (1995) Influences of housing conditions and ethanol intake on binding characteristics of D2, 5-HT1A, and benzodiazepine receptors of rats. Pharmacol Biochem Behav 52:23–28PubMedCrossRefGoogle Scholar
  92. Rosmond R (2004) Obesity and depression: same disease, different names? Med Hypotheses 62:976–979PubMedCrossRefGoogle Scholar
  93. Rosmond R, Dallman MF, Bjorntorp P (1998) Stress-related cortisol secretion in men: relationships with abdominal obesity and endocrine, metabolic and hemodynamic abnormalities. J Clin Endocrinol Metab 83:1853–1859PubMedGoogle Scholar
  94. Sapolsky RM (2005) The influence of social hierarchy on primate health. Science 308:648–652Google Scholar
  95. Schulkin J, Gold PW, McEwen BS (1998) Induction of corticotropin-releasing hormone gene expression by glucocorticoids: implication for understanding the states of fear and anxiety and allostatic load. Psychoneuroendocrinology 23:219–243PubMedCrossRefGoogle Scholar
  96. Scott KM, McGee MA, Wells JE, Oakley Browne MA (2008) Obesity and mental disorders in the adult general population. J Psychosom Res 64:97–105PubMedCrossRefGoogle Scholar
  97. Shively CA (1998) Social subordination stress, behavior, and central monoaminergic function in female cynomolgus monkeys. Biol Psychiatry 44:882–891PubMedCrossRefGoogle Scholar
  98. Shively C, Kaplan J (1984) Effects of social factors on adrenal weight and related physiology of Macaca fascicularis. Physiol Behav 33:777–782PubMedCrossRefGoogle Scholar
  99. Shively CA, Laber-Laird K, Anton RF (1997) Behavior and physiology of social stress and depression in female cynomolgus monkeys. Biol Psychiatry 41:871–882PubMedCrossRefGoogle Scholar
  100. Shively CA, Register TC, Clarkson TB (2009) Social stress, visceral obesity, and coronary artery atherosclerosis in female primates. Obesity (Silver Spring) 17:1513–1520CrossRefGoogle Scholar
  101. Shungin D, Winkler TW, Croteau-Chonka DC, Ferreira T, Locke AE, Magi R, Strawbridge RJ, Pers TH, Fischer K, Justice AE, Workalemahu T, Wu JM, Buchkovich ML, Heard-Costa NL, Roman TS, Drong AW, Song C, Gustafsson S, Day FR, Esko T, Fall T, Kutalik Z, Luan J, Randall JC, Scherag A, Vedantam S, Wood AR, Chen J, Fehrmann R, Karjalainen J, Kahali B, Liu CT, Schmidt EM, Absher D, Amin N, Anderson D, Beekman M, Bragg-Gresham JL, Buyske S, Demirkan A, Ehret GB, Feitosa MF, Goel A, Jackson AU, Johnson T, Kleber ME, Kristiansson K, Mangino M, Mateo Leach I, Medina-Gomez C, Palmer CD, Pasko D, Pechlivanis S, Peters MJ, Prokopenko I, Stancakova A, Ju Sung Y, Tanaka T, Teumer A, Van Vliet-Ostaptchouk JV, Yengo L, Zhang W, Albrecht E, Arnlov J, Arscott GM, Bandinelli S, Barrett A, Bellis C, Bennett AJ, Berne C, Bluher M, Bohringer S, Bonnet F, Bottcher Y, Bruinenberg M, Carba DB, Caspersen IH, Clarke R, Daw EW, Deelen J, Deelman E, Delgado G, Doney AS, Eklund N, Erdos MR, Estrada K, Eury E, Friedrich N, Garcia ME, Giedraitis V, Gigante B, Go AS, Golay A, Grallert H, Grammer TB, Grassler J, Grewal J, Groves CJ, Haller T, Hallmans G, Hartman CA, Hassinen M, Hayward C, Heikkila K, Herzig KH, Helmer Q, Hillege HL, Holmen O, Hunt SC, Isaacs A, Ittermann T, James AL, Johansson I, Juliusdottir T, Kalafati IP, Kinnunen L, Koenig W, Kooner IK, Kratzer W, Lamina C, Leander K, Lee NR, Lichtner P, Lind L, Lindstrom J, Lobbens S, Lorentzon M, Mach F, Magnusson PK, Mahajan A, McArdle WL, Menni C, Merger S, Mihailov E, Milani L, Mills R, Moayyeri A, Monda KL, Mooijaart SP, Muhleisen TW, Mulas A, Muller G, Muller-Nurasyid M, Nagaraja R, Nalls MA, Narisu N, Glorioso N, Nolte IM, Olden M, Rayner NW, Renstrom F, Ried JS, Robertson NR, Rose LM, Sanna S, Scharnagl H, Scholtens S, Sennblad B, Seufferlein T, Sitlani CM, Vernon Smith A, Stirrups K, Stringham HM, Sundstrom J, Swertz MA, Swift AJ, Syvanen AC, Tayo BO, Thorand B, Thorleifsson G, Tomaschitz A, Troffa C, van Oort FV, Verweij N, Vonk JM, Waite LL, Wennauer R, Wilsgaard T, Wojczynski MK, Wong A, Zhang Q, Hua Zhao J, Brennan EP, Choi M, Eriksson P, Folkersen L, Franco-Cereceda A, Gharavi AG, Hedman AK, Hivert MF, Huang J, Kanoni S, Karpe F, Keildson S, Kiryluk K, Liang L, Lifton RP, Ma B, McKnight AJ, McPherson R, Metspalu A, Min JL, Moffatt MF, Montgomery GW, Murabito JM, Nicholson G, Nyholt DR, Olsson C, Perry JR, Reinmaa E, Salem RM, Sandholm N, Schadt EE, Scott RA, Stolk L, Vallejo EE, Westra HJ, Zondervan KT, Amouyel P, Arveiler D, Bakker SJ, Beilby J, Bergman RN, Blangero J, Brown MJ, Burnier M, Campbell H, Chakravarti A, Chines PS, Claudi-Boehm S, Collins FS, Crawford DC, Danesh J, de Faire U, de Geus EJ, Dorr M, Erbel R, Eriksson JG, Farrall M, Ferrannini E, Ferrieres J, Forouhi NG, Forrester T, Franco OH, Gansevoort RT, Gieger C, Gudnason V, Haiman CA, Harris TB, Hattersley AT, Heliovaara M, Hicks AA, Hingorani AD, Hoffmann W, Hofman A, Homuth G, Humphries SE, Hypponen E, Illig T, Jarvelin MR, Johansen B, Jousilahti P, Jula AM, Kaprio J, Kee F, Keinanen-Kiukaanniemi SM, Kooner JS, Kooperberg C, Kovacs P, Kraja AT, Kumari M, Kuulasmaa K, Kuusisto J, Lakka TA, Langenberg C, Le Marchand L, Lehtimaki T, Lyssenko V, Mannisto S, Marette A, Matise TC, McKenzie CA, McKnight B, Musk AW, Mohlenkamp S, Morris AD, Nelis M, Ohlsson C, Oldehinkel AJ, Ong KK, Palmer LJ, Penninx BW, Peters A, Pramstaller PP, Raitakari OT, Rankinen T, Rao DC, Rice TK, Ridker PM, Ritchie MD, Rudan I, Salomaa V, Samani NJ, Saramies J, Sarzynski MA, Schwarz PE, Shuldiner AR, Staessen JA, Steinthorsdottir V, Stolk RP, Strauch K, Tonjes A, Tremblay A, Tremoli E, Vohl MC, Volker U, Vollenweider P, Wilson JF, Witteman JC, Adair LS, Bochud M, Boehm BO, Bornstein SR, Bouchard C, Cauchi S, Caulfield MJ, Chambers JC, Chasman DI, Cooper RS, Dedoussis G, Ferrucci L, Froguel P, Grabe HJ, Hamsten A, Hui J, Hveem K, Jockel KH, Kivimaki M, Kuh D, Laakso M, Liu Y, Marz W, Munroe PB, Njolstad I, Oostra BA, Palmer CN, Pedersen NL, Perola M, Perusse L, Peters U, Power C, Quertermous T, Rauramaa R, Rivadeneira F, Saaristo TE, Saleheen D, Sinisalo J, Slagboom PE, Snieder H, Spector TD, Thorsteinsdottir U, Stumvoll M, Tuomilehto J, Uitterlinden AG, Uusitupa M, van der Harst P, Veronesi G, Walker M, Wareham NJ, Watkins H, Wichmann HE, Abecasis GR, Assimes TL, Berndt SI, Boehnke M, Borecki IB, Deloukas P, Franke L, Frayling TM, Groop LC, Hunter DJ, Kaplan RC, O’Connell JR, Qi L, Schlessinger D, Strachan DP, Stefansson K, van Duijn CM, Willer CJ, Visscher PM, Yang J, Hirschhorn JN, Zillikens MC, McCarthy MI, Speliotes EK, North KE, Fox CS, Barroso I, Franks PW, Ingelsson E, Heid IM, Loos RJ, Cupples LA, Morris AP, Lindgren CM, Mohlke KL (2015) New genetic loci link adipose and insulin biology to body fat distribution. Nature 518:187–196PubMedPubMedCentralCrossRefGoogle Scholar
  102. Simon GE, Arterburn DE (2009) Does comorbid psychiatric disorder argue for or against surgical treatment of obesity? Gen Hosp Psychiatry 31:401–402PubMedPubMedCentralCrossRefGoogle Scholar
  103. Smagin GN, Howell LA, Redmann S Jr, Ryan DH, Harris RB (1999) Prevention of stress-induced weight loss by third ventricle CRF receptor antagonist. Am J Physiol 276:R1461–R1468PubMedGoogle Scholar
  104. Stice E, Spoor S, Bohon C, Small DM (2008) Relation between obesity and blunted striatal response to food is moderated by TaqIA A1 allele. Science 322:449–452Google Scholar
  105. Strack AM, Akana SF, Horsley CJ, Dallman MF (1997) A hypercaloric load induces thermogenesis but inhibits stress responses in the SNS and HPA system. Am J Physiol 272:R840–R848PubMedGoogle Scholar
  106. Sullivan EL, Grove KL (2010) Metabolic imprinting in obesity. Forum Nutr 63:186–194PubMedPubMedCentralCrossRefGoogle Scholar
  107. Tannenbaum BM, Brindley DN, Tannenbaum GS, Dallman MF, McArthur MD, Meaney MJ (1997) High-fat feeding alters both basal and stress-induced hypothalamic-pituitary-adrenal activity in the rat. Am J Physiol 273:E1168–R1177PubMedGoogle Scholar
  108. Tomiyama AJ, Dallman MF, Epel ES (2011) Comfort food is comforting to those most stressed: evidence of the chronic stress response network in high stress women. Psychoneuroendocrinology 36:1513–1519Google Scholar
  109. Vicennati V, Pasquali R (2000) Abnormalities of the hypothalamic-pituitary-adrenal axis in nondepressed women with abdominal obesity and relations with insulin resistance: evidence for a central and a peripheral alteration. J Clin Endocrinol Metab 85:4093–4098PubMedCrossRefGoogle Scholar
  110. Volkow ND, Fowler JS, Wang GJ (2003) The addicted human brain: insights from imaging studies. J Clin Investig 111:1444–1451PubMedPubMedCentralCrossRefGoogle Scholar
  111. Volkow ND, Wang GJ, Fowler JS, Tomasi D (2012) Addiction circuitry in the human brain. Annu Rev Pharmacol Toxicol 52:321–336PubMedPubMedCentralCrossRefGoogle Scholar
  112. Walker BR, Soderberg S, Lindahl B, Olsson T (2000) Independent effects of obesity and cortisol in predicting cardiovascular risk factors in men and women. J Intern Med 247:198–204PubMedCrossRefGoogle Scholar
  113. Wang GJ, Volkow ND, Thanos PK, Fowler JS (2004) Similarity between obesity and drug addiction as assessed by neurofunctional imaging: a concept review. J Addict Dis 23:39–53PubMedCrossRefGoogle Scholar
  114. Warrington NM, Howe LD, Paternoster L, Kaakinen M, Herrala S, Huikari V, Wu YY, Kemp JP, Timpson NJ, Pourcain BS, Davey Smith G, Tilling K, Jarvelin MR, Pennell CE, Evans DM, Lawlor DA, Briollais L, Palmer LJ (2015) A genome-wide association study of body mass index across early life and childhood. Int J Epidemiol 44:700–712Google Scholar
  115. Weissman MM, Olfson M (1995) Depression in women: implications for health care research. Science 269:799–801Google Scholar
  116. Werrij MQ, Mulkens S, Hospers HJ, Jansen A (2006) Overweight and obesity: the significance of a depressed mood. Patient Educ Couns 62:126–131PubMedCrossRefGoogle Scholar
  117. Wilson ME, Pazol K, Legendre A, Fisher J, Chikazawa K (2005) Gonadal steroid modulation of the limbic–hypothalamic–pituitary–adrenal (LHPA) axis is influenced by social status in female rhesus monkeys. Endocrine 26:89–97Google Scholar
  118. Wilson ME, Fisher J, Fischer A, Lee V, Harris RB, Bartness TJ (2008) Quantifying food intake in socially housed monkeys: social status effects on caloric consumption. Physiol Behav 94:586–594PubMedPubMedCentralCrossRefGoogle Scholar
  119. Wurtman JJ (1993) Depression and weight gain: the serotonin connection. J Affect Disord 29:183–192PubMedCrossRefGoogle Scholar
  120. Wurtman RJ, Wurtman JJ (1995) Brain serotonin, carbohydrate-craving, obesity and depression. Obes Res 3(Suppl 4):477S–480SPubMedCrossRefGoogle Scholar
  121. Zellner DA, Loaiza S, Gonzalez Z, Pita J, Morales J, Pecora D, Wolf A (2006) Food selection changes under stress. Physiol Behav 87:789–793PubMedCrossRefGoogle Scholar
  122. Zellner DA, Saito S, Gonzalez J (2007) The effect of stress on men’s food selection. Appetite 49:696–699PubMedCrossRefGoogle Scholar
  123. Zhang D, Li Z, Wang H, Yang M, Liang L, Fu J, Wang C, Ling J, Zhang Y, Zhang S, Xu Y, Zhu Y, Lai M (2015) Interactions between obesity-related copy number variants and dietary behaviors in childhood obesity. Nutrients 7:3054–3066PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of Psychiatry and Behavioral SciencesEmory University School of Medicine, Yerkes National Primate Research CenterAtlantaUSA

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