Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Article
  • Published:

Acute stress potentiates brain response to milkshake as a function of body weight and chronic stress

International Journal of Obesity volume 37, pages 309–316 (2013)Cite this article

Subjects

Abstract

OBJECTIVE:

Stress is associated with an increased intake of palatable foods and with weight gain, particularly in overweight women. Stress, food and body mass index (BMI) have been separately shown to affect amygdala activity. However, it is not known whether stress influences amygdala responses to palatable foods, and whether this response is associated with chronic stress or BMI.

DESIGN:

A total of 14 overweight and obese women participated in a functional magnetic resonance imaging (fMRI) scan as they consumed a palatable milkshake during script-driven, autobiographical, guided imagery of stressful and neutral-relaxing scenarios.

RESULTS:

We report that a network including insula, somatomotor mouth area, ventral striatum and thalamus responds to milkshake receipt, but none of these areas are affected by stress. In contrast, whereas the left amygdala responds to milkshake irrespective of condition, the right amygdala responds to milkshake only under stressful conditions. Moreover, this right amygdala response is positively associated with basal cortisol levels, an objective measure of chronic stress. We also found a positive relationship between BMI and stress-related increased response to milkshake in the orbitofrontal cortex (OFC).

CONCLUSION:

These results demonstrate that acute stress potentiates response to food in the right amygdala and OFC as a function of chronic stress and body weight, respectively. This suggests that the influence of acute stress in potentiating amygdala and OFC responses to food is dependent upon individual factors like BMI and chronic stress. We conclude that BMI and chronic stress play a significant role in brain response to food and in stress-related eating.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

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

    Article  CAS  PubMed  Google Scholar 

  2. Finkelstein EA, Trogdon JG, Cohen JW, Dietz W . Annual medical spending attributable to obesity: payer-and service-specific estimates. Health Aff 2009; 28: w822–w831.

    Article  Google Scholar 

  3. Dallman MF, Pecoraro N, Akana SF, la Fleur SE, Gomez F, Houshyar H et al. Chronic stress and obesity: a new view of “comfort food”. Proc Natl Acad Sci USA 2003; 100: 11696–11701.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Epel ES, Lapidus R, McEwen BS, Brownell K . Stress may add bite to appetite in women: a laboratory study of stress-induced cortisol and eating behavior. Psychoneuroendocrinology 2001; 26: 37–49.

    Article  CAS  PubMed  Google Scholar 

  5. Dallman MF, Pecoraro N, la Fleur SE . Chronic stress and comfort foods: self-medication and abdominal obesity. Brain Behav Immun 2005; 19: 275–280.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  Google Scholar 

  8. Rutters F, Nieuwenhuizen AG, Lemmens SGT, Born JM, Westerterp-Plantenga MS . Acute stress-related changes in eating in the absence of hunger. Obesity 2008; 17: 72–77.

    Article  PubMed  Google Scholar 

  9. Ely DR, Dapper V, Marasca J, Corrêa JB, Gamaro GD, Xavier MH et al. Effect of restraint stress on feeding behavior of rats. Physiol Behav 1997; 61: 395–398.

    Article  CAS  PubMed  Google Scholar 

  10. Ng DM, Jeffery RW . Relationships between perceived stress and health behaviors in a sample of working adults. Health Psychol 2003; 22: 638–642.

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  12. Greeno CG, Wing RR . Stress-induced eating. Psychol Bull 1994; 115: 444–464.

    Article  CAS  PubMed  Google Scholar 

  13. Laitinen J, Ek E, Sovio U . Stress-related eating and drinking behavior and body mass index and predictors of this behavior. Prev Med 2002; 34: 29–39.

    Article  PubMed  Google Scholar 

  14. Small DM, Veldhuizen MG, Felsted JA, Mak YE, McGlone F . Separable substrates for anticipatory and consummatory food chemosensation. Neuron 2008; 57: 786–797.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Felsted JA, Ren X, Chouinard-Decorte F, Small DM . Genetically determined differences in brain response to a primary food reward. J Neurosci 2010; 30: 2428–2432.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Gottfried JA, O’Doherty J, Dolan RJ . Encoding predictive reward value in human amygdala and orbitofrontal cortex. Science 2003; 301: 1104–1107.

    Article  CAS  PubMed  Google Scholar 

  17. Beaver JD, Lawrence AD, van Ditzhuijzen J, Davis MH, Woods A, Calder AJ . Individual differences in reward drive predict neural responses to images of food. J Neurosci 2006; 26: 5160–5166.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Small DM, Gerber JC, Mak YE, Hummel T . Differential neural responses evoked by orthonasal versus retronasal odorant perception in humans. Neuron 2005; 47: 593–605.

    Article  CAS  PubMed  Google Scholar 

  19. Stice E, Yokum S, Blum K, Bohon C . Weight gain is associated with reduced striatal response to palatable food. J Neurosci 2010; 30: 13105–13109.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Yokum S, Ng J, Stice E . Attentional bias to food images associated with elevated weight and future weight gain: an fMRI study, 2011; 19: 1775–1783.

  21. Stice E, Spoor S, Bohon C, Small DM . Relation between obesity and blunted striatal response to food is moderated by TaqIA A1 allele. Science 2008; 322: 449–452.

    Article  CAS  PubMed  Google Scholar 

  22. Chouinard-Decorte F, Felsted JA, Small DM . Increased amygdala response and decreased influence of internal state on amygdala response to food in overweight compared to healthy weight individuals. Appetite 2010; 54: 639.

    Article  Google Scholar 

  23. Duvarci S, Pare D . Glucocorticoids enhance the excitability of principal basolateral amygdala neurons. J Neurosci 2007; 27: 4482–4491.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Mitra R, Jadhav S, McEwen BS, Vyas A, Chattarji S . Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala. Proc Natl Acad Sci USA 2005; 102: 9371–9376.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Pelletier JG, Likhtik E, Filali M, Par D . Lasting increases in basolateral amygdala activity after emotional arousal: implications for facilitated consolidation of emotional memories. Learn Mem 2005; 12: 96–102.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Cousijn H, Rijpkema M, Qin S, van Marle HJF, Franke B, Hermans EJ et al. Acute stress modulates genotype effects on amygdala processing in humans. Proc Natl Acad Sci USA 2010; 107: 9867–9872.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Tillfors M, Furmark T, Marteinsdottir I, Fischer H, Pissiota A, Langstrom B et al. Cerebral blood flow in subjects with social phobia during stressful speaking tasks: a PET study. Am J Psychiatry 2001; 158: 1220–1226.

    Article  CAS  PubMed  Google Scholar 

  28. Tillfors M, Furmark T, Marteinsdottir I, Fredrikson M . Cerebral blood flow during anticipation of public speaking in social phobia: a PET study. Biol Psychiatry 2002; 52: 1113–1119.

    Article  PubMed  Google Scholar 

  29. Gianaros PJ, Sheu LK, Matthews KA, Jennings JR, Manuck SB, Hariri AR . Individual differences in stressor-evoked blood pressure reactivity vary with activation, volume, and functional connectivity of the amygdala. J Neurosci 2008; 28: 990–999.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Taylor SE, Burklund LJ, Eisenberger NI, Lehman BJ, Hilmert CJ, Lieberman MD . Neural bases of moderation of cortisol stress responses by psychosocial resources. J Pers Soc Psychol 2008; 95: 197–211.

    Article  PubMed  Google Scholar 

  31. Holland PC, Petrovich GD, Gallagher M . The effects of amygdala lesions on conditioned stimulus-potentiated eating in rats. Physiol Behav 2002; 76: 117–129.

    Article  CAS  PubMed  Google Scholar 

  32. Weingarten H . Conditioned cues elicit feeding in sated rats: a role for learning in meal initiation. Science 1983; 220: 431–433.

    Article  CAS  PubMed  Google Scholar 

  33. LaBar KS, Gitelman DR, Parrish TB, Kim YH, Nobre AC, Mesulam MM . Hunger selectively modulates corticolimbic activation to food stimuli in humans. Behav Neurosci 2001; 115: 493–500.

    Article  CAS  PubMed  Google Scholar 

  34. O’Doherty JP, Deichmann R, Critchley HD, Dolan RJ . Neural responses during anticipation of a primary taste reward. Neuron 2002; 33: 815–826.

    Article  PubMed  Google Scholar 

  35. Mohanty A, Gitelman DR, Small DM, Mesulam MM . The spatial attention network interacts with limbic and monoaminergic systems to modulate motivation-induced attention shifts. Cerebral Cortex 2008; 18: 2604–2613.

    Article  PubMed  PubMed Central  Google Scholar 

  36. O’Doherty J, Rolls ET, Francis S, Bowtell R, McGlone F, Kobal G et al. Sensory-specific satiety-related olfactory activation of the human orbitofrontal cortex. NeuroReport 2000; 11: 893–897.

    Article  PubMed  Google Scholar 

  37. Malik S, McGlone F, Bedrossian D, Dagher A . Ghrelin modulates brain activity in areas that control appetitive behavior. Cell Metabol 2008; 7: 400–409.

    Article  CAS  Google Scholar 

  38. Stoeckel LE, Weller RE, Cook III EW, Twieg DB, Knowlton RC, Cox JE . Widespread reward-system activation in obese women in response to pictures of high-calorie foods. NeuroImage 2008; 41: 636–647.

    Article  PubMed  Google Scholar 

  39. Small DM . Toward an understanding of the brain substrates of reward in humans. Neuron 2002; 33: 668–671.

    Article  CAS  PubMed  Google Scholar 

  40. Nolan-Poupart S, Veldhuizen MG . Midbrain and Medial Orbital Cortex Response to Milkshake Predicts Ad Lib Milkshake Intake. Poster presented at: Organization for Human Brain Mapping Annual Meeting, 26–30 June 2011, Quebec City, Canada.

  41. Sinha R . Modeling stress and drug craving in the laboratory: implications for addiction treatment development. Addict Biol 2009; 14: 84–98.

    Article  PubMed  Google Scholar 

  42. Sinha R, Catapano D, O’Malley S . Stress-induced craving and stress response in cocaine dependent individuals. Psychopharmacology 1999; 142: 343–351.

    Article  CAS  PubMed  Google Scholar 

  43. Britton JC, Phan KL, Taylor SF, Fig LM, Liberzon I . Corticolimbic blood flow in posttraumatic stress disorder during script-driven imagery. Biol Psychiatry 2005; 57: 832–840.

    Article  PubMed  Google Scholar 

  44. McEwen BS, Stellar E . Stress and the individual: mechanisms leading to disease. Arch Intern Med 1993; 153: 2093–2101.

    Article  CAS  PubMed  Google Scholar 

  45. Wüst S, Federenko I, Hellhammer DH, Kirschbaum C . Genetic factors, perceived chronic stress, and the free cortisol response to awakening. Psychoneuroendocrinology 2000; 25: 707–720.

    Article  PubMed  Google Scholar 

  46. Schulz P, Kirschbaum C, Pruessner JC, Hellhammer DH . Increased free cortisol secretion after awakening in chronically stressed individuals due to work overload. Stress Health 1998; 14: 91–97.

    Google Scholar 

  47. Sinha R, Lovallo W, Parsons O . Cardiovascular differentiation of emotions. Psychosom Med 1992; 54: 422–435.

    Article  CAS  PubMed  Google Scholar 

  48. Miller GA, Levin DN, Kozak MJ, Cook EW, McLean A, Lang PJ . Individual differences in imagery and the psychophysiology of emotion. Cogn Emotion 1987; 1: 367.

    Article  Google Scholar 

  49. Veldhuizen MG, Bender G, Constable RT, Small DM . Trying to detect taste in a tasteless solution: modulation of early gustatory cortex by attention to taste. Chem Senses 2007; 1987; 32: 569.

    Article  PubMed  Google Scholar 

  50. Friston KJ, Holmes AP, Worsley KJ, Poline J-P, Frith CD, Frackowiak RSJ . Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp 1994; 2: 189–210.

    Article  Google Scholar 

  51. Worsley KJ, Friston KJ . Analysis of fMRI time-series revisited--again. NeuroImage 1995; 2: 173–181.

    Article  CAS  PubMed  Google Scholar 

  52. Strange B, Portas C, Dolan RJ, Holmes AP, Friston KJ . Random effects analysis for event-related fMRI. NeuroImage 1999; 9): 1053–1089.

    Google Scholar 

  53. Nichols T, Brett M, Anderson J, Wager T, Poline J-P . Valid conjunction inference with the minimum statistic. NeuroImage 2005; 25: 653–660.

    Article  PubMed  Google Scholar 

  54. Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH . An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. NeuroImage 2003; 19: 1233–1239.

    Article  PubMed  Google Scholar 

  55. Holsen LM, Zarcone JR, Brooks WM, Butler MG, Thompson TI, Ahluwalia JS et al. Neural mechanisms underlying hyperphagia in Prader-Willi syndrome. Obesity 2006; 14: 1028–1037.

    Article  PubMed  Google Scholar 

  56. Petrovich GD, Setlow B, Holland PC, Gallagher M . Amygdalo-hypothalamic circuit allows learned cues to override satiety and promote eating. J Neurosci 2002; 22: 8748–8753.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Ng J, Stice E, Yokum S, Bohon C . An fMRI study of obesity, food reward, and perceived caloric density. Does a low-fat label make food less appealing? Appetite 2011; 57: 65–72.

    Article  PubMed  PubMed Central  Google Scholar 

  58. Steptoe A, Cropley M, Griffith J, Kirschbaum C . Job strain and anger expression predict early morning elevations in salivary cortisol. Psychosom Med 2000; 62: 286–292.

    Article  CAS  PubMed  Google Scholar 

  59. Marciani L, Pfeiffer JC, Hort J, Head K, Bush D, Taylor AJ et al. Improved methods for fMRI studies of combined taste and aroma stimuli. J Neurosci Meth 2006; 158: 186–194.

    Article  Google Scholar 

  60. Rothemund Y, Preuschhof C, Bohner G, Bauknecht H-C, Klingebiel R, Flor H et al. Differential activation of the dorsal striatum by high-calorie visual food stimuli in obese individuals. NeuroImage 2007; 37: 410–421.

    Article  PubMed  Google Scholar 

  61. Karhunen LJ, Lappalainen RI, Vanninen EJ, Kuikka JT, Uusitupa MI . Regional cerebral blood flow during food exposure in obese and normal-weight women. Brain 1997; 120: 1675–1684.

    Article  PubMed  Google Scholar 

  62. Martin LE, Holsen LM, Chambers RJ, Bruce AS, Brooks WM, Zarcone JR et al. Neural mechanisms associated with food motivation in obese and healthy weight adults. Obesity 2009; 18: 254–260.

    Article  PubMed  Google Scholar 

  63. Stice E, Yokum S, Bohon C, Marti N, Smolen A . Reward circuitry responsivity to food predicts future increases in body mass: moderating effects of DRD2 and DRD4. NeuroImage 2010; 50: 1618–1625.

    Article  CAS  PubMed  Google Scholar 

  64. Pruessner M, Hellhammer DH, Pruessner JC, Lupien SJ . Self-reported depressive symptoms and stress levels in healthy young men: associations with the cortisol response to awakening. Psychosom Med 2003; 65: 92–99.

    Article  CAS  PubMed  Google Scholar 

  65. Mcewen BS . Protection and damage from acute and chronic stress: allostasis and allostatic overload and relevance to the pathophysiology of psychiatric disorders. Ann NY Acad Sci 2004; 1032: 1–7.

    Article  PubMed  Google Scholar 

  66. Tataranni PA, Larson DE, Snitker S, Young JB, Flatt JP, Ravussin E . Effects of glucocorticoids on energy metabolism and food intake in humans. Am J Physiol-Endoc M 1996; 271: E317–E325.

    CAS  Google Scholar 

  67. Bjorntorp P, Rosmond R . Neuroendocrine abnormalities in visceral obesity. Int J Obes 2000; 24 (Suppl 2): S80–S85.

    Article  CAS  Google Scholar 

  68. Mårin P, Darin N, Amemiya T, Andersson B, Jern S, Björntorp P . Cortisol secretion in relation to body fat distribution in obese premenopausal women. Metabolism 1992; 41: 882–886.

    Article  PubMed  Google Scholar 

  69. Koo-Loeb JH, Costello N, Light KC, Girdler SS . Women with eating disorder tendencies display altered cardiovascular, neuroendocrine, and psychosocial profiles. Psychosom Med 2000; 62: 539–548.

    Article  CAS  PubMed  Google Scholar 

  70. Abell TL, Malagelada JR, Lucas AR, Brown ML, Camilleri M, Go VL et al. Gastric electromechanical and neurohormonal function in anorexia nervosa. Gastroenterology 1987; 93: 958–965.

    Article  CAS  PubMed  Google Scholar 

  71. Gluck ME, Geliebter A, Lorence M . Cortisol stress response is positively correlated with central obesity in obese women with binge eating disorder (BED) before and after cognitive-behavioral treatment. Ann NY Acad Sci 2004; 1032: 202–207.

    Article  CAS  PubMed  Google Scholar 

  72. Torres S, Nowson C . Relationship between stress, eating behavior, and obesity. Nutrition 2007; 23: 887–894.

    Article  PubMed  Google Scholar 

  73. Davidson RJ . Anxiety and affective style: role of prefrontal cortex and amygdala. Biol Psychiatry 2002; 51: 68–80.

    Article  PubMed  Google Scholar 

  74. Davidson RJ, Irwin W . The functional neuroanatomy of emotion and affective style. Trends Cog Sci 1999; 3: 11–21.

    Article  CAS  Google Scholar 

  75. Coleman-Mesches K, McGaugh JL . Differential involvement of the right and left amygdalae in expression of memory for aversively motivated training. Brain Res 1995; 670: 75–81.

    Article  CAS  PubMed  Google Scholar 

  76. Adamec RE, Morgan HD . The effect of kindling of different nuclei in the left and right amygdala on anxiety in the rat. Physiol Behav 1994; 55: 1–12.

    Article  CAS  PubMed  Google Scholar 

  77. Morris JS, Ohman A, Dolan RJ . A subcortical pathway to the right amygdala mediating “unseen” fear. Proc Natl Acad Sci USA 1999; 96: 1680–1685.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Bremner JD, Narayan M, Anderson ER, Staib LH, Miller HL, Charney DS . Hippocampal volume reduction in major depression. Am J Psychiatry 2000; 157: 115–118.

    Article  CAS  PubMed  Google Scholar 

  79. Angrilli A, Mauri A, Palomba D, Flor H, Birbaumer N, Sartori G et al. Startle reflex and emotion modulation impairment after a right amygdala lesion. Brain 1996; 119: 1991–2004.

    Article  PubMed  Google Scholar 

  80. Adolphs R, Tranel D, Damasio H . Emotion recognition from faces and prosody following temporal lobectomy. Neuropsychology 2001; 15: 396–404.

    Article  CAS  PubMed  Google Scholar 

  81. Rauch SL, Whalen PJ, Shin LM, McInerney SC, Macklin ML, Lasko NB et al. Exaggerated amygdala response to masked facial stimuli in posttraumatic stress disorder: a functional MRI study. Biol Psychiatry 2000; 47: 769–776.

    Article  CAS  PubMed  Google Scholar 

  82. Born JM, Lemmens SGT, Rutters F, Nieuwenhuizen AG, Formisano E, Goebel R et al. Acute stress and food-related reward activation in the brain during food choice during eating in the absence of hunger. Int J Obes 2009; 34: 172–181.

    Article  Google Scholar 

  83. Bohon C, Stice E, Spoor S . Female emotional eaters show abnormalities in consummatory and anticipatory food reward: a functional magnetic resonance imaging study. Int J Eat Disord 2009; 42: 210–221.

    Article  PubMed  PubMed Central  Google Scholar 

  84. Hinton EC, Parkinson JA, Holland AJ, Arana FS, C Roberts A, Owen AM . Neural contributions to the motivational control of appetite in humans. Eur J Neurosci 2004; 20: 1411–1418.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Sandra Stankovic and Dr Keri Bergquist for assistance in study design and Dr Marga Veldhuizen for assistance in data processing. This work was funded by the National Institutes of Health (NIH) R01DK085579 and U54 DA022292 pilot project awarded to DMS, as well as the NIH Roadmap for Medical Research Common Fund grants UL1-RR024139 (Yale Clinical and Translational Science Award), UL1-DE019586 and the PL1-DA024859 awarded to RS and NIH NRSA F31-DC010557-01 awarded to KJR.

Author information

Authors and Affiliations

  1. Interdepartmental Neuroscience Program, Yale University, New Haven, CT, USA

    K J Rudenga

  2. The John B Pierce Laboratory, New Haven, CT, USA

    K J Rudenga & D M Small

  3. Department of Psychiatry, Yale University School of Medicine, New Haven, CT, USA

    R Sinha & D M Small

Authors
  1. K J Rudenga
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R Sinha
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D M Small
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D M Small.

Ethics declarations

Competing interests

The authors declare no conflict of interest.

Additional information

Supplementary Information accompanies the paper on International Journal of Obesity website

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rudenga, K., Sinha, R. & Small, D. Acute stress potentiates brain response to milkshake as a function of body weight and chronic stress. Int J Obes 37, 309–316 (2013). https://doi.org/10.1038/ijo.2012.39

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ijo.2012.39

Keywords

This article is cited by

Search

Advanced search

Quick links