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Pleasurable behaviors reduce stress via brain reward pathways
Yvonne M. Ulrich-Lai,a1 Anne M. Christiansen,a Michelle M. Ostrander,aAmanda A. Jones,a Kenneth R. Jones,a Dennis C. Choi,a2 Eric G. Krause,a Nathan K. Evanson,a Amy R. Furay,a3 Jon F. Davis,a Matia B. Solomon,a Annette D. de Kloet,a Kellie L. Tamashiro,a4 Randall R. Sakai,aRandy J. Seeley,b Stephen C. Woods,a and James P. Hermana
Departments of aPsychiatry and Behavioral Neuroscience and
bInternal Medicine, University of Cincinnati, Cincinnati, OH 45237
1To whom correspondence should be addressed. E-mail:
Edited by Bruce S. McEwen, The Rockefeller University, New York, NY, and approved September 22, 2010 (received for review June 3, 2010)
Contributed by
Author contributions: Y.M.U.-L., A.M.C., M.M.O., A.A.J., K.R.J., D.C.C., E.G.K., N.K.E., A.R.F., J.F.D., M.B.S., A.D.d.K., K.L.T., R.R.S., R.J.S., S.C.W., and J.P.H. designed research; Y.M.U.-L., A.M.C., M.M.O., A.A.J., K.R.J., D.C.C., E.G.K., N.K.E., A.R.F., J.F.D., M.B.S., A.D.d.K., and K.L.T. performed research; Y.M.U.-L., A.M.C., M.M.O., A.A.J., D.C.C., E.G.K., N.K.E., and A.R.F. analyzed data; and Y.M.U.-L. wrote the paper.
2Present address: Howard Hughes Medical Institute, Center for Behavioral Neuroscience, Yerkes National Primate Research Center, Emory University, Atlanta, GA 30303.
3Present address: Department of Psychiatry and Behavioral Sciences, University of Washington, Seattle, WA 98195.
4Present address: Department of Psychiatry and Behavioral Sciences, The Johns Hopkins University, Baltimore, MD 21205.
Individuals often eat calorically dense, highly palatable “comfort” foods during stress for stress relief. This article demonstrates that palatable food intake (limited intake of sucrose drink) reduces neuroendocrine, cardiovascular, and behavioral responses to stress in rats. Artificially sweetened (saccharin) drink reproduces the stress dampening, whereas oral intragastric gavage of sucrose is without effect. Together, these results suggest that the palatable/rewarding properties of sucrose are necessary and sufficient for stress dampening. In support of this finding, another type of natural reward (sexual activity) similarly reduces stress responses. Ibotenate lesions of the basolateral amygdala (BLA) prevent stress dampening by sucrose, suggesting that neural activity in the BLA is necessary for the effect. Moreover, sucrose intake increases mRNA and protein expression in the BLA for numerous genes linked with functional and/or structural plasticity. Lastly, stress dampening by sucrose is persistent, which is consistent with long-term changes in neural activity after synaptic remodeling. Thus, natural rewards, such as palatable foods, provide a general means of stress reduction, likely via structural and/or functional plasticity in the BLA. These findings provide a clearer understanding of the motivation for consuming palatable foods during times of stress and influence therapeutic strategies for the prevention and/or treatment of obesity and other stress-related disorders.
Keywords: corticosterone, anxiety-related behavior, synaptophysin, cAMP response element-binding protein, calcium/calmodulin-dependent protein kinase
The obesity epidemic is fueled by the easy availability of palatable, calorically dense foods amid an ever-escalating level of daily stress (13). Humans and rodents increase palatable food consumption when stressed (36), and the term “comfort food” is commonly used to signify possible stress-dampening properties of certain foods (particularly calorically dense foods containing high amounts of carbohydrates and/or fats). Indeed, comfort food intake in humans is linked with improved emotional states (7), and a high-carbohydrate diet is associated with reduced resting and stress-evoked cortisol levels (811).
Stress (a real or perceived threat to homeostasis or well-being) typically evokes both physiological and emotional responses (reviewed in ref. 12). The physiological responses include activation of the hypothalamic–pituitary–adrenocortical (HPA) axis and the sympathetic branch of the autonomic nervous system. Activation of the sympathetic nervous system has numerous effects, including increases in heart rate and blood pressure. Activation of the HPA axis results in elevations in circulating adrenocorticotropic hormone (ACTH) and glucocorticoids (e.g., cortisol in humans and corticosterone in rats). Glucocorticoids have widespread action on numerous physiological processes, including mobilization of stored energy and maintenance of vascular tone. Perceived stressors also engage emotional responses, recruiting fear, anxiety, and defense-related neurocircuitry to trigger context-appropriate behavioral responses. In toto, the stress response produces a new physiological and emotional state designed to optimize survival in the face of real or perceived adversity.
The mechanism providing stress buffering by comfort foods (613) likely resides at the interface among stress, reward, and/or metabolic circuitry in the brain. We now demonstrate that rewarding properties of palatable foods can effectively buffer all major physiological and behavioral responses to stress, and we identify key neural circuits underlying the comfort food effect. Identification of these neural circuits provides potential strategies for intervening to prevent or curtail increasing rates of obesity and other metabolic disorders.