Hyperphagia and depression-like behavior by adolescence social isolation in female rats

International Journal of Developmental Neuroscience

Volumn 30, Issue 1, 2012, Pages 47-53

  Jahng, Jeong Won ^a   Yoo, Sang Bae ^a   Ryu, Vitaly ^a,b   Lee, Jong Ho ^a  

^a School of Dentistry   (South Korea)

^b WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Adolescence; Corticosterone; Early life stress; Eating disorders; Social isolation

Indexed keywords

CORTICOSTERONE;

ACUTE STRESS; ADOLESCENT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DEPRESSION; ELEVATED PLUS MAZE TEST; FEMALE; FOOD INTAKE; FORCED SWIMMING TEST; HYPERACTIVITY; HYPERPHAGIA; MAZE TEST; MOBILIZATION; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PSYCHOEMOTIONAL BEHAVIOR; RAT; REARING; SOCIAL ISOLATION; WEIGHT GAIN;

AGING; ANIMALS; BEHAVIOR, ANIMAL; BODY WEIGHT; DEPRESSIVE DISORDER; FEMALE; HYPERPHAGIA; MALE; RATS; RATS, SPRAGUE-DAWLEY; SEX FACTORS; SOCIAL ISOLATION; STRESS, PSYCHOLOGICAL;

RATTUS;

EID: 83855162778     PISSN: 07365748     EISSN: 1873474X     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2011.10.001     Document Type: Article

References (79)

1. Albanidou-Farmaki E., Poulopoulos A.K., 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, 214:291-296.
2. Anisman H., Matheson K. Stress, depression, and anhedonia: caveats concerning animal models. Neurosci. Biobehav. Rev. 2005, 29:525-546.
3. Bickerdike M.J., Wright I.K., Marsden C.A. Social isolation attenuates rat forebrain 5-HT release induced by KCl stimulation and exposure to a novel environment. Behav. Pharmacol. 1993, 4:231-236.
4. Boggiano M.M., Chandler P.C., Viana J.B., Oswald K.D., Maldonado C.R., Wauford P.K. Combined dieting and stress evoke exaggerated responses to opioids in binge-eating rats. Behav. Neurosci. 2005, 119:1207-1214.
5. Brown B.B. Adolescents' relationships with peers. Handbook of Adolescent Psychology 2004, 363-394. Wiley, New Jersey. 2nd ed. R.M. Lerner, L. Steinberg (Eds.).
6. Bruce M.L., Hoff R.A. Social and physical health risk factors for first onset major depressive disorder in a community sample. Soc. Psychiatry Psychiatr. Epidemiol. 1994, 29:165-171.
7. Chandler-Laney P.C., Castañeda E., Viana J.B., Oswald K.D., Maldonado C.R., Boggiano M.M. A history of human-like dieting alters serotonergic control of feeding and neurochemical balance in a rat model of binge-eating. Int. J. Eat. Disord. 2007, 40:136-142.
8. Daniels W.M., Pietersen C.Y., Carstens M.E., Stein D.J. Maternal separation in rats lead 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.
9. Darke S., Ross J. Suicide among heroin users: rates, risk factors and methods. Addiction 2002, 97:1383-1394.
10. Ding Y., Kang L., Li B., Ma L. Enhanced cocaine self-administration in adult rats with adolescent isolation experience. Pharmacol. Biochem. Behav. 2005, 82:673-677.
11. Douglas L., Varlinskaya E., Spear L. Rewarding properties of social interactions in adolescent and adult male and female rates: impact of social versus isolate housing of subjects and partners. Dev. Psychobiol. 2004, 45:153-162.
12. Dubé L., LeBel J.L., Lu J. Affect asymmetry and comfort food consumption. Physiol. Behav. 2005, 86:559-567.
13. Falkner N.H., Neumark-Sztainer D., Story M., Jeffery R.W., Beuhring T., Resnick M.D. Social, educational, and psychological correlates of weight status in adolescents. Obes. Res. 2001, 9:32-42.
14. Faraday M.M. Rat sex and strain differences in responses to stress. Physiol. Behav. 2002, 75:507-522.
15. Faraday M.M., O'Donoghue V.A., Grunberg N.E. Effects of nicotine and stress on locomotion in Sprague-Dawley and Long-Evans male and female rats. Pharmacol. Biochem. Behav. 2003, 74:325-333.
16. Fone K.C.F., Porkess M.V. Behavioural and neurochemical effects of post-weaning social isolation in rodents-relevance to developmental neuropsychiatric disorders. Neurosci. Biobehav. Rev. 2008, 32:1087-1102.
17. Fone K.C., Shalders K., Fox Z.D., Arthur R., Marsden C.A. Increased 5-HT2C receptor responsiveness occurs on rearing rats in social isolation. Psychopharmacology 1996, 123:346-352.
18. Fulford A.J., Marsden C.A. Conditioned release of 5-hydroxytryptamine in vivo in the nucleus accumbens following isolation-rearing in the rat. Neuroscience 1998, 83:481-487.
19. Fulford A.J., Marsden C.A. Effect of isolation-rearing on conditioned dopamine release in vivo in the nucleus accumbens of the rat. J. Neurochem. 1998, 70:384-390.
20. Gluck M.E., 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. N. Y. Acad. Sci. 2004, 1032:202-207.
21. Goossens L., Braet C., Van Vlierberghe L., Mels S. Loss of control over eating in overweight youngsters: the role of anxiety, depression and emotional eating. Eur. Eat. Disord. Rev. 2009, 17:68-78.
22. Grilo C.M., White M.A., Masheb R.M. DSM-IV psychiatric disorder comorbidity and its correlates in binge eating disorder. Int. J. Eat. Disord. 2009, 42:228-234.
23. Grissett N.I., Norvell N.K. Perceived social support, social skills, and quality of relationships in bulimic women. J. Consult. Clin. Psychol. 1992, 2:293-299.
24. Hagan M.M., Chandler P.C., Wauford P.K., Rybak R.J., Oswald K.D. The role of palatable food and hunger as trigger factors in an animal model of stress induced binge eating. Int. J. Eat. Disord. 2003, 34:183-197.
25. Hall F.S. Social deprivation of neonatal, adolescent, and adult rats has distinct neurochemical and behavioral consequences. Crit. Rev. Neurobiol. 1998, 12:129-162.
26. Hall F.S., Huang S., Fong G.F., Pert A. The effects of social isolation on the forced swim test in Fawn hooded and Wistar rats. J. Neurosci. Methods 1998, 79:47-51.
27. Hall F.S., Humby T., Wilkinson L.S., Robbins T.W. The effects of isolation-rearing on preference by rats for a novel environment. Physiol. Behav. 1997, 62:299-303.
28. Hall F.S., Sundstrom J.M., Lerner J., Perth A. Enhanced corticosterone release after a modified forced swim test in Fawn hooded rats is independent of rearing experience. Pharmacol. Biochem. Behav. 2001, 69:629-634.
29. Harlow H.F., Harlow M.K. The effect of rearing conditions on behavior. Int. J. Psychiatry 1965, 1:43-51.
30. Harmer C.J., Phillips G.D. Isolation rearing enhances acquisition in a conditioned inhibition paradigm. Physiol. Behav. 1998, 65:525-533.
31. Harris R.J. Where is the child's environment?. A group socialization theory of development. Psychol. Rev. 1995, 102:458-489.
32. Heaven P.C.L. Contemporary Adolescence: A Social Psychological Approach 1994, Macmillan, Melbourne.
33. Heim C., Newport D.J., Heit S., Graham Y.P., Wilcox M., Bonsall R., Miller A.H., Nemeroff C.B. Pituitary-adrenal and autonomic responses to stress in women after sexual and physical abuse in childhood. JAMA 2000, 284:593-597.
34. Heim C., Plotsky P.M., Nemeroff C.B. Importance of studying the contributions of early adverse experience to neurobiological findings in depression. Neuropsychopharmacology 2004, 29:641-648.
35. Hellemans K.G., Benge L.C., Olmstead M.C. Adolescent enrichment partially reverses the social isolation syndrome. Dev. Brain Res. 2004, 150:103-115.
36. Hirschfeld R., Weissmann M. Secondary risk factors for major depression and bipolar disorder. Neuropsychopharmacology: The Fifth Generation of Progress 2002, 1018-1025. Lippincott Williams & Wilkin, Philadelphia, PA. K.L. Davis, D. Charney, J.T. Coyle, C.B. Nemeroff (Eds.).
37. Howes S.R., Dalley J.W., Morrison C.H., Robbins T.W., Everitt B.J. Leftward shift in the acquisition of cocaine self-administration in isolation-reared rats: relationship to extracellular levels of dopamine, serotonin and glutamate in the nucleus accumbens and amygdala-striatal FOS expression. Psychopharmacology 2000, 151:55-63.
38. Jahng J.W. An animal model of eating disorders associated with stressful experience in early life. Horm. Behav. 2011, 59:213-220.
39. Javaras K.N., Pope H.G., Lalonde J.K., Roberts J.L., Nillni Y.I., Laird N.M., Bulik C.M., Crow S.J., McElroy S.L., Walsh B.T., Tsuang M.T., Rosenthal N.R., Hudson J.I. Co-occurrence of binge eating disorder with psychiatric and mental disorders. J. Clin. Psychiatry 2008, 69:266-273.
40. Johnston A.L., File S.E. Sex differences in animal tests of anxiety. Physiol. Behav. 1991, 49:245-250.
41. Jones G.H., Hernandez T.D., Kendall D.A., Marsden C.A., Robbins T.W. Dopaminergic and serotonergic function following isolation rearing in rats: study of behavioural responses and postmortem and in vivo neurochemistry. Pharmacol. Biochem. Behav. 1992, 3:17-35.
42. Kelley A.E., Schiltz C.A., Landry C.F. Neural systems recruited by drug- and food-related cues: studies of gene activation in corticolimbic regions. Physiol. Behav. 2005, 86:11-14.
43. Kenardy J., Brown W.J., Vogt E. Dieting and health in young Australian women. Eur. Eat. Disord. Rev. 2001, 9:242-254.
44. Kendler K.S., Bulik C.M., Silberg J., Hettema J.M., Myers J., Prescott C.A. Childhood sexual abuse and adult psychiatric and substance use disorders in women. Arch. Gen. Psychiatry 2000, 57:953-959.
45. Koo-Loeb J.H., Costello N., Light K.C., Girdler S.S. Women with eating disorder tendencies display altered cardiovascular, neuroendocrine, and physiological profiles. Psychosom. Med. 2000, 62:539-548.
46. Krolow R., Noschang C.G., Arcego D., Andreazza A.C., Peres W., Goncalves C.A., Dalmaz C. Consumption of a palatable diet by chronically stressed rats prevents effects on anxiety-like behavior but increases oxidative stress in a sex-specific manner. Appetite 2010, 55:108-116.
47. La Greca A.M., Prinstein M.J., Fetter M.D. Adolescent peer crow affiliation: linkages with health-risk behaviors and close friendships. J. Pediatric Psychol. 2001, 26:131-143.
48. Lehmann J., Pryce C.R., Bettschen D., Feldon J. The maternal separation paradigm and adult emotionality and cognition in male and female Wistar rats. Pharmacol. Biochem. Behav. 1999, 64:705-715.
49. Lowry C.A., Hale M.W., Plant A., Windle R.J., Shanks N., Wood S.A., Ingram C.D., Renner K.J., Lightman S.L., Summers C.H. Fluoxetine inhibits corticotropin-releasing factor (CRF)-induced behavioural responses in rats. Stress 2009, 12:225-239.
50. Lucion A.B., Charchat H., Pereira G.A., Rasia-Filho A.A. Influence of early postnatal gonadal hormones on anxiety in adult male rats. Physiol. Behav. 1996, 60:1419-1423.
51. Lukkes J.L., Watt M.J., Lowry C.A., Foster G.L. Consequences of post-weaning social isolation on anxiety behavior and related neural circuits in rodents. Front. Behav. Neurosci. 2009, 3:18.
52. McCormick C.M., Robarts D., Kopeikina K., Kelsey J.E. Long-lasting, sex- and age-specific effects of social stressors on corticosterone responses to restraint and on locomotor responses to psychostimulants in rats. Horm. Behav. 2005, 48:64-74.
53. McCormick C.M., Smith C., Mathews I.Z. Effects of chronic social stress in adolescence on anxiety and neuroendocrine response to mild stress in male and female rats. Behav. Brain Res. 2008, 187:228-238.
54. Muchimapura S., Fulford A.J., Mason R., Marsden C.A. Isolation rearing in the rat disrupts the hippocampal response to stress. Neuroscience 2002, 112:697-705.
55. Panksepp J.B., Lahvis G.P. Social reward among juvenile mice. Genes Brain Behav. 2007, 6:661-671.
56. Paul E.D., Hale M.W., Lukkes J.L., Valentine M.J., Sarchet D.M., Lowry C.A. Repeated social defeat increases reactive emotional coping behavior and alters functional responses in serotonergic neurons in the rat dorsal raphe nucleus. Physiol. Behav. 2011, 104:272-282.
57. Paxton S.J., Schutz H.K., Wertheim E.H., Muir S.L. Friendship clique and peer influences on body image attitudes, dietary restraint, extreme weight loss behaviours and binge eating in adolescent girls. J. Abnorm. Psychol. 1999, 108:255-266.
58. Pine D.S., Cohen P., Brook J., Coplan J.D. Psychiatric symptoms of adolescence as predictors of obesity in early adulthood: a longitudinal study. Am. J. Public Health 1997, 7:1303-1310.
59. Porsolt R.D., Le Pichon M., Jalfre M. Depression: a new animal model sensitive to antidepressant treatments. Nature 1977, 266:730-732.
60. Potegal M., Einon D. Aggressive behaviors in adult rats deprived of playfighting experience as juveniles. Dev. Psychobiol. 1989, 22:159-172.
61. Putignano P., Dubini A., Toja P., Invitti C., Bonfanti S., Redaelli G., Zappulli D., Cavagnini F. Salivary cortisol measurement in normal-weight, obese and anorexic women: comparison with plasma cortisol. Eur. J. Endocrinol. 2001, 145:165-171.
62. Rada P., Avena N.M., Hoebel B.G. Daily bingeing on sugar repeatedly releases dopamine in the accumbens shell. Neuroscience 2005, 134:737-744.
63. Rapoport J.L., Addington A.M., Frangou S., Psych M.R. The neurodevelopmental model of schizophrenia: update 2005. Mol. Psychiatry 2005, 10:434-449.
64. Robbins T.W., Jones G.H., Wilkinson L.S. Behavioural and neurochemical effects of early social deprivation in the rat. J. Psychopharmacol. 1996, 10:39-47.
65. Ryu V., Lee J.H., Yoo S.B., Gu X.F., Moon Y.W., Jahng J.W. Sustained hyperphagia in adolescent rats that experienced neonatal maternal separation. Int. J. Obes. 2008, 32:1355-1362.
66. Ryu V., Yoo S.B., Kang D.W., Lee J.H., Jahng J.W. Post-weaning isolation promotes food intake and body weight gain in rats that experienced neonatal maternal separation. Brain Res. 2009, 1295:127-134.
67. Sahakian B.J., Burdess C., Luckhurst H., Trayhurn P. Hyperactivity and obesity: the interaction of social isolation and cafeteria feeding. Physiol. Behav. 1982, 28:117-124.
68. Schutz H.K., Paxton S.J. Friendship quality, body dissatisfaction, dieting and disordered eating in adolescent girls. Br. J. Clin. Psychol. 2007, 46:67-83.
69. Serra M., Pisu M.G., Floris I., Biggio G. Social isolation-induced changes in the hypothalamic-pituitary-adrenal axis in the rat. Stress 2005, 8:259-264.
70. Striegel-Moore R.H., Silberstein L.R., Rodin J. The social self in bulimia nervosa: public self-consciousness, social anxiety and perceived fraudulence. J. Abnorm. Psychol. 1993, 102:297-303.
71. Ulrich-Lai Y.M., Ostrander M.M., Thomas I.M., Packard B.A., Furay A.R., Dolgas C.M., Van Hooren D.C., Figueiredo H.F., Mueller N.K., Choi D.C., Herman J.P. Daily limited access to sweetened drink attenuates hypothalamic-pituitary-adrenocortical axis stress responses. Endocrinology 2007, 148:1823-1834.
72. Varlinskaya E.I., Spear L.P. Social interactions in adolescent and adult Sprague-Dawley rats: impact of social deprivation and test context familiarity. Behav. Brain Res. 2008, 188:398-405.
73. Weiss I.C., Domeney A.M., Heidbreder C.A., Moreau J.L., Feldon J. Early social isolation, but not maternal separation, affects behavioral sensitization to amphetamine in male and female adult rats. Pharmacol. Biochem. Behav. 2001, 70:397-409.
74. Weiss I.C., Pryce C.R., Jongen-Rêlo A.L., Nanz-Bahr N.I., Feldon J. Effect of social isolation on stress-induced behavioral and neuroendocrine state in the rat. Behav. Brain Res. 2004, 152:279-295.
75. Whitaker-Azmitia P., Zhou F., Hobin J., Borella A. Isolation-rearing of rats produces deficits as adults in the serotonergic innervation of hippocampus. Peptides 2000, 21:1755-1759.
76. Wigger A., Neumann I.D. Periodic maternal deprivation induces gender-dependent alterations in behavioral and neuroendocrine responses to emotional stress in adult rats. Physiol. Behav. 1999, 66:293-302.
77. Wongwitdecha N., Marsden C.A. Effects of social isolation rearing on learning in the Morris water maze. Brain Res. 1996, 715:119-124.
78. Wright I.K., Upton N., Marsden C.A. Resocialisation of isolation-reared rats does not alter their anxiogenic profile on the elevated X-maze model of anxiety. Physiol. Behav. 1991, 50:1129-1132.
79. Zakrzewska K.E., Cusin I., Stricker-Krongard A., Boss O., Ricquier D., Jeanrenaud B., Rohner-Jeanrenaud F. Induction of obesity and hyperleptinemia by central glucocorticoid infusion in the rat. Diabetes 1999, 48:365-370.