Highly palatable food during adolescence improves anxiety-like behaviors and hypothalamic-pituitary-adrenal axis dysfunction in rats that experienced neonatal maternal separation

Endocrinology and Metabolism

Volumn 29, Issue 2, 2014, Pages 169-178

  Lee, Jong Ho ^a,b   Kim, Jin Young ^a   Jahng, Jeong Won ^b  

^a BK 21 Plus   (South Korea)

^b Seoul National University   (South Korea)

Author keywords

Anxiety; Depression; Early life stress; Palatable food

Indexed keywords

EID: 84975686225     PISSN: 2093596X     EISSN: 20935978     Source Type: Journal    
DOI: 10.3803/EnM.2014.29.2.169     Document Type: Article

References (61)

1. Ladd CO, Huot RL, Thrivikraman KV, NemeroffCB, Meaney MJ, Plotsky PM. Long-term behavioral and neuroendocrine adaptations to adverse early experience. Prog Brain Res 2000;122:81-103.
2. El Khoury A, Gruber SH, Mork A, Mathe AA. Adult life behavioral consequences of early maternal separation are alleviated by escitalopram treatment in a rat model of depression. Prog Neuropsychopharmacol Biol Psychiatry 2006;30:535-40.
3. Kalinichev M, Easterling KW, Plotsky PM, Holtzman SG. Long-lasting changes in stress-induced corticosterone response and anxiety-like behaviors as a consequence of neonatal maternal separation in Long-Evans rats. Pharmacol Biochem Behav 2002;73:131-40.
4. Daniels WM, Pietersen CY, Carstens ME, Stein DJ. Maternal separation in rats leads to anxiety-like behavior and a blunted ACTH response and altered neurotransmitter levels in response to a subsequent stressor. Metab Brain Dis 2004; 19:3-14.
5. Ladd CO, Owens MJ, NemeroffCB. Persistent changes in corticotropin-releasing factor neuronal systems induced by maternal deprivation. Endocrinology 1996;137:1212-8.
6. van Oers HJ, de Kloet ER, Levine S. Early vs. late maternal deprivation differentially alters the endocrine and hypothalamic responses to stress. Brain Res Dev Brain Res 1998; 111:245-52.
7. Vazquez DM, Lopez JF, Van Hoers H, Watson SJ, Levine S. Maternal deprivation regulates serotonin 1A and 2A receptors in the infant rat. Brain Res 2000;855:76-82.
8. Jahng JW. An animal model of eating disorders associated with stressful experience in early life. Horm Behav 2011; 59:213-20.
9. Desmet PM, Schifferstein HN. Sources of positive and negative emotions in food experience. Appetite 2008;50: 290-301.
10. Teegarden SL, Bale TL. Decreases in dietary preference produce increased emotionality and risk for dietary relapse. Biol Psychiatry 2007;61:1021-9.
11. Buwalda B, Blom WA, Koolhaas JM, van Dijk G. Behavioral and physiological responses to stress are affected by high-fat feeding in male rats. Physiol Behav 2001;73:371-7.
12. Pecoraro N, Reyes F, Gomez F, Bhargava A, Dallman MF. Chronic stress promotes palatable feeding, which reduces signs of stress: feedforward and feedback effects of chronic stress. Endocrinology 2004;145:3754-62.
13. Prasad A, Prasad C. Short-term consumption of a diet rich in fat decreases anxiety response in adult male rats. Physiol Behav 1996;60:1039-42.
14. Albanidou-Farmaki E, Poulopoulos AK, Epivatianos A, Farmakis K, Karamouzis M, Antoniades D. Increased anxiety level and high salivary and serum cortisol concentrations in patients with recurrent aphthous stomatitis. Tohoku J Exp Med 2008;214:291-6.
15. Heim C, Newport DJ, Heit S, Graham YP, Wilcox M, Bonsall R, Miller AH, NemeroffCB. Pituitary-adrenal and autonomic responses to stress in women after sexual and physical abuse in childhood. JAMA 2000;284:592-7.
16. Kim HJ, Lee JH, Choi SH, Lee YS, Jahng JW. Fasting-induced increases of arcuate NPY mRNA and plasma corticosterone are blunted in the rat experienced neonatal maternal separation. Neuropeptides 2005;39:587-94.
17. Lee JH, Kim HJ, Kim JG, Ryu V, Kim BT, Kang DW, Jahng JW. Depressive behaviors and decreased expression of serotonin reuptake transporter in rats that experienced neonatal maternal separation. Neurosci Res 2007;58:32-9.
18. Ryu V, Lee JH, Yoo SB, Gu XF, Moon YW, Jahng JW. Sustained hyperphagia in adolescent rats that experienced neonatal maternal separation. Int J Obes (Lond) 2008;32: 1355-62.
19. Ryu V, Yoo SB, Kang DW, Lee JH, Jahng JW. Post-weaning isolation promotes food intake and body weight gain in rats that experienced neonatal maternal separation. Brain Res 2009;1295:127-34.
20. KalueffAV, Aldridge JW, LaPorte JL, Murphy DL, Tuohimaa P. Analyzing grooming microstructure in neurobehavioral experiments. Nat Protoc 2007;2:2538-44.
21. Porsolt RD, Le Pichon M, Jalfre M. Depression: a new animal model sensitive to antidepressant treatments. Nature 1977;266:730-2.
22. Ramos A, Mormede P. Stress and emotionality: a multidimensional and genetic approach. Neurosci Biobehav Rev 1998;22:33-57.
23. Barros HM, Tannhauser SL, Tannhauser MA, Tannhauser M. The effects of GABAergic drugs on grooming behaviour in the open field. Pharmacol Toxicol 1994;74:339-44.
24. KalueffAV, Tuohimaa P. Contrasting grooming phenotypes in three mouse strains markedly different in anxiety and activity (129S1, BALB/c and NMRI). Behav Brain Res 2005;160:1-10.
25. Ferre P, Fernandez-Teruel A, Escorihuela RM, Driscoll P, Corda MG, Giorgi O, Tobena A. Behavior of the Roman/Verh high-and low-avoidance rat lines in anxiety tests: relationship with defecation and self-grooming. Physiol Behav 1995;58:1209-13.
26. Nosek K, Dennis K, Andrus BM, Ahmadiyeh N, Baum AE, Solberg Woods LC, Redei EE. Context and strain-dependent behavioral response to stress. Behav Brain Funct 2008;4:23.
27. KalueffAV, Tuohimaa P. Grooming analysis algorithm for neurobehavioural stress research. Brain Res Brain Res Protoc 2004;13:151-8.
28. Kompagne H, Bardos G, Szenasi G, Gacsalyi I, Harsing LG, Levay G. Chronic mild stress generates clear depressive but ambiguous anxiety-like behaviour in rats. Behav Brain Res 2008;193:311-4.
29. Piato AL, Detanico BC, Jesus JF, Lhullier FL, Nunes DS, Elisabetsky E. Effects of Marapuama in the chronic mild stress model: further indication of antidepressant properties. J Ethnopharmacol 2008;118:300-4.
30. Yalcin I, Aksu F, Bodard S, Chalon S, Belzung C. Antidepressant-like effect of tramadol in the unpredictable chronic mild stress procedure: possible involvement of the noradrenergic system. Behav Pharmacol 2007;18:623-31.
31. Stetler C, Miller GE. Depression and hypothalamic-pituitary-adrenal activation: a quantitative summary of four decades of research. Psychosom Med 2011;73:114-26.
32. Garcia de Miguel B, Nutt DJ, Hood SD, Davies SJ. Elucidation of neurobiology of anxiety disorders in children through pharmacological challenge tests and cortisol measurements: a systematic review. J Psychopharmacol 2012;26:431-42.
33. Dietrich A, Ormel J, Buitelaar JK, Verhulst FC, Hoekstra PJ, Hartman CA. Cortisol in the morning and dimensions of anxiety, depression, and aggression in children from a general population and clinic-referred cohort: an integrated analysis. The TRAILS study. Psychoneuroendocrinology 2013;38:1281-98.
34. Romeo RD, McEwen BS. Stress and the adolescent brain. Ann N Y Acad Sci 2006;1094:202-14.
35. Romeo RD, Waters EM, McEwen BS. Steroid-induced hippocampal synaptic plasticity: sex differences and similarities. Neuron Glia Biol 2004;1:219-29.
36. Goldman L, Winget C, Hollingshead GW, Levine S. Postweaning development of negative feedback in the pituitary-adrenal system of the rat. Neuroendocrinology 1973; 12:199-211.
37. Vazquez DM, Morano MI, Lopez JF, Watson SJ, Akil H. Short-term adrenalectomy increases glucocorticoid and mineralocorticoid receptor mRNA in selective areas of the developing hippocampus. Mol Cell Neurosci 1993;4:455-71.
38. Boukouvalas G, Antoniou K, Papalexi E, Kitraki E. Post weaning high fat feeding affects rats' behavior and hypothalamic pituitary adrenal axis at the onset of puberty in a sexually dimorphic manner. Neuroscience 2008;153:373-82.
39. Boukouvalas G, Gerozissis K, Markaki E, Kitraki E. High-fat feeding influences the endocrine responses of pubertal rats to an acute stress. Neuroendocrinology 2010;92:235-45.
40. Soulis G, Papalexi E, Kittas C, Kitraki E. Early impact of a fat-enriched diet on behavioral responses of male and female rats. Behav Neurosci 2007;121:483-90.
41. Saiyudthong S, Marsden CA. Acute effects of bergamot oil on anxiety-related behaviour and corticosterone level in rats. Phytother Res 2011;25:858-62.
42. Scharf SH, Sterlemann V, Liebl C, Muller MB, Schmidt MV. Chronic social stress during adolescence: interplay of paroxetine treatment and ageing. Neuropharmacology 2013;72:38-46.
43. Salamone JD, Correa M. Motivational views of reinforcement: implications for understanding the behavioral functions of nucleus accumbens dopamine. Behav Brain Res 2002;137:3-25.
44. Di Chiara G, Loddo P, Tanda G. Reciprocal changes in prefrontal and limbic dopamine responsiveness to aversive and rewarding stimuli after chronic mild stress: implications for the psychobiology of depression. Biol Psychiatry 1999; 46:1624-33.
45. Gorwood P. Neurobiological mechanisms of anhedonia. Dialogues Clin Neurosci 2008;10:291-9.
46. Imperato A, Angelucci L, Casolini P, Zocchi A, Puglisi-Allegra S. Repeated stressful experiences differently affect limbic dopamine release during and following stress. Brain Res 1992;577:194-9.
47. Saal D, Dong Y, Bonci A, Malenka RC. Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons. Neuron 2003;37:577-82.
48. Jahng JW, Ryu V, Yoo SB, Noh SJ, Kim JY, Lee JH. Mesolimbic dopaminergic activity responding to acute stress is blunted in adolescent rats that experienced neonatal maternal separation. Neuroscience 2010;171:144-52.
49. Hernandez L, Hoebel BG. Food reward and cocaine increase extracellular dopamine in the nucleus accumbens as measured by microdialysis. Life Sci 1988;42:1705-12.
50. Small DM, Jones-Gotman M, Dagher A. Feeding-induced dopamine release in dorsal striatum correlates with meal pleasantness ratings in healthy human volunteers. Neuroimage 2003;19:1709-15.
51. Carlezon WA Jr, Thomas MJ. Biological substrates of reward and aversion: a nucleus accumbens activity hypothesis. Neuropharmacology 2009;56 Suppl 1:122-32.
52. Etkin A, Prater KE, Schatzberg AF, Menon V, Greicius MD. Disrupted amygdalar subregion functional connectivity and evidence of a compensatory network in generalized anxiety disorder. Arch Gen Psychiatry 2009;66:1361-72.
53. Tye KM, Prakash R, Kim SY, Fenno LE, Grosenick L, Zarabi H, Thompson KR, Gradinaru V, Ramakrishnan C, Deisseroth K. Amygdala circuitry mediating reversible and bidirectional control of anxiety. Nature 2011;471:358-62.
54. Cardinal RN, Parkinson JA, Hall J, Everitt BJ. Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci Biobehav Rev 2002;26: 321-52.
55. Rezayof A, Zarrindast MR, Sahraei H, Haeri-Rohani AH. Involvement of dopamine D2 receptors of the central amygdala on the acquisition and expression of morphine-induced place preference in rat. Pharmacol Biochem Behav 2002; 74:187-97.
56. Thiel KJ, Wenzel JM, Pentkowski NS, Hobbs RJ, Alleweireldt AT, Neisewander JL. Stimulation of dopamine D2/D3 but not D1 receptors in the central amygdala decreases cocaine-seeking behavior. Behav Brain Res 2010; 214:386-94.
57. Guarraci FA, Frohardt RJ, Young SL, Kapp BS. A functional role for dopamine transmission in the amygdala during conditioned fear. Ann N Y Acad Sci 1999;877:732-6.
58. Silberman Y, Winder DG. Corticotropin releasing factor and catecholamines enhance glutamatergic neurotransmission in the lateral subdivision of the central amygdala. Neuropharmacology 2013;70:316-23.
59. Hui GK, Figueroa IR, Poytress BS, Roozendaal B, McGaugh JL, Weinberger NM. Memory enhancement of classical fear conditioning by post-training injections of corticosterone in rats. Neurobiol Learn Mem 2004;81:67-74.
60. Shepard JD, Barron KW, Myers DA. Corticosterone delivery to the amygdala increases corticotropin-releasing factor mRNA in the central amygdaloid nucleus and anxiety-like behavior. Brain Res 2000;861:288-95.
61. Shepard JD, Barron KW, Myers DA. Stereotaxic localization of corticosterone to the amygdala enhances hypothalamo-pituitary-adrenal responses to behavioral stress. Brain Res 2003;963:203-13.