Abstract
One proposed contributor to the recent surge in obesity prevalence is the increased availability of highly palatable foods coupled with the drive to consume these foods under stressful conditions. Studies of humans suggest that stress exposure promotes increased caloric intake and a preference for energy-dense foods, and this may be particularly true for women, as they more often show higher rates of obesity and report a higher incidence of emotional feeding relative to men. Socially housed female rhesus macaques provide a unique, ethologically relevant model for studying the effects of psychosocial stress on appetite within varying dietary environments. Macaque groups, regardless of size, are organized by a matrilineal dominance hierarchy that functions to maintain group stability. Lower ranking animals receive more aggression from higher ranking group mates and terminate these interactions by emitting submissive behavior. Subordinates have less control over their environment, and continual harassment from dominant animals results in dysregulation of the limbic–hypothalamic–pituitary–adrenal (LHPA) axis. Metabolic and anthropometric phenotypes differ between dominant and subordinate monkeys when maintained on a standard low-fat, high-fiber laboratory diet, as dominant females are more often heavier with greater fat and bone mass. Recent studies, using validated automated feeders, suggest that under conditions of a low-caloric density diet (LCD), subordinate monkeys consume similar calories but are more active during the daytime relative to dominant monkeys. However, once a highly palatable, high-caloric density diet that is high in fat and sugar (HFSD) is added to the LCD environment, subordinate females become significantly hyperphagic and exhibit significant increases in fat mass within a 2-week period. These studies also suggest a significant effect of diet history whereby subordinate animals previously exposed to the HFSD continue to be hyperphagic when returned to a LCD-only condition. Future studies are warranted to explore the long-term effects of psychosocial stress on appetite within a rich dietary environment analogous to that of humans.
Key words
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
World Health Organization (2010) Vital signs: state-specific obesity prevalence among adults United States, 2009. MMWR Morb Mortal Wkly Rep 59:951–955
Flegal KM (2005) Epidemiologic aspects of overweight and obesity in the United States. Physiol Behav 86:599–602
Epel E et al (2001) Stress may add bite to appetite in women: a laboratory study of stress-induced cortisol and eating behavior. Psychoneuroendocrinology 26:37–49
Gibson EL (2006) Emotional influences on food choice: sensory, physiological, and psychological pathways. Physiol Behav 83:53–61
Oliver G, Wardle J, Gibson EL (2000) Stress and food choice: a laboratory study. Psychosom Med 62:853–865
Adam TC, Epel ES (2007) Stress, eating and the reward system. Physiol Behav 91:449–458
Kassirer JP, Angell M (1998) Losing weight–an ill-fated New Year’s resolution. N Engl J Med 338:52–54
Hays NP, Roberts SB (2008) Aspects of eating behaviors “disinhibition” and “restraint” are related to weight gain and BMI in women. Obesity (Silver Spring) 16:52–58
Simon GE, Arterburn DE (2009) Does comorbid psychiatric disorder argue for or against surgical treatment of obesity? Gen Hosp Psychiatry 31:401–402
Werrij MQ et al (2006) Overweight and obesity: the significance of a depressed mood. Patient Educ Couns 62:126–131
McEwen BS (2002) Sex, stress and the hippocampus: allostasis, allostatic load and the aging process. Neurobiol Aging 23:921–939
Chrousos GP (2009) Stress and disorders of the stress system. Nat Rev Endocrinol 5:374–381
Juster RP, McEwen BS, Lupien SJ (2010) Allostatic load biomarkers of chronic stress and impact on health and cognition. Neurosci Biobehav Rev 35:2–16
McEwen BS (2008) Central effects of stress hormones in health and disease: understanding the protective and damaging effects of stress and stress mediators. Eur J Pharmacol 583:174–185
Hill JO (2006) Understanding and addressing the epidemic of obesity: an energy balance perspective. Endocr Rev 27:750–761
Withrow D, Alter DA (2010) The economic burden of obesity worldwide: a systematic review of the direct costs of obesity. Obes Rev 12:131–141
Choi DC et al (2008) The role of the posterior medial bed nucleus of the stria terminalis in modulating hypothalamic-pituitary-adrenocortical axis responsiveness to acute and chronic stress. Psychoneuroendocrinology 33:659–669
Herman JP et al (2003) Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Front Neuroendocrinol 24:151–180
Jankord R, Herman JP (2008) Limbic regulation of hypothalamo-pituitary-adrenocortical function during acute and chronic stress. Ann NY Acad Sci 1148:64–73
Ulrich-Lai YM, Herman JP (2009) Neural regulation of endocrine and autonomic stress responses. Nat Rev Neurosci 10:397–409
Bjorntorp P (2001) Do stress reactions cause abdominal obesity and comorbidities? Obes Rev 2:73–86
Dallman MF, Pecoraro NC, la Fleur SE (2005) Chronic stress and comfort foods: self-medication and abdominal obesity. Brain Behav Immun 19:275–280
Rosmond R (2004) Obesity and depression: same disease, different names? Med Hypotheses 62:976–979
Scott KM et al (2008) Obesity and mental disorders in the adult general population. J Psychosom Res 64:97–105
Armario A (2006) The hypothalamic-pituitary-adrenal axis: what can it tell us about stressors? CNS Neurol Disord Drug Targets 5:485–501
Bhatnagar S, Dallman M (1998) Neuroanatomical basis for facilitation of hypothalamic-pituitary-adrenal responses to a novel stressor after chronic stress. Neuroscience 84:1025–1039
Bhatnagar S et al (1998) The effects of prior chronic stress on cardiovascular responses to acute restraint and formalin injection. Brain Res 797:313–320
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 43:158–165
Bhatnagar S et al (2006) Changes in hypothalamic-pituitary-adrenal function, body temperature, body weight and food intake with repeated social stress exposure in rats. J Neuroendocrinol 18:13–24
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 147:4917–4930
Anisman H, Matheson K (2005) Stress, depression, and anhedonia: caveats concerning animal models. NeurosciBiobehav Rev 29:525–546
Huhman KL (2006) Social conflict models: can they inform us about human psychopathology? Horm Behav 50:640–646
Tamashiro KL, Nguyen MM, Sakai RR (2005) Social stress: from rodents to primates. Front Neuroendocrinol 26:27–40
Zellner DA et al (2006) Food selection changes under stress. Physiol Behav 87:789–793
Zellner DA, Saito S, Gonzalez J (2007) The effect of stress on men’s food selection. Appetite 49:696–699
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 18:458–466
Jones LE, Carney CP (2006) Increased risk for metabolic syndrome in persons seeking care for mental disorders. Ann Clin Psychiatry 18:149–155
Weissman MM, Olfson M (1995) Depression in women: implications for health care research. Science 269:799–801
Wurtman JJ (1993) Depression and weight gain: the serotonin connection. J Affect Disord 29:183–192
Wurtman RJ, Wurtman JJ (1995) Brain serotonin, carbohydrate-craving, obesity and depression. Obes Res 3(Suppl 4):477S–480S
Bernstein IS, Gordon TP (1974) The function of aggression in primate societies. Am Sci 62:304–311
Bernstein IS (1976) Dominance, aggression and reproduction in primate societies. J Theor Biol 60:459–472
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) 21:81–107
Shively C, Kaplan J (1984) Effects of social factors on adrenal weight and related physiology of Macaca fascicularis. Physiol Behav 33:777–782
Arce M et al (2010) Diet choice, cortisol reactivity, and emotional feeding in socially housed rhesus monkeys. Physiol Behav 101:446–455
Collura LA, Hoffman JB, Wilson ME (2009) Administration of human leptin differentially affects parameters of cortisol secretion in socially housed female rhesus monkeys. Endocrine 36:530–537
Jarrell H et al (2008) Polymorphisms in the serotonin reuptake transporter gene modify the consequences of social status on metabolic health in female rhesus monkeys. Physiol Behav 93:807–819
Kaplan JR et al (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. Hum Reprod 25:3083–3094
Riddick NV et al (2009) Behavioral and neurobiological characteristics influencing social hierarchy formation in female cynomolgus monkeys. Neuroscience 158:1257–1265
Shively CA (1998) Social subordination stress, behavior, and central monoaminergic function in female cynomolgus monkeys. Biol Psychiatry 44:882–891
Shively CA, Laber-Laird K, Anton RF (1997) Behavior and physiology of social stress and depression in female cynomolgus monkeys. Biol Psychiatry 41:871–882
Stavisky RC et al (2001) Dominance, cortisol, and behavior in small groups of female cynomolgus monkeys (Macaca fascicularis). Horm Behav 39:232–238
Michopoulos V et al (2012) Social subordination produces distinct stress-related phenotypes in female rhesus monkeys. Psychoneuroendocrinology 37:1071–1085
Bernstein IS (1970) Primate status hierarchies. In: Rosenblum LA (ed) Primate behavior: developments in field and laboratory research. Academic, New York, pp 71–109
Kaplan JR et al (1984) Psychosocial influences on female ‘protection’ among cynomolgus macaques. Atherosclerosis 53:283–295
Michopoulos V, Toufexis D, Wilson ME (2011) Social stress promotes emotional feeding and interacts with diet to shape appetite in females. Psychoneuroendocrinology 2012 Feb 27 Epub
Adams MR, Kaplan JR, Koritnik DR (1985) Psychosocial influences on ovarian endocrine and ovulatory function in Macaca fascicularis. Physiol Behav 35:935–940
Cohen S (1999) Social status and susceptibility to respiratory infections. Ann NY Acad Sci 896:246–253
Gust DA et al (1991) Formation of a new social group of unfamiliar female rhesus monkeys affects the immune and pituitary adrenocortical systems. Brain Behav Immun 5:296–307
Kaplan JR et al (1996) Psychosocial factors, sex differences, and atherosclerosis: lessons from animal models. Psychosom Med 58:598–611
Morgan D et al (2002) Social dominance in monkeys: dopamine D2 receptors and cocaine self-administration. Nat Neurosci 5:169–174
Paiardini M (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 23:286–293
Sapolsky RM (2005) The influence of social hierarchy on primate health. Science 308:648–652
Wilson ME et al (2008) Quantifying food intake in socially housed monkeys: social status effects on caloric consumption. Physiol Behav 94:586–594
Marti O, Marti J, Armario A (1994) Effects of chronic stress on food intake in rats: influence of s stressor intensity and duration of daily exposure. Physiol Behav 55:747–753
Smagin GN et al (1999) Prevention of stress-induced weight loss by third ventricle CRF receptor antagonist. Am J Physiol 276:R1461–1468
Gamaro GD et al (2003) Effects of chronic variate stress on feeding behavior and on monoamine levels in different rat brain structures. Neurochem Int 42:107–114
Jochman KA et al (2005) Corticotropin-releasing factor-1 receptors in the basolateral amygdala mediate stress-induced anorexia. Behav Neurosci 119:1448–1458
Dallman M, Bhatnagar S (2001) Chronic stress and energy balance:Role of the HPA axis. In: Epel E et al (eds) Are stress eaters at risk for the metabolic syndrome? Ann NY Acad Sci 1032:208–210
Houshyar H, Manalo S, Dallman MF (2004) Time-dependent alterations in mRNA expression of brain neuropeptides regulating energy balance and hypothalamo-pituitary-adrenal activity after withdrawal from intermittent morphine treatment. J Neurosci 24:9414–9424
Heinrichs SC, Richard D (1999) The role of corticotropin-releasing factor and urocortin in the modulation of ingestive behavior. Neuropeptides 33:350–359
Hotta M et al (1999) Corticotropin-releasing factor receptor type 1 mediates emotional stress induced inhibition of food intake and behavioral changes in rats. Brain Res 823:221–225
Krahn DD et al (1988) Behavioral effects of corticotropin-releasing factor: localization and characterization of central effects. Brain Res 443:63–69
Richard D, Lin Q, Timofeeva E (2002) The corticotropin-releasing factor family of peptides and CRF receptors: their roles in the regulation of energy balance. Eur J Pharmacol 440:189–197
Sullivan EL et al (2006) Individual differences in physical activity are closely associated with changes in body weight in adult female rhesus monkeys (Macaca mulatta). Am J Physiol Regul Integr Comp Physiol 291:R633–642
Michopoulos V, Wilson ME (2011) Body weight decreases induced by estradiol in female rhesus monkeys are dependent upon social status. Physiol Behav 102:382–388
Foster MT et al (2008) Palatable foods, stress, and energy stores sculpt corticotropin-releasing factor, adrenocorticotropin and corticosterone concentrations after restraint. Endocrinology 150:2325–2333
Pecoraro N et al (2004) Stress promotes palatable feeding, which reduces signs of stress: feedforward and feedback effects of chronic stress. Endocrinology 145:3754–3762
Tamashiro KL, Hegeman MA, Sakai RR (2006) Chronic social stress in a changing dietary environment. Physiol Behav 89:536–542
Moyer AE et al (1994) Stress-induced cortisol response and fat distribution in women. Obes Res 2:255–262
Zakrzewska KE et al (1997) Glucocorticoids as counterregulatory hormones of leptin: toward an understanding of leptin resistance. Diabetes 46:717–719
Andrews RC, Walker BR (1999) Glucocorticoids and insulin resistance: old hormones, new targets. Clin Sci (Lond) 96:513–523
Leal-Cerro A et al (2001) Influence of cortisol status on leptin secretion. Pituitary 4:111–116
Fu JH et al (2009) The combination of a high-fat diet and chronic stress aggravates insulin resistance in Wistar male rats. Exp Clin Endocrinol Diabetes 117:354–360
Caspi A et al (2003) Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 301:386–389
Stice E et al (2008) Relation between obesity and blunted striatal response to food is moderated by TaqIA A1 allele. Science 322:449–452
Bennett AJ et al (2002) Early experience and serotonin transporter gene variation interact to influence primate CNS function. Mol Psychiatry 7:118–122
Champoux M et al (2002) Serotonin transporter gene polymorphism, differential early rearing, and behavior in rhesus monkey neonates. Mol Psychiatry 7:1058–1063
Suomi SJ (2006) Risk, resilience, and gene × environment interactions in rhesus monkeys. Ann NY Acad Sci 1094:52–62
Bagot RC, Meaney MJ (2010) Epigenetics and the biological basis of gene × environment interactions. J Am Acad Child Adolesc Psychiatry 49:752–771
Michopoulos V et al (2010) Increased ghrelin sensitivity and calorie consumption in subordinate monkeys is affected by short-term astressin B administration. Endocine 38:227–234
Buwalda B et al (2001) Behavioral and physiological responses to stress are affected by high-fat feeding in male rats. Physiol Behav 73:371–377
Strack AM et al (1997) A hypercaloric load induces thermogenesis but inhibits stress responses in the SNS and HPA system. Am J Physiol 272:R840–848
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 36:1513–1519
Bell ME et al (2000) Voluntary sucrose ingestion, like corticosterone replacement, prevents the metabolic deficits of adrenalectomy. J Neuroendocrinol 12:461–470
Bhatnagar S et al (2000) Corticosterone facilitates saccharin intake in adrenalectomized rats: does corticosterone increase stimulus salience? J Neuroendocrinol 12:453–460
la Fleur SE et al (2004) Interaction between corticosterone and insulin in obesity: regulation of lard intake and fat stores. Endocrinology 145:2174–2185
Kitraki E, Soulis G, Gerozissis K (2004) Impaired neuroendocrine response to stress following a short-term fat-enriched diet. Neuroendocrinology 79:338–345
Legendre A, Harris RB (2006) Exaggerated response to mild stress in rats fed high-fat diet. Am J Physiol Regul Integr Comp Physiol 291:R1288–1294
Legendre A et al (2007) Differences in response to corticotropin-releasing factor after short- and long-term consumption of a high-fat diet. Am J Physiol 293:R1076–1085
Soulis G, Kitraki E, Gerozissis K (2005) Early neuroendocrine alterations in female rats following a diet moderately enriched in fat. Cell Mol Neurobiol 25:869–880
Tannenbaum BM et al (1997) High-fat feeding alters both basal and stress-induced hypothalamic-pituitary-adrenal activity in the rat. Am J Physiol 273:E1168–1177
Pasquali R et al (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 87:166–175
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 83:1853–1859
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 85:4093–4098
Alsio J et al (2009) Inverse association of high-fat diet preference and anxiety-like behavior: a putative role for urocortin 2. Genes Brain Behav 8:193–202
Teegarden SL, Bale TL (2007) Decreases in dietary preference produce increased emotionality and risk for dietary relapse. Biol Psychiatry 61:1021–1029
Volkow ND, Fowler JS, Wang GJ (2003) The addicted human brain: insights from imaging studies. J Clin Invest 111:1444–1451
Kalivas PW, Duffy P (1989) Similar effects of daily cocaine and stress on mesocorticolimbic dopamine neurotransmission in the rat. Biol Psychiatry 25:913–928
Izzo E, Sanna PP, Koob GF (2005) Impairment of dopaminergic system function after chronic treatment with corticotropin-releasing factor. Pharmacol Biochem Behav 81:701–708
Koob GF (2000) Neurobiology of addiction. Toward the development of new therapies. Ann NY Acad Sci 909:170–185
Lucas LR et al (2006) Excitability of dopamine neurons: modulation and physiological consequences. CNS Neurol Disord Drug Targets 5:79–97
Johnson PM, Kenny PJ (2010) Dopamine D2 receptors in addiction-like reward dysfunction and compulsive eating in obese rats. Nat Neurosci 13:635–641
Wang GJ et al (2004) Similarity between obesity and drug addiction as assessed by neurofunctional imaging: a concept review. J Addict Dis 23:39–53
Bassareo V, Di Chiara G (1999) Differential responsiveness of dopamine transmission to food-stimuli in nucleus accumbens shell/core compartments. Neuroscience 89:637–641
Blackburn JR et al (1986) Increased dopamine metabolism in the nucleus accumbens and striatum following consumption of a nutritive meal but not a palatable non-nutritive saccharin solution. Pharmacol Biochem Behav 25:1095–1100
Small DM, Jones-Gotman M, Dagher A (2003) Feeding-induced dopamine release in dorsal striatum correlates with meal pleasantness ratings in healthy human volunteers. NeuroImage 19:1709–1715
Grant KA et al (1998) Effect of social status on striatal dopamine D2 receptor binding characteristics in cynomolgus monkeys assessed with positron emission tomography. Synapse 29:80–83
Acknowledgments
We would like to thank Jennifer Whitley, Shannon Bounar, Jodi Godfrey, Christine Marsteller, Jonathon Lowe, Rebecca Herman, Robert Johnston, and Gregory Henry for their expert technical assistance in conducting the feeding studies. We also thank Dr. Donna Toufexis for helping shape our understanding of stress–feeding relationships. 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 (MW), MH081816 (DT), and RR00165, and F31MH085445 (VM). 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.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2013 Springer Science+Business Media, LLC
About this protocol
Cite this protocol
Michopoulos, V., Moore, C., Wilson, M.E. (2013). Psychosocial Stress and Diet History Promote Emotional Feeding in Female Rhesus Monkeys. In: Avena, N. (eds) Animal Models of Eating Disorders. Neuromethods, vol 74. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-62703-104-2_8
Download citation
DOI: https://doi.org/10.1007/978-1-62703-104-2_8
Published:
Publisher Name: Humana Press, Totowa, NJ
Print ISBN: 978-1-62703-103-5
Online ISBN: 978-1-62703-104-2
eBook Packages: Springer Protocols