DOI QR코드

DOI QR Code

The Alleviating Effects of Sweet Drinks on Restraint Stress-Induced Anxiety and Depressive Behavior in Adolescent Rats

청소년기 동물모델에서 구속 스트레스로 유발된 불안, 우울행동에 미치는 영향

  • 김윤주 (경희대학교 간호과학대학) ;
  • 송민경 (럿거스대학교 의과대학) ;
  • 박종민 (부산대학교 간호대학) ;
  • 김연정 (경희대학교 간호과학대학)
  • Received : 2020.09.25
  • Accepted : 2020.11.29
  • Published : 2020.11.30

Abstract

Purpose: Some of the adolescent drinks more sugar-sweetened beverages. However, there is little evidence on the effect of eating behavior on emotional state and neurochemical changes under stress, especially on the levels of typical inhibitory neurotransmitters and gamma-aminobutyric acid. This article demonstrates that sucrose or saccharin drink reduces stress-related behavior responses and GABAergic deficits in adolescent rats. Methods: We randomly assigned 7-weeks-old Sprague-Dawley male rats to three groups: control group (Control), restraint stress only group (Stress), and restraint stress with unrestricted access to saccharin solution (Saccharin) and sucrose solution (Sucrose) as a positive control. We evaluated both anxious and depressive moods using an open field test and forced swim test, respectively. Using western blot analyses, the expression of a GABA-synthesizing enzyme, glutamate decarboxylase-67 (GAD67) and GABAergic markers, including calbindin and parvalbumin was assessed in the prefrontal cortex and the amygdala. Results: We found that both the drinks alleviated anxiety and depressive moods, induced significant attenuation in GAD67 level, and reduced calbindin level under stress in the prefrontal cortex and the amygdala. Conclusion: The results provide an understanding of the effect of sucrose or saccharin drink on stress-related responses. We propose the consumption of sweet drinks as a plausible strategy to alleviate stress-related alterations in adolescents.

Keywords

References

  1. Rosinger A, Herrick K, Gahche J, Park S. Sugar-sweetened beverage consumption among U.S. youth, 2011-2014. NCHS data brief. 2017;271:1-8.
  2. Kim J, Yun S, Oh K. Beverage consumption among korean adolescents: data from 2016 korea youth uisk behavior Survey. Nutrition Research and Practice. 2019;13(1):70. http://doi.org/10.4162/nrp.2019.13.1.70
  3. Kim A, Kim J, Kye S. Sugar-sweetened beverage consumption and influencing factors in korean adolescents: based on the 2017 korea youth risk behavior web-based survey. Journal of Nutrition and Health. 2018;51(5):465-479. https://doi.org/10.4163/jnh.2018.51.5.465
  4. Errisuriz VL, Pasch KE, Perry CL. Perceived stress and dietary choices: the moderating role of stress management. Eating Behaviors. 2016;22:211-216. http://doi.org/10.1016/j.eatbeh.2016.06.008
  5. Jacques A, Chaaya N, Beecher K, Ali SA, Belmer A, Bartlett S. The impact of sugar consumption on stress driven, emotional and addictive behaviors. Neuroscience & Biobehavioral Reviews. 2019;103:178-199. http://doi.org/10.1016/j.neubiorev.2019.05.021
  6. Sinha R. Role of addiction and stress neurobiology on food intake and obesity. Biological Psychology. 2018;131(2011):5-13. http://doi.org/10.1016/j.biopsycho.2017.05.001.
  7. Smeets PAM, Weijzen P, de Graaf C, Viergever MA. Consumption of caloric and non-caloric versions of a soft drink differentially affects brain activation during tasting. NeuroImage. 2011;54(2):1367-1374. http://doi.org/10.1016/j.neuroimage.2010.08.054
  8. Burke M V, Small DM. Physiological mechanisms by which non-nutritive sweeteners may impact body weight and metabolism. Physiology & Behavior. 2015;152:381-388. http://doi.org/10.1016/j.physbeh.2015.05.036
  9. Sheth C, McGlade E, Yurgelun-Todd D. Chronic stress in adolescents and its neurobiological and psychopathological consequences: an RDoC perspective. Chronic Stress. 2017;1:247054701771564. http://doi.org/10.1177/2470547017715645
  10. Pizzagalli DA. Depression, stress, and anhedonia: toward a synthesis and integrated model. Annual Review of Clinical Psychology. 2014;10(1):393-423. http://doi.org/10.1146/annurev-clinpsy-050212-185606
  11. Tzanoulinou S, Garcia-Mompo C, Castillo-Gomez E, Veenit V, Nacher J, Sandi C. Long-term behavioral programming induced by peripuberty stress in rats is accompanied by GABAergic-related alterations in the amygdala. PLoS ONE. 2014;9(4):e94666. http://doi.org/10.1371/journal.pone.0094666
  12. Zhang W, Rosenkranz JA. Effects of repeated stress on age-dependent gabaergic regulation of the lateral nucleus of the amygdala. Neuropsychopharmacology. 2016;41(9):2309-2323. http://doi.org/10.1038/npp.2016.33
  13. Martijena ID, Rodriguez Manzanares PA, Lacerra C, Molina VA. Gabaergic modulation of the stress response in frontal cortex and amygdala. Synapse. 2002;45(2):86-94. http://doi.org/10.1002/syn.10085.
  14. Ma K, Xu A, Cui S, Sun MR, Xue YC, Wang JH. Impaired GABA synthesis, uptake and release are associated with depression-like behaviors induced by chronic mild stress. Translational Psychiatry. 2016;6(10):e910. http://doi.org/10.1038/tp.2016.181
  15. Liu ZP, Song C, Wang M, He Y, Xu X Bin, Pan HQ, et al. Chronic stress impairs GABAergic control of amygdala through suppressing the tonic GABAA receptor currents. Molecular Brain. 2014;7(32):1-14. http://doi.org/10.1186/1756-6606-7-32
  16. Banasr M, Lepack A, Fee C, Duric V, Maldonado-Aviles J, DiLeone R, et al. Characterization of GABAergic marker expression in the chronic unpredictable stress model of depression. Chronic Stress. 2017;1:247054701772045. http://doi.org/10.1177/2470547017720459
  17. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C. Interneurons of the neocortical inhibitory system. Nature Reviews Neuroscience. 2004;5(10):793-807. http://doi.org/10.1038/nrn1519
  18. Rajkowska G, O'Dwyer G, Teleki Z, Stockmeier CA, Miguel-Hidalgo JJ. GAB-Aergic neurons immunoreactive for calcium binding proteins are reduced in the prefrontal cortex in major depression. Neuropsychopharmacology. 2007;32(2):471-482. http://doi.org/10.1038/sj.npp.1301234
  19. Tottenham N, Galvan A. Stress and the adolescent brain: amygdala-prefrontal cortex circuitry and ventral striatum as developmental targets. Neuroscience and Biobehavioral Reviews. 2016;70:217-227. http://doi.org/10.1016/j.neubiorev.2016.07.030
  20. Romeo RD. The impact of stress on the structure of the adolescent brain: implications for adolescent mental health. Brain Research. 2017;1654:185-191. http://doi.org/10.1016/j.brainres.2016.03.021
  21. Yang Q. Gain weight by "going diet?" artificial sweeteners and the neurobiology of sugar cravings: neuroscience 2010. The Yale journal of biology and medicine. 2010;83(2):101-108.
  22. Ulrich-Lai YM, Ostrander MM, Herman JP. HPA axis dampening by limited sucrose intake: reward frequency vs. caloric consumption. Physiology and Behavior. 2011;103(1):104-110. http://doi.org/10.1016/j.physbeh.2010.12.011
  23. Park JM, Song MK, Kim YJ, Kim YJ. Effect of saccharin intake in restraint-induced stress response reduction in rats. Journal of Korean Biological Nursing Science. 2016;18(1):36-42. http://doi.org/10.7586/jkbns.2016.18.1.36
  24. Salzman CD, Fusi S. Emotion, cognition, and mental state representation in amygdala and prefrontal cortex. Annual Review of Neuroscience. 2010;33:173-202. http://doi.org/10.1146/annurev.neuro.051508.135256
  25. Ulrich-Lai YM, Christiansen AM, Ostrander MM, Jones AA, Jones KR, Choi DC, et al. Pleasurable behaviors reduce stress via brain reward pathways. Proceedings of the National Academy of Sciences of the United States of America. 2010;107(47):20529-20534. http://doi.org/10.1073/pnas.1007740107
  26. Gilbert RM, Sherman IP. Palatability-induced polydipsia: saccharin, sucrose, and water intake in rats, with and without food deprivation. Psychological reports. 1970;27(2):319-325. http://doi.org/10.2466/pr0.1970.27.2.319
  27. Dess NK. Divergent responses to saccharin vs. sucrose availability after stress in rats. Physiology and Behavior. 1992;52(1):115-125. http://doi.org/10.1016/0031-9384(92)90440-d
  28. Seibenhener ML, Wooten MC. Use of the open field maze to measure locomotor and anxiety-like behavior in mice. Journal of Visualized Experiments. 2015;(96):e52434. http://doi.org/10.3791/52434
  29. Yankelevitch-Yahav R, Franko M, Huly A, Doron R. The forced swim test as a model of depressive-like behavior. Journal of Visualized Experiments. 2015;(97):52587. http://doi.org/10.3791/52587
  30. Ali EF, MacKay JC, Graitson S, James JS, Cayer C, Audet MC, et al. Palatable food dampens the long-term behavioral and endocrine effects of juvenile stressor exposure but may also provoke metabolic syndrome in rats. Frontiers in Behavioral Neuroscience. 2018;12:216. http://doi.org/10.3389/fnbeh.2018.00216
  31. Manzanares PAR, Isoardi NA, Carrer HF, Molina VA. Previous stress facilitates fear memory, attenuates GABAergic inhibition, and increases synaptic plasticity in the rat basolateral amygdala. Journal of Neuroscience. 2005;25(38):8725-8734. http://doi.org/10.1523/JNEUROSCI.2260-05.2005
  32. Liu WZ, Zhang WH, Zheng ZH, Zou JX, Liu XX, Huang SH, et al. Identification of a prefrontal cortex-to-amygdala pathway for chronic stress-induced anxiety. Nature Communications. 2020;11(1):2221. http://doi.org/10.1038/s41467-020-15920-7
  33. Wei J, Zhong P, Qin L, Tan T, Yan Z. Chemicogenetic restoration of the prefrontal cortex to amygdala pathway ameliorates stress-induced deficits. Cerebral cortex. 2018;28(6):1980-1990. http://doi.org/10.1093/cercor/bhx104
  34. Sharp BM. Basolateral amygdala and stress-induced hyperexcitability affect motivated behaviors and addiction. Translational psychiatry. 2017;7(8):e1194. http://doi.org/10.1038/tp.2017.161
  35. Jie F, Yin G, Yang W, Yang M, Gao S, Lv J, et al. Stress in regulation of GABA amygdala system and relevance to neuropsychiatric diseases. Frontiers in Neuroscience. 2018;12:1-9. http://doi.org/10.3389/fnins.2018.00562
  36. Prager EM, Bergstrom HC, Wynn GH, Braga MFM. The basolateral amygdala γ-aminobutyric acidergic system in health and disease. Journal of Neuroscience Research. 2016;94(6):548-567. http://doi.org/10.1002/jnr.23690
  37. Capogna M. GABAergic cell type diversity in the basolateral amygdala. Current Opinion in Neurobiology. 2014;26:110-116. http://doi.org/10.1016/j.conb.2014.01.006
  38. Loh DA, Moy FM, Zaharan NL, Jalaludin MY, Mohamed Z. Sugar-sweetened beverage intake and its associations with cardiometabolic risks among adolescents. Pediatric Obesity. 2017;12(1):e1-e5. http://doi.org/10.1111/ijpo.12108
  39. Chan TF, Lin WT, Huang HL, Lee CY, Wu PW, Chiu YW, et al. Consumption of Sugar-sweetened beverages is associated with components of the metabolic syndrome in adolescents. Nutrients. 2014;6(5):2088-2103. http://doi.org/10.3390/nu6052088
  40. Shin S, Kim SA, Ha J, Lim K. Sugar-sweetened beverage consumption in relation to obesity and metabolic syndrome among Korean adults: a cross-sectional study from the 2012-2016 Korean national health and nutrition examination survey (KNHANES). Nutrients. 2018;10(10):1467. http://doi.org/10.3390/nu10101467
  41. Jaaskelainen A, Nevanpera N, Remes J, Rahkonen F, Jarvelin M-R, Laitinen J. Stress-related eating, obesity and associated behavioural traits in adolescents: a prospective population-based cohort study. BMC Public Health. 2014;14(1):321. http://doi.org/10.1186/1471-2458-14-321