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Enhanced motivation for food reward induced by stress and attenuation by corticotrophin-releasing factor receptor antagonism in rats: implications for overeating and obesity

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Abstract

Rationale

Overeating beyond individuals’ homeostatic needs critically contributes to obesity. The neurobehavioral mechanisms underlying the motivation to consume excessive foods with high calories are not fully understood.

Objective

The present study examined whether a pharmacological stressor, yohimbine, enhances the motivation to procure food reward with an emphasis on comparisons between standard lab chow and high-fat foods. The effects of corticotropin-releasing factor (CRF) receptor blockade by a CRF1-selective antagonist NBI on the stress-enhanced motivation for food reward were also assessed.

Methods

Male Sprague-Dawley rats with chow available ad libitum in their home cages were trained to press a lever under a progressive ratio schedule for deliveries of either standard or high-fat food pellets. For testing yohimbine stress effects, rats received an intraperitoneal administration of yohimbine 10 min before start of the test sessions. For testing effects of CRF1 receptor blockade on stress responses, NBI was administered 20 min prior to yohimbine challenge.

Results

The rats emitted higher levels of lever responses to procure the high-fat food pellets compared with their counterparts on standard food pellets. Yohimbine challenge facilitated lever responses for the reward in all of the rats, whereas the effect was more robust in the rats on high-fat food pellets compared with their counterparts on standard food pellets. An inhibitory effect of pretreatment with NBI was observed on the enhancing effect of yohimbine challenge but not on the responses under baseline condition without yohimbine administration.

Conclusions

Stress challenge significantly enhanced the motivation of satiated rats to procure extra food reward, especially the high-fat food pellets. Activation of CRF1 receptors is required for the stress-enhanced motivation for food reward. These results may have implications for our better understanding of the biobehavioral mechanisms of overeating and obesity.

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References

  • Abercrombie ED, Keller RW Jr, Zigmond MJ (1988) Characterization of hippocampal norepinephrine release as measured by microdialysis perfusion: pharmacological and behavioral studies. Neuroscience 27:897–904

    CAS  PubMed  Google Scholar 

  • Abizaid A, Gao Q, Horvath TL (2006) Thoughts for food: brain mechanisms and peripheral energy balance. Neuron 51:691–702

    CAS  PubMed  Google Scholar 

  • Adam TC, Epel ES (2007) Stress, eating and the reward system. Physiol Behav 91:449–458

    CAS  PubMed  Google Scholar 

  • Aghajanian GK, VanderMaelen CP (1982) Alpha 2-adrenoceptor-mediated hyperpolarization of locus coeruleus neurons: intracellular studies in vivo. Science 215:1394–1396

    CAS  PubMed  Google Scholar 

  • Baldo BA, Kelley AE (2007) Discrete neurochemical coding of distinguishable motivational processes: insights from nucleus accumbens control of feeding. Psychopharmacology (Berl) 191:439–459

    CAS  Google Scholar 

  • Bello NT, Walters AL, Verpeut JL, Cunha PP (2013) High-fat diet-induced alterations in the feeding suppression of low-dose nisoxetine, a selective norepinephrine reuptake inhibitor. J Obes 2013:457047

    PubMed Central  PubMed  Google Scholar 

  • Berghofer A, Pischon T, Reinhold T, Apovian CM, Sharma AM, Willich SN (2008) Obesity prevalence from a European perspective: a systematic review. BMC Public Health 8:200

    PubMed Central  PubMed  Google Scholar 

  • Berridge KC (2009) 'Liking' and 'wanting' food rewards: brain substrates and roles in eating disorders. Physiol Behav 97:537–550

    PubMed Central  CAS  PubMed  Google Scholar 

  • Berthoud HR (2004) Neural control of appetite: cross-talk between homeostatic and non-homeostatic systems. Appetite 43:315–317

    PubMed  Google Scholar 

  • Berthoud HR (2012) The neurobiology of food intake in an obesogenic environment. Proc Nutr Soc 71:478–487

    PubMed Central  PubMed  Google Scholar 

  • Berthoud HR, Morrison C (2008) The brain, appetite, and obesity. Annu Rev Psychol 59:55–92

    PubMed  Google Scholar 

  • Bertiere MC, Sy TM, Baigts F, Mandenoff A, Apfelbaum M (1984) Stress and sucrose hyperphagia: role of endogenous opiates. Pharmacol, Biochem Behav 20:675–679

    CAS  Google Scholar 

  • 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 18:13–24

    CAS  PubMed  Google Scholar 

  • Block JP, He Y, Zaslavsky AM, Ding L, Ayanian JZ (2009) Psychosocial stress and change in weight among US adults. Am J Epidemiol 170:181–192

    PubMed Central  PubMed  Google Scholar 

  • Born JM, Lemmens SG, Rutters F, Nieuwenhuizen AG, Formisano E, Goebel R, Westerterp-Plantenga MS (2010) Acute stress and food-related reward activation in the brain during food choice during eating in the absence of hunger. Int J Obes (Lond) 34:172–181

    CAS  Google Scholar 

  • Bossert JM, Ghitza UE, Lu L, Epstein DH, Shaham Y (2005) Neurobiology of relapse to heroin and cocaine seeking: an update and clinical implications. Eur J Pharmacol 526:36–50

    CAS  PubMed  Google Scholar 

  • Bossert JM, Marchant NJ, Calu DJ, Shaham Y (2013) The reinstatement model of drug relapse: recent neurobiological findings, emerging research topics, and translational research. Psychopharmacology 229:453–476

    PubMed Central  CAS  PubMed  Google Scholar 

  • Bremner JD, Krystal JH, Southwick SM, Charney DS (1996a) Noradrenergic mechanisms in stress and anxiety: I preclinical studies. Synapse 23:28–38

    CAS  PubMed  Google Scholar 

  • Bremner JD, Krystal JH, Southwick SM, Charney DS (1996b) Noradrenergic mechanisms in stress and anxiety: II clinical studies. Synapse 23:39–51

    CAS  PubMed  Google Scholar 

  • Bruijnzeel AW, Prado M, Isaac S (2009) Corticotropin-releasing factor-1 receptor activation mediates nicotine withdrawal-induced deficit in brain reward function and stress-induced relapse. Biol Psychiatry 66:110–117

    PubMed Central  CAS  PubMed  Google Scholar 

  • Brunner EJ, Chandola T, Marmot MG (2007) Prospective effect of job strain on general and central obesity in the Whitehall II Study. Am J Epidemiol 165:828–837

    PubMed  Google Scholar 

  • Caballero B (2007) The global epidemic of obesity: an overview. Epidemiol Rev 29:1–5

    PubMed  Google Scholar 

  • Calu DJ, Kawa AB, Marchant NJ, Navarre BM, Henderson MJ, Chen B, Yau HJ, Bossert JM, Schoenbaum G, Deisseroth K, Harvey BK, Hope BT, Shaham Y (2013) Optogenetic inhibition of dorsal medial prefrontal cortex attenuates stress-induced reinstatement of palatable food seeking in female rats. J Neurosci 33:214–226

    PubMed Central  CAS  PubMed  Google Scholar 

  • Calvez J, Fromentin G, Nadkarni N, Darcel N, Even P, Tome D, Ballet N, Chaumontet C (2011) Inhibition of food intake induced by acute stress in rats is due to satiation effects. Physiol Behav 104:675–683

    CAS  PubMed  Google Scholar 

  • Carels RA, Hoffman J, Collins A, Raber AC, Cacciapaglia H, O’Brien WH (2001) Ecological momentary assessment of temptation and lapse in dieting. Eat Behav 2:307–321

    CAS  PubMed  Google Scholar 

  • Carels RA, Douglass OM, Cacciapaglia HM, O’Brien WH (2004) An ecological momentary assessment of relapse crises in dieting. J Consult Clin Psychol 72:341–348

    PubMed  Google Scholar 

  • Charney DS, Heninger GR, Redmond DE Jr (1983) Yohimbine induced anxiety and increased noradrenergic function in humans: effects of diazepam and clonidine. Life Sci 33:19–29

    CAS  PubMed  Google Scholar 

  • Chopin P, Pellow S, File SE (1986) The effects of yohimbine on exploratory and locomotor behaviour are attributable to its effects at noradrenaline and not at benzodiazepine receptors. Neuropharmacology 25:53–57

    CAS  PubMed  Google Scholar 

  • Cifani C, Koya E, Navarre BM, Calu DJ, Baumann MH, Marchant NJ, Liu QR, Khuc T, Pickel J, Lupica CR, Shaham Y, Hope BT (2012) Medial prefrontal cortex neuronal activation and synaptic alterations after stress-induced reinstatement of palatable food seeking: a study using c-fos-GFP transgenic female rats. J Neurosci 32:8480–8490

    PubMed Central  CAS  PubMed  Google Scholar 

  • Cippitelli A, Damadzic R, Hansson AC, Singley E, Sommer WH, Eskay R, Thorsell A, Heilig M (2010) Neuropeptide Y (NPY) suppresses yohimbine-induced reinstatement of alcohol seeking. Psychopharmacology 208:417–426

    CAS  PubMed  Google Scholar 

  • Dallman MF (2010) Stress-induced obesity and the emotional nervous system. Trends Endocrinol Metab 21:159–165

    PubMed Central  CAS  PubMed  Google Scholar 

  • Dallman MF, Pecoraro NC, la Fleur SE (2005) Chronic stress and comfort foods: self-medication and abdominal obesity. Brain Behav Immun 19:275–280

    PubMed  Google Scholar 

  • Dal-Zotto S, Marti O, Delgado R, Armario A (2004) Potentiation of glucocorticoid release does not modify the long-term effects of a single exposure to immobilization stress. Psychopharmacology 177:230–237

    CAS  PubMed  Google Scholar 

  • Davis M, Redmond DE Jr, Baraban JM (1979) Noradrenergic agonists and antagonists: effects on conditioned fear as measured by the potentiated startle paradigm. Psychopharmacology 65:111–118

    CAS  PubMed  Google Scholar 

  • Depoortere RY, Li DH, Lane JD, Emmett-Oglesby MW (1993) Parameters of self-administration of cocaine in rats under a progressiveratio schedule. Pharmacol Biochem Behav 45:539–548

  • Diane A, Victoriano M, Fromentin G, Tome D, Larue-Achagiotis C (2008) Acute stress modifies food choice in Wistar male and female rats. Appetite 50:397–407

    PubMed  Google Scholar 

  • dos Santos RL, Mansur SS, Steffens SM, Faria MS, Marino-Neto J, Paschoalini MA (2009) Food intake increased after injection of adrenaline into the median raphe nucleus of free-feeding rats. Behav Brain Res 197:411–416

    PubMed  Google Scholar 

  • Duca FA, Covasa M (2012) Current and emerging concepts on the role of peripheral signals in the control of food intake and development of obesity. Br J Nutr 108:778–793

    CAS  PubMed  Google Scholar 

  • Elfhag K, Rossner S (2005) Who succeeds in maintaining weight loss? A conceptual review of factors associated with weight loss maintenance and weight regain. Obes Rev 6:67–85

    CAS  PubMed  Google Scholar 

  • 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 26:37–49

    CAS  PubMed  Google Scholar 

  • Epstein DH, Preston KL, Stewart J, Shaham Y (2006) Toward a model of drug relapse: an assessment of the validity of the reinstatement procedure. Psychopharmacology 189:1–16

    PubMed Central  CAS  PubMed  Google Scholar 

  • Erb S, Shaham Y, Stewart J (1998) The role of corticotropin-releasing factor and corticosterone in stress- and cocaine-induced relapse to cocaine seeking in rats. J Neurosci 18:5529–5536

    CAS  PubMed  Google Scholar 

  • Feltenstein MW, See RE (2006) Potentiation of cue-induced reinstatement of cocaine-seeking in rats by the anxiogenic drug yohimbine. Behav Brain Res 174:1–8

    CAS  PubMed  Google Scholar 

  • Figlewicz DP (2003) Adiposity signals and food reward: expanding the CNS roles of insulin and leptin. Am J Physiol Regul Integr Comp Physiol 284:R882–R892

    CAS  PubMed  Google Scholar 

  • Flegal KM, Carroll MD, Ogden CL, Curtin LR (2010) Prevalence and trends in obesity among US adults, 1999–2008. JAMA 303:235–241

    CAS  PubMed  Google Scholar 

  • Foster MT, Warne JP, Ginsberg AB, Horneman HF, Pecoraro NC, Akana SF, Dallman MF (2009) Palatable foods, stress, and energy stores sculpt corticotropin-releasing factor, adrenocorticotropin, and corticosterone concentrations after restraint. Endocrinology 150:2325–2333

    PubMed Central  CAS  PubMed  Google Scholar 

  • Funk D, Li Z, Le AD (2006) Effects of environmental and pharmacological stressors on c-fos and corticotropin-releasing factor mRNA in rat brain: relationship to the reinstatement of alcohol seeking. Neuroscience 138:235–243

    CAS  PubMed  Google Scholar 

  • Gao Q, Horvath TL (2007) Neurobiology of feeding and energy expenditure. Annu Rev Neurosci 30:367–398

    CAS  PubMed  Google Scholar 

  • Gautron L, Elmquist JK (2011) Sixteen years and counting: an update on leptin in energy balance. J Clin Invest 121:2087–2093

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ghitza UE, Gray SM, Epstein DH, Rice KC, Shaham Y (2006) The anxiogenic drug yohimbine reinstates palatable food seeking in a rat relapse model: a role of CRF1 receptors. Neuropsychopharmacology 31:2188–2196

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ghitza UE, Nair SG, Golden SA, Gray SM, Uejima JL, Bossert JM, Shaham Y (2007) Peptide YY3-36 decreases reinstatement of high-fat food seeking during dieting in a rat relapse model. J Neurosci 27:11522–11532

    PubMed Central  CAS  PubMed  Google Scholar 

  • Giardino WJ, Ryabinin AE (2013) CRF1 receptor signaling regulates food and fluid intake in the drinking-in-the-dark model of binge alcohol consumption. Alcohol Clin Exp Res 37:1161–1170

    PubMed Central  CAS  PubMed  Google Scholar 

  • Gibson EL (2006) Emotional influences on food choice: sensory, physiological and psychological pathways. Physiol Behav 89:53–61

    PubMed  Google Scholar 

  • Graf EN, Hoks MA, Baumgardner J, Sierra J, Vranjkovic O, Bohr C, Baker DA, Mantsch JR (2011) Adrenal activity during repeated long-access cocaine self-administration is required for later CRF-induced and CRF-dependent stressor-induced reinstatement in rats. Neuropsychopharmacology 36:1444–1454

    PubMed Central  CAS  PubMed  Google Scholar 

  • Grossman SP (1960) Eating or drinking elicited by direct adrenergic or cholinergic stimulation of hypothalamus. Science 132:301–302

    CAS  PubMed  Google Scholar 

  • Harris RB, Zhou J, Youngblood BD, Rybkin II, Smagin GN, Ryan DH (1998) Effect of repeated stress on body weight and body composition of rats fed low- and high-fat diets. Am J Physiol 275:R1928–R1938

    CAS  PubMed  Google Scholar 

  • Havel PJ (2001) Peripheral signals conveying metabolic information to the brain: short-term and long-term regulation of food intake and energy homeostasis. Exp Biol Med (Maywood) 226:963–977

    CAS  Google Scholar 

  • Herzog H (2003) Neuropeptide Y and energy homeostasis: insights from Y receptor knockout models. Eur J Pharmacol 480:21–29

    CAS  PubMed  Google Scholar 

  • Hodos W (1961) Progressive ratio as a measure of reward strength. Science 134:943–944

    CAS  PubMed  Google Scholar 

  • Holmberg G, Gershon S (1961) Autonomic and psychic effects of yohimbine hydrochloride. Psychopharmacologia 2:93–106

    CAS  PubMed  Google Scholar 

  • Jackson HC, Needham AM, Hutchins LJ, Mazurkiewicz SE, Heal DJ (1997) Comparison of the effects of sibutramine and other monoamine reuptake inhibitors on food intake in the rat. Br J Pharmacol 121:1758–1762

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kaplan HI, Kaplan HS (1957) The psychosomatic concept of obesity. J Nerv Ment Dis 125:181–201

    CAS  PubMed  Google Scholar 

  • Kelley AE, Baldo BA, Pratt WE, Will MJ (2005) Corticostriatal-hypothalamic circuitry and food motivation: integration of energy, action and reward. Physiol Behav 86:773–795

    CAS  PubMed  Google Scholar 

  • Kenny PJ (2011) Reward mechanisms in obesity: new insights and future directions. Neuron 69:664–679

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kinzig KP, Hargrave SL, Honors MA (2008) Binge-type eating attenuates corticosterone and hypophagic responses to restraint stress. Physiol Behav 95:108–113

    CAS  PubMed  Google Scholar 

  • Koob GF (2009) Brain stress systems in the amygdala and addiction. Brain Res 1293:61–75

    PubMed Central  CAS  PubMed  Google Scholar 

  • Koob GF, Heinrichs SC, Pich EM, Menzaghi F, Baldwin H, Miczek K, Britton KT (1993) The role of corticotropin-releasing factor in behavioural responses to stress. Ciba Found Symp 172:277–289, discussion 290-275

    CAS  PubMed  Google Scholar 

  • Kupferschmidt DA, Tribe E, Erb S (2009) Effects of repeated yohimbine on the extinction and reinstatement of cocaine seeking. Pharmacol, Biochem Behav 91:473–480

    CAS  Google Scholar 

  • Kyrou I, Chrousos GP, Tsigos C (2006) Stress, visceral obesity, and metabolic complications. Ann N Y Acad Sci 1083:77–110

    CAS  PubMed  Google Scholar 

  • la Fleur SE, Houshyar H, Roy M, Dallman MF (2005) Choice of lard, but not total lard calories, damps adrenocorticotropin responses to restraint. Endocrinology 146:2193–2199

    PubMed  Google Scholar 

  • Lang WJ, Gershon S (1963) Effects of psychoactive drugs on yohimbine induced responses in conscious dogs. A proposed screening procedure for anti-anxiety agents. Arch Int Pharmacodyn Ther 142:457–472

    CAS  PubMed  Google Scholar 

  • Lattimore P, Maxwell L (2004) Cognitive load, stress, and disinhibited eating. Eat Behav 5:315–324

    PubMed  Google Scholar 

  • Le A, Shaham Y (2002) Neurobiology of relapse to alcohol in rats. Pharmacol Ther 94:137–156

    CAS  PubMed  Google Scholar 

  • Le AD, Harding S, Juzytsch W, Watchus J, Shalev U, Shaham Y (2000) The role of corticotrophin-releasing factor in stress-induced relapse to alcohol-seeking behavior in rats. Psychopharmacology 150:317–324

    CAS  PubMed  Google Scholar 

  • Le AD, Harding S, Juzytsch W, Funk D, Shaham Y (2005) Role of alpha-2 adrenoceptors in stress-induced reinstatement of alcohol seeking and alcohol self-administration in rats. Psychopharmacology 179:366–373

    CAS  PubMed  Google Scholar 

  • Le AD, Funk D, Juzytsch W, Coen K, Navarre BM, Cifani C, Shaham Y (2011) Effect of prazosin and guanfacine on stress-induced reinstatement of alcohol and food seeking in rats. Psychopharmacology 218:89–99

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lee B, Tiefenbacher S, Platt DM, Spealman RD (2004) Pharmacological blockade of alpha2-adrenoceptors induces reinstatement of cocaine-seeking behavior in squirrel monkeys. Neuropsychopharmacology 29:686–693

    CAS  PubMed  Google Scholar 

  • Leibowitz SF (1986) Brain monoamines and peptides: role in the control of eating behavior. Fed Proc 45:1396–1403

    CAS  PubMed  Google Scholar 

  • Lemmens SG, Rutters F, Born JM, Westerterp-Plantenga MS (2011) Stress augments food 'wanting' and energy intake in visceral overweight subjects in the absence of hunger. Physiol Behav 103:157–163

    CAS  PubMed  Google Scholar 

  • Levin BE, Richard D, Michel C, Servatius R (2000) Differential stress responsivity in diet-induced obese and resistant rats. Am J Physiol Regul Integr Comp Physiol 279:R1357–R1364

    CAS  PubMed  Google Scholar 

  • Liu X (2010) Contribution of drug cue, priming, and stress to reinstatement of nicotine-seeking behavior in a rat model of relapse. In: Egger J, KAlb M (eds) Smoking relapse: causes, prevention, and recovery. Nova Science Publisher, New York, pp 143–163

    Google Scholar 

  • Liu X (2012) Stress as a risk factor for transition to heightened nicotine intake: evidence from a rat model of nicotine self-administration. In: Giovanni D (ed) Nicotine addiction: prevention, health effects and treatment options. Nova Science Publisher, Hauppauge, pp 115–134

    Google Scholar 

  • Liu X, Weiss F (2002) Additive effect of stress and drug cues on reinstatement of ethanol seeking: exacerbation by history of dependence and role of concurrent activation of corticotropin-releasing factor and opioid mechanisms. J Neurosci 22:7856–7861

    CAS  PubMed  Google Scholar 

  • Lu L, Shepard JD, Hall FS, Shaham Y (2003) Effect of environmental stressors on opiate and psychostimulant reinforcement, reinstatement and discrimination in rats: a review. Neurosci Biobehav Rev 27:457–491

    CAS  PubMed  Google Scholar 

  • Lutter M, Nestler EJ (2009) Homeostatic and hedonic signals interact in the regulation of food intake. J Nutr 139:629–632

    PubMed Central  CAS  PubMed  Google Scholar 

  • Maniam J, Morris MJ (2012) The link between stress and feeding behaviour. Neuropharmacology 63:97–110

    CAS  PubMed  Google Scholar 

  • Markou A, Weiss F, Gold LH, Caine SB, Schulteis G, Koob GF (1993) Animal models of drug craving. Psychopharmacology 112:163–182

    CAS  PubMed  Google Scholar 

  • 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 55:747–753

    CAS  PubMed  Google Scholar 

  • Miyasaka K, Kanai S, Ohta M, Hosoya H, Takano S, Sekime A, Sakurai C, Kaneko T, Tahara S, Funakoshi A (2005) Overeating after restraint stress in cholecystokinin-a receptor-deficient mice. Jpn J Physiol 55:285–291

    CAS  PubMed  Google Scholar 

  • Nair SG, Gray SM, Ghitza UE (2006) Role of food type in yohimbine- and pellet-priming-induced reinstatement of food seeking. Physiol Behav 88:559–566

    PubMed Central  CAS  PubMed  Google Scholar 

  • Nair SG, Golden SA, Shaham Y (2008) Differential effects of the hypocretin 1 receptor antagonist SB 334867 on high-fat food self-administration and reinstatement of food seeking in rats. Br J Pharmacol 154:406–416

    PubMed Central  CAS  PubMed  Google Scholar 

  • Nair SG, Adams-Deutsch T, Pickens CL, Smith DG, Shaham Y (2009) Effects of the MCH1 receptor antagonist SNAP 94847 on high-fat food-reinforced operant responding and reinstatement of food seeking in rats. Psychopharmacology 205:129–140

    PubMed Central  CAS  PubMed  Google Scholar 

  • Nair SG, Navarre BM, Cifani C, Pickens CL, Bossert JM, Shaham Y (2011) Role of dorsal medial prefrontal cortex dopamine D1-family receptors in relapse to high-fat food seeking induced by the anxiogenic drug yohimbine. Neuropsychopharmacology 36:497–510

    PubMed Central  CAS  PubMed  Google Scholar 

  • Nieuwenhuizen AG, Rutters F (2008) The hypothalamic-pituitary-adrenal-axis in the regulation of energy balance. Physiol Behav 94:169–177

    CAS  PubMed  Google Scholar 

  • Nishitani N, Sakakibara H (2006) Relationship of obesity to job stress and eating behavior in male Japanese workers. Int J Obes (Lond) 30:528–533

    CAS  Google Scholar 

  • Nishitani N, Sakakibara H, Akiyama I (2009) Eating behavior related to obesity and job stress in male Japanese workers. Nutrition 25:45–50

    PubMed  Google Scholar 

  • O’Connor DB, Jones F, Conner M, McMillan B, Ferguson E (2008) Effects of daily hassles and eating style on eating behavior. Health Psychol 27:S20–S31

    PubMed  Google Scholar 

  • Oliver G, Wardle J, Gibson EL (2000) Stress and food choice: a laboratory study. Psychosom Med 62:853–865

    CAS  PubMed  Google Scholar 

  • Oliver KG, Huon GF, Zadro L, Williams KD (2001) The role of interpersonal stress in overeating among high and low disinhibitors. Eat Behav 2:19–26

    CAS  PubMed  Google Scholar 

  • Ozier AD, Kendrick OW, Leeper JD, Knol LL, Perko M, Burnham J (2008) Overweight and obesity are associated with emotion- and stress-related eating as measured by the eating and appraisal due to emotions and stress questionnaire. J Am Diet Assoc 108:49–56

    PubMed  Google Scholar 

  • 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 145:3754–3762

    CAS  PubMed  Google Scholar 

  • Pickens CL, Cifani C, Navarre BM, Eichenbaum H, Theberge FR, Baumann MH, Calu DJ, Shaham Y (2012) Effect of fenfluramine on reinstatement of food seeking in female and male rats: implications for the predictive validity of the reinstatement model. Psychopharmacology 221:341–353

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ramachandrappa S, Farooqi IS (2011) Genetic approaches to understanding human obesity. J Clin Invest 121:2080–2086

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ricart-Jane D, Rodriguez-Sureda V, Benavides A, Peinado-Onsurbe J, Lopez-Tejero MD, Llobera M (2002) Immobilization stress alters intermediate metabolism and circulating lipoproteins in the rat. Metabolism 51:925–931

    CAS  PubMed  Google Scholar 

  • Richards JK, Simms JA, Steensland P, Taha SA, Borgland SL, Bonci A, Bartlett SE (2008) Inhibition of orexin-1/hypocretin-1 receptors inhibits yohimbine-induced reinstatement of ethanol and sucrose seeking in Long-Evans rats. Psychopharmacology 199:109–117

    PubMed Central  CAS  PubMed  Google Scholar 

  • Rodaros D, Caruana DA, Amir S, Stewart J (2007) Corticotropin-releasing factor projections from limbic forebrain and paraventricular nucleus of the hypothalamus to the region of the ventral tegmental area. Neuroscience 150:8–13

    CAS  PubMed  Google Scholar 

  • Rowland NE, Antelman SM (1976) Stress-induced hyperphagia and obesity in rats: a possible model for understanding human obesity. Science 191:310–312

    CAS  PubMed  Google Scholar 

  • Rutters F, Nieuwenhuizen AG, Lemmens SG, Born JM, Westerterp-Plantenga MS (2009) Acute stress-related changes in eating in the absence of hunger. Obesity (Silver Spring) 17:72–77

    Google Scholar 

  • Rybkin II, Zhou Y, Volaufova J, Smagin GN, Ryan DH, Harris RB (1997) Effect of restraint stress on food intake and body weight is determined by time of day. Am J Physiol 273:R1612–R1622

    CAS  PubMed  Google Scholar 

  • Salamone JD, Cousins MS, McCullough LD, Carriero DL, Berkowitz RJ (1994) Nucleus accumbens dopamine release increases during instrumental lever pressing for food but not free food consumption. Pharmacol, Biochem Behav 49:25–31

    CAS  Google Scholar 

  • Sarlio-Lahteenkorva S, Rissanen A, Kaprio J (2000) A descriptive study of weight loss maintenance: 6 and 15 year follow-up of initially overweight adults. Int J Obes Relat Metab Disord 24:116–125

    CAS  PubMed  Google Scholar 

  • Schachter S (1968) Obesity and eating. Internal and external cues differentially affect the eating behavior of obese and normal subjects. Science 161:751–756

    CAS  PubMed  Google Scholar 

  • Schroeder BE, Schiltz CA, Kelley AE (2003) Neural activation profile elicited by cues associated with the anxiogenic drug yohimbine differs from that observed for reward-paired cues. Neuropsychopharmacology 28:14–21

    CAS  PubMed  Google Scholar 

  • Scott C, Johnstone AM (2012) Stress and eating behaviour: implications for obesity. Obes Facts 5:277–287

    PubMed  Google Scholar 

  • Shaham Y, Funk D, Erb S, Brown TJ, Walker CD, Stewart J (1997) Corticotropin-releasing factor, but not corticosterone, is involved in stress-induced relapse to heroin-seeking in rats. J Neurosci 17:2605–2614

    CAS  PubMed  Google Scholar 

  • Shaham Y, Erb S, Stewart J (2000) Stress-induced relapse to heroin and cocaine seeking in rats: a review. Brain Res Brain Res Rev 33:13–33

    CAS  PubMed  Google Scholar 

  • Shaham Y, Shalev U, Lu L, De Wit H, Stewart J (2003) The reinstatement model of drug relapse: history, methodology and major findings. Psychopharmacology 168:3–20

    CAS  PubMed  Google Scholar 

  • Shepard JD, Bossert JM, Liu SY, Shaham Y (2004) The anxiogenic drug yohimbine reinstates methamphetamine seeking in a rat model of drug relapse. Biol Psychiatry 55:1082–1089

    CAS  PubMed  Google Scholar 

  • Sinha R, Jastreboff AM (2013) Stress as a common risk factor for obesity and addiction. Biol Psychiatry 73:827–835

    PubMed Central  CAS  PubMed  Google Scholar 

  • Solomon MB, Foster MT, Bartness TJ, Huhman KL (2007) Social defeat and footshock increase body mass and adiposity in male Syrian hamsters. Am J Physiol Regul Integr Comp Physiol 292:R283–R290

    CAS  PubMed  Google Scholar 

  • Steffens AB, Strubbe JH (1987) Regulation of body weight and food intake. Sci Prog 71:545–561

    CAS  PubMed  Google Scholar 

  • Sumithran P, Proietto J (2013) The defence of body weight: a physiological basis for weight regain after weight loss. Clin Sci (Lond) 124:231–241

    Google Scholar 

  • Swiergiel AH, Wieczorek M (2008) Noradrenaline-induced feeding responses in the rat do not depend on food characteristics. Acta Neurobiol Exp 68:354–361

    Google Scholar 

  • Tellez LA, Ferreira JG, Medina S, Land BB, DiLeone RJ, de Araujo IE (2013) Flavor-independent maintenance, extinction, and reinstatement of fat self-administration in mice. Biol Psychiatry 73:851–859

    PubMed Central  CAS  PubMed  Google Scholar 

  • Torres SJ, Nowson CA (2007) Relationship between stress, eating behavior, and obesity. Nutrition 23:887–894

    PubMed  Google Scholar 

  • Uhde TW, Boulenger JP, Post RM, Siever LJ, Vittone BJ, Jimerson DC, Roy-Byrne PP (1984) Fear and anxiety: relationship to noradrenergic function. Psychopathology 17(Suppl 3):8–23

    PubMed  Google Scholar 

  • Valles A, Marti O, Garcia A, Armario A (2000) Single exposure to stressors causes long-lasting, stress-dependent reduction of food intake in rats. Am J Physiol Regul Integr Comp Physiol 279:R1138–R1144

    CAS  PubMed  Google Scholar 

  • Volkow ND, Wang GJ, Tomasi D, Baler RD (2013) Obesity and addiction: neurobiological overlaps. Obes Rev 14:2–18

    CAS  PubMed  Google Scholar 

  • Wallach MB, Dawber M, McMahon M, Rogers C (1977) A new anorexigen assay: stress-induced hyperphagia in rats. Pharmacol, Biochem Behav 6:529–531

    CAS  Google Scholar 

  • Wallis DJ, Hetherington MM (2009) Emotions and eating. Self-reported and experimentally induced changes in food intake under stress. Appetite 52:355–362

    CAS  PubMed  Google Scholar 

  • Wanat MJ, Hopf FW, Stuber GD, Phillips PE, Bonci A (2008) Corticotropin-releasing factor increases mouse ventral tegmental area dopamine neuron firing through a protein kinase C-dependent enhancement of Ih. J Physiol 586:2157–2170

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wellman PJ (2005) Modulation of eating by central catecholamine systems. Curr Drug Targets 6:191–199

    CAS  PubMed  Google Scholar 

  • Westerterp KR, Speakman JR (2008) Physical activity energy expenditure has not declined since the 1980s and matches energy expenditures of wild mammals. Int J Obes (Lond) 32:1256–1263

    CAS  Google Scholar 

  • Williams KW, Elmquist JK (2012) From neuroanatomy to behavior: central integration of peripheral signals regulating feeding behavior. Nat Neurosci 15:1350–1355

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wirtshafter D, Stratford TR (2010) Evidence for motivational effects elicited by activation of GABA-A or dopamine receptors in the nucleus accumbens shell. Pharmacol, Biochem Behav 96:342–346

    CAS  Google Scholar 

  • Woods SC, Seeley RJ, Porte D Jr, Schwartz MW (1998) Signals that regulate food intake and energy homeostasis. Science 280:1378–1383

    CAS  PubMed  Google Scholar 

  • Zarrindast MR, Homayoun H, Babaie A, Etminani A, Gharib B (2000) Involvement of adrenergic and cholinergic systems in nicotine-induced anxiogenesis in mice. Eur J Pharmacol 407:145–158

    CAS  PubMed  Google Scholar 

  • Zellner DA, Loaiza S, Gonzalez Z, Pita J, Morales J, Pecora D, Wolf A (2006) Food selection changes under stress. Physiol Behav 87:789–793

    CAS  PubMed  Google Scholar 

  • Zheng H, Lenard NR, Shin AC, Berthoud HR (2009) Appetite control and energy balance regulation in the modern world: reward-driven brain overrides repletion signals. Int J Obes (Lond) 33(Suppl 2):S8–S13

    CAS  Google Scholar 

  • Zislis G, Desai TV, Prado M, Shah HP, Bruijnzeel AW (2007) Effects of the CRF receptor antagonist D-Phe CRF(12-41) and the alpha2-adrenergic receptor agonist clonidine on stress-induced reinstatement of nicotine-seeking behavior in rats. Neuropharmacology 53:958–966

    PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by National Institutes of Health grants R01DA017288 and R01DA037277 from the National Institute on Drug Abuse and funds from the Department of Psychiatry and Human Behavior, University of Mississippi Medical Center. The author thanks Courtney Jernigan, Lisa Biswas, Laura Beloate, Ramachandram Avusula, Treniea Tolliver, Trisha Patel, and Jonathan Lee for their excellent technical assistance.

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  1. Department of Psychiatry and Human Behavior, University of Mississippi Medical Center, 2500 North State Street, Jackson, MS, 39216, USA

    Xiu Liu

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Liu, X. Enhanced motivation for food reward induced by stress and attenuation by corticotrophin-releasing factor receptor antagonism in rats: implications for overeating and obesity. Psychopharmacology 232, 2049–2060 (2015). https://doi.org/10.1007/s00213-014-3838-1

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