Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-10T23:30:46.811Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects of maternal separation on the dietary preference and behavioral satiety sequence in rats

Published online by Cambridge University Press:  31 March 2014

M. C. da Silva ,
J. A. de Souza ,
L. O. dos Santos ,
I. L. Pinheiro ,
T. K. F. Borba ,
A. A. M. da Silva ,
R. M. de Castro  and
S. L. de Souza
M. C. da Silva*
Affiliation:
Academic Center of Victoria, University of Pernambuco, Vitoria de Santo Antao, Pernambuco, Brazil
J. A. de Souza
Affiliation:
Department of Anatomy, Federal University of Pernambuco, Recife-PE, Brazil
L. O. dos Santos
Affiliation:
Academic Center of Victoria, University of Pernambuco, Vitoria de Santo Antao, Pernambuco, Brazil
I. L. Pinheiro
Affiliation:
Nutrition Department, Federal University of Pernambuco, Recife-PE, Brazil
T. K. F. Borba
Affiliation:
Department of Anatomy, Federal University of Pernambuco, Recife-PE, Brazil
A. A. M. da Silva
Affiliation:
Department of Anatomy, Federal University of Pernambuco, Recife-PE, Brazil
R. M. de Castro
Affiliation:
Nutrition Department, Federal University of Pernambuco, Recife-PE, Brazil
S. L. de Souza
Affiliation:
Department of Anatomy, Federal University of Pernambuco, Recife-PE, Brazil
*
*Address for correspondence: M. C. da Silva, Academic Victory Center, Federal University of Pernambuco, Rua do Alto reservoir S/N-Bela Vista Cep: 50608-680, Vitoria de Santo Antao, Pernambuco-Brazil. (Email Sanlopesufpe@gmail.com)
Get access Rights & Permissions [Opens in a new window]

Abstract

This study investigated the effects of maternal separation on the feeding behavior of rats. A maternal separation model was used on postnatal day 1 (PND1), forming the following groups: in the maternal separation (MS) group, pups were separated from their mothers each day from PND1 to PND14, whereas in the control (C) group pups were kept with their mothers. Subgroups were formed to study the effects of light and darkness: control with dark and light exposure, female and male (CF and CM), and maternal separation with dark and light exposure, female and male (SDF, SDM, SLF and SLM). Female rats had higher caloric intake relative to body weight compared with male controls in the dark period only (CF=23.3±0.5 v. CM=18.2±0.7, P<0.001). Macronutrient feeding preferences were observed, with male rats exhibiting higher caloric intake from a protein diet as compared with female rats (CF=4.1±0.7, n=8 v. CM=7.0±0.5, n=8, P<0.05) and satiety development was not interrupted. Female rats had a higher adrenal weight as compared with male rats independently of experimental groups and exhibited a higher concentration of serum triglycerides (n=8, P<0.001). The study indicates possible phenotypic adjustments in the structure of feeding behavior promoted by maternal separation, especially in the dark cycle. The dissociation between the mother’s presence and milk intake probably induces adjustments in feeding behavior during adulthood.

Keywords

feeding behaviormaternal separationmacronutrient feeding preferences
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 5 , Issue 3 , June 2014 , pp. 219 - 228
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1. Ader, R. The effects of early experience on the adrenocortical response to different magnitudes of stimulation. Physiol Behav. 1970; 5, 837–839.CrossRefGoogle ScholarPubMed
2. Amorim, EM, Damasceno, DC, Perobelli, JE, et al. Short- and long-term reproductive effects of prenatal and lactational growth restriction caused by maternal diabetes in male rats. Reprod Biol Endocrinol. 2011; 9, 154.CrossRefGoogle Scholar
3. Bass, J, Takahashi., JS. Circadian integration of metabolism and energetics. Science. 2010; 330 1349–1354.CrossRefGoogle ScholarPubMed
4. Biagini, G, Pich, EM, Carani, C, Marrama, P, Agnati, LF. Postnatal maternal separation during the stress hyporesponsive period enhances the adrenocortical response to novelty in adult rats by affecting feedback regulation in the CA1 hippocampal field. Int J Dev Neurosci. 1998; 16, 187–197.CrossRefGoogle ScholarPubMed
5. Blaustein, JD, Wade, GN. Ovarian influences on the meal patterns of female rats. Physiol Behav. 1976; 17, 201–208.CrossRefGoogle ScholarPubMed
6. Blundell, JE, Halford, JC. Regulation of nutrient supply: the brain and appetite control. Proc Nutr Soc. 1994; 53, 407–418.CrossRefGoogle ScholarPubMed
7. Brown-Grant, K, Exley, D, Naftolin, F. Peripheral plasma oestradiol and luteinizing hormone concentrations during the oestrous cycle of the rat. J Endocrinol. 1970; 48, 295–296.CrossRefGoogle ScholarPubMed
8. Burgess, LH, Handa, RJ. Estrogen-induced alterations in the regulation of mineralocorticoid and glucocorticoid receptor messenger RNA expression in the female rat anterior pituitary gland and brain. Mol Cell Neurosci. 1993; 4, 191–198.CrossRefGoogle ScholarPubMed
9. Carey, MP, Deterd, CH, de Koning, J, Helmerhorst, F, de Kloet, ER. The influence of ovarian steroids on hypothalamic-pituitary-adrenal regulation in the female rat. J Endocrinol. 1995; 144, 311–321.CrossRefGoogle ScholarPubMed
10. Cusin, I, Rouru, J, Rohner-Jeanrenaud, F. Intracerebroventricular glucocorticoid infusion in normal rats: induction of parasympathetic-mediated obesity and insulin resistance. Obes Res. 2001; 9, 401–406.CrossRefGoogle ScholarPubMed
11. Dallman, MF, Akana, SF, Laugero, KD, et al. A spoonful of sugar: feedback signals of energy stores and corticosterone regulate responses to chronic stress. Physiol Behav. 2003; 79, 3–12.CrossRefGoogle ScholarPubMed
12. Darnaudery, M, Maccari, S. Epigenetic programming of the stress response in male and female rats by prenatal restraint stress. Brain Res Rev. 2008; 57, 571–585.CrossRefGoogle ScholarPubMed
13. de Jongh, R, Geyer, MA, Olivier, B, Groenink, L. The effects of sex and neonatal maternal separation on fear-potentiated and light-enhanced startle. Behav Brain Res. 2005; 161, 190–196.CrossRefGoogle ScholarPubMed
14. dos Santos Oliveira, L, de Lima, DP, da Silva, AA, da Silva, MC, de Souza, SL, Manhães-de-Castro, R. Early weaning programs rats to have a dietary preference for fat and palatable foods in adulthood. Behav Processes. 2011; 86, 75–80.CrossRefGoogle ScholarPubMed
15. Drewett, RF. Oestrous and dioestrous components of the ovarian inhibition on hunger in the rat. Anim Behav. 1973; 21, 772–780.CrossRefGoogle ScholarPubMed
16. Dsilna, A, Christensson, K, Gustafsson, AS, Lagercrantz, H, Alfredsson, L. Behavioral stress is affected by the mode of tube feeding in very low birth weight infants. Clin J Pain. 2008; 24, 447–455.CrossRefGoogle ScholarPubMed
17. Fatehi, M, Fatehi-Hassanabad, Z. Effects of 17beta-estradiol on neuronal cell excitability and neurotransmission in the suprachiasmatic nucleus of rat. Neuropsychopharmacology. 2008; 33, 1354–1364.CrossRefGoogle ScholarPubMed
18. Ferrini, M, Lima, A, De Nicola, AF. Estradiol abolishes autologous down regulation of glucocorticoid receptors in brain. Life Sci. 1995; 57, 2403–2412.CrossRefGoogle ScholarPubMed
19. Gibson, EL. Emotional influences on food choice: sensory, physiological and psychological pathways. Physiol Behav. 2006; 89, 53–61.CrossRefGoogle ScholarPubMed
20. 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 N Y Acad Sci. 2004; 1032, 202–207.CrossRefGoogle ScholarPubMed
21. Halford, JC, Wanninayake, SC, Blundell, JE. Behavioral Satiety Sequence (BSS) for the diagnosis of drug action on food intake. Pharmacol Biochem Behav. 1998; 61, 159–168.CrossRefGoogle ScholarPubMed
22. Hall, WG, Rosenblatt, JS. Development of nutritional control of food intake in suckling rat pups. Behav Biol. 1978; 24, 413–427.CrossRefGoogle ScholarPubMed
23. Hancock, S, Grant, V. Early maternal separation increases symptoms of activity-based anorexia in male and female rats. J Exp Psychol Anim Behav Process. 2009; 35, 394–406.CrossRefGoogle ScholarPubMed
24. Harro, J, Merenakk, L, Nordquist, N, Konstabel, K, Comasco, E, Oreland, L. Personality and the serotonin transporter gene: associations in a longitudinal population-based study. Biol Psychol. 2009; 81, 9–13.CrossRefGoogle Scholar
25. Hofer, MA. Early relationships as regulators of infant physiology and behavior. Acta Paediatr Suppl. 1994; 397, 9–18.CrossRefGoogle ScholarPubMed
26. Husum, H, Mathe, AA. Early life stress changes concentrations of neuropeptide Y and corticotropin-releasing hormone in adult rat brain. Lithium treatment modifies these changes. Neuropsychopharmacology. 2002; 27, 756–764.CrossRefGoogle ScholarPubMed
27. Husum, H, Termeer, E, Mathé, AA, Bolwig, TG, Ellenbroek, BA. Early maternal deprivation alters hippocampal levels of neuropeptide Y and calcitonin-gene related peptide in adult rats. Neuropharmacology. 2002; 42, 798–806.CrossRefGoogle ScholarPubMed
28. Jiménez-Vasquez, PA, Mathé, AA, Thomas, JD, Riley, EP, Ehlers, CL. Early maternal separation alters neuropeptide Y concentrations in selected brain regions in adult rats. Brain Res Dev Brain Res. 2001; 131, 149–152.CrossRefGoogle ScholarPubMed
29. Kennedy, GC, Mitra, J. Spontaneous pseudopregnancy and obesity in the rat. J Physiol. 1963; 166, 419–424.CrossRefGoogle ScholarPubMed
30. Kikusui, T, Nakamura, K, Kakuma, Y, Mori, Y. Early weaning augments neuroendocrine stress responses in mice. Behav Brain Res. 2006; 175, 96–103.CrossRefGoogle ScholarPubMed
31. 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, 587–594.CrossRefGoogle ScholarPubMed
32. 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.CrossRefGoogle ScholarPubMed
33. Ladd, CO, Huot, RL, Thrivikraman, KV, Nemeroff, CB, Meaney, MJ, Plotsky, PM. Long-term behavioral and neuroendocrine adaptations to adverse early experience. Prog Brain Res. 2000; 122, 81–103.CrossRefGoogle ScholarPubMed
34. Lehmann, J, Stöhr, T, Feldon, J. Long-term effects of prenatal stress experiences and postnatal maternal separation on emotionality and attentional processes. Behav Brain Res. 2000; 107, 133–144.CrossRefGoogle ScholarPubMed
35. Liu, D, Diorio, J, Day, JC, Francis, DD, Meaney, MJ. Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nat Neurosci. 2000; 3, 799–806.CrossRefGoogle ScholarPubMed
36. Lopes de Souza, S, Orozco-Solis, R, Grit, I, Manhães de Castro, R, Bolaños-Jiménez, R. Perinatal protein restriction reduces the inhibitory action of serotonin on food intake. Eur J Neurosci. 2008; 27, 1400–1408.CrossRefGoogle ScholarPubMed
37. Makimura, H, Mizuno, TM, Isoda, F, Beasley, J, Silverstein, JH, Mobbs, CV. Role of glucocorticoids in mediating effects of fasting and diabetes on hypothalamic gene expression. BMC Physiol. 2003; 3, 5.CrossRefGoogle ScholarPubMed
38. Maniam, J, Morris, MJ. Long-term postpartum anxiety and depression-like behavior in mother rats subjected to maternal separation are ameliorated by palatable high fat diet. Behav Brain Res. 2010; 208, 72–79.CrossRefGoogle ScholarPubMed
39. Matthews, K, Wilkinson, LS, Isoda, F, Beasley, J, Silverstein, JH, Mobbs, CV. Repeated maternal separation of preweanling rats attenuates behavioral responses to primary and conditioned incentives in adulthood. Physiol Behav. 1996; 59, 99–107.CrossRefGoogle ScholarPubMed
40. Morimoto, M, Morita, N, Ozawa, H, Yokoyama, K, Kawata, M. Distribution of glucocorticoid receptor immunoreactivity and mRNA in the rat brain: an immunohistochemical and in situ hybridization study. Neurosci Res. 1996; 26, 235–269.CrossRefGoogle Scholar
41. Ogawa, T, Mikuni, M, Kuroda, Y, Muneoka, K, Mori, KJ, Takahashi, K. Periodic maternal deprivation alters stress response in adult offspring: potentiates the negative feedback regulation of restraint stress-induced adrenocortical response and reduces the frequencies of open field-induced behaviors. Pharmacol Biochem Behav. 1994; 49, 961–967.CrossRefGoogle ScholarPubMed
42. Ohta, H, Honma, S, Abe, H, Honma, K. Effects of nursing mothers on rPer1 and rPer2 circadian expressions in the neonatal rat suprachiasmatic nuclei vary with developmental stage. Eur J Neurosci. 2002; 15, 1953–1960.CrossRefGoogle ScholarPubMed
43. Ohta, H, Honma, S, Abe, H, Honma, K. Periodic absence of nursing mothers phase-shifts circadian rhythms of clock genes in the suprachiasmatic nucleus of rat pups. Eur J Neurosci. 2003; 17, 1628–1634.CrossRefGoogle ScholarPubMed
44. Orozco-Sólis, R, Lopes de Souza, S, Barbosa Matos, RJ, et al. Perinatal undernutrition-induced obesity is independent of the developmental programming of feeding. Physiol Behav. 2009; 96, 481–492.CrossRefGoogle ScholarPubMed
45. Orozco-Solís, R, Matos, RJ, Lopes de Souza, S, et al. Nutritional programming in the rat is linked to long-lasting changes in nutrient sensing and energy homeostasis in the hypothalamus. PLoS One. 2010; 5, e13537.CrossRefGoogle ScholarPubMed
46. Orozco-Solis, R, Matos, RJ, Lopes de Souza, S, et al. Perinatal nutrient restriction induces long-lasting alterations in the circadian expression pattern of genes regulating food intake and energy metabolism. Int J Obes (Lond). 2011; 35, 990–1000.CrossRefGoogle ScholarPubMed
47. Patchev, VK, Hayashi, S, Orikasa, C, Almeida, OF. Implications of estrogen-dependent brain organization for gender differences in hypothalamo-pituitary-adrenal regulation. FASEB J. 1995; 9, 419–423.CrossRefGoogle ScholarPubMed
48. Peiffer, A, Barden, N. Estrogen-induced decrease of glucocorticoid receptor messenger ribonucleic acid concentration in rat anterior pituitary gland. Mol Endocrinol. 1987; 1, 435–440.CrossRefGoogle ScholarPubMed
49. Plotsky, PM, Meaney, MJ. Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Brain Res Mol Brain Res. 1993; 18, 195–200.CrossRefGoogle ScholarPubMed
50. Ponsalle, P, Srivastava, LS, Uht, RM, White, JD. Glucocorticoids are required for food deprivation-induced increases in hypothalamic neuropeptide Y expression. J Neuroendocrinol. 1992; 4, 585–591.CrossRefGoogle ScholarPubMed
51. Presl, J, Horsky, J, Herzmann, J, Mikulás, I, Henzl, M. Fluorimetric estimation of oestrogen in the blood of infant female rats. J Endocrinol. 1987; 38, 201–202.CrossRefGoogle Scholar
52. Ruedi-Bettschen, D, Feldon, J, et al. Circadian- and temperature-specific effects of early deprivation on rat maternal care and pup development: short-term markers for long-term effects? Dev Psychobiol. 2004; 45, 59–71.CrossRefGoogle ScholarPubMed
53. Schroeder, M, Moran, TH, Weller, A. Attenuation of obesity by early-life food restriction in genetically hyperphagic male OLETF rats: peripheral mechanisms. Horm Behav. 2010; 57, 455–462.CrossRefGoogle ScholarPubMed
54. Silveira, PP, Portella, AK, Clemente, Z, et al. Neonatal handling alters feeding behavior of adult rats. Physiol Behav. 2004; 80, 739–745.CrossRefGoogle ScholarPubMed
55. Simon, CE, Pryce, JG, Roff, LL, Klemmack, D. Secondary traumatic stress and oncology social work: protecting compassion from fatigue and compromising the worker’s worldview. J Psychosoc Oncol. 2005; 23, 1–14.CrossRefGoogle ScholarPubMed
56. Stephan, FK, Zucker, I. Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proc Natl Acad Sci USA. 1972; 69, 1583–1586.CrossRefGoogle ScholarPubMed
57. Suchecki, D, Tufik, S. Long-term effects of maternal deprivation on the corticosterone response to stress in rats. Am J Physiol. 1997; 273(Pt 2), R1332–R1338.Google ScholarPubMed
58. Takahashi, K, Deguchi, T. Entrainment of the circadian rhythms of blinded infant rats by nursing mothers. Physiol Behav. 1983; 31, 373–378.CrossRefGoogle ScholarPubMed
59. Takamata, A, Torii, K, Miyake, K, Morimoto, K. Chronic oestrogen replacement in ovariectomised rats attenuates food intake and augments c-Fos expression in the suprachiasmatic nucleus specifically during the light phase. Br J Nutr. 2011; 106, 1283–1289.CrossRefGoogle ScholarPubMed
60. Tonjes, R, Hecht, K, Brautzsch, M, Lucius, R, Dörner, G. Behavioural changes in adult rats produced by early postnatal maternal deprivation and treatment with choline chloride. Exp Clin Endocrinol. 1986; 88, 151–157.CrossRefGoogle ScholarPubMed
61. Torres-Farfan, C, Mendez, N, Abarzua-Catalan, L, Vilches, N, Valenzuela, GJ, Seron-Ferre, M. A circadian clock entrained by melatonin is ticking in the rat fetal adrenal. Endocrinology. 2011; 152, 1891–1900.CrossRefGoogle ScholarPubMed
62. Valenstein, ES, Kakolewski, JW, Cox, VC. Sex differences in taste preference for glucose and saccharin solutions. Science. 1967; 156, 942–943.CrossRefGoogle ScholarPubMed
63. Varma, M, Meguid, MM, Hammond, WG, Gleason, JR. Lack of influence of hysterectomy on meal size and meal number in Fischer-344 rats. Physiol Behav. 1999; 66, 559–565.CrossRefGoogle ScholarPubMed
64. Vida, B, Hrabovszky, E, Kalamatianos, T, Coen, CW, Liposits, Z, Kalló, I. Oestrogen receptor alpha and beta immunoreactive cells in the suprachiasmatic nucleus of mice: distribution, sex differences and regulation by gonadal hormones. J Neuro Endocrinol. 2008; 20, 1270–1277.Google ScholarPubMed
65. Viswanathan, N. Maternal entrainment in the circadian activity rhythm of laboratory mouse (C57BL/6 J). Physiol Behav. 1999; 68, 157–162.CrossRefGoogle Scholar
66. Wade, GN. Gonadal hormones and behavioral regulation of body weight. Physiol Behav. 1972; 8, 523–534.CrossRefGoogle ScholarPubMed
67. Wade, GN. Some effects of ovarian hormones on food intake and body weight in female rats. J Comp Physiol Psychol. 1975; 88, 183–193.CrossRefGoogle ScholarPubMed
68. Ward, IL, Renz, FJ. Consequences of perinatal hormone manipulation on the adult sexual behavior of female rats. J Comp Physiol Psychol. 1972; 78, 349–355.CrossRefGoogle ScholarPubMed
69. Weiser, MJ, Handa, RJ. Estrogen impairs glucocorticoid dependent negative feedback on the hypothalamic-pituitary-adrenal axis via estrogen receptor alpha within the hypothalamus. Neuroscience. 2009; 159, 883–895.CrossRefGoogle ScholarPubMed
70. Yokosuka, M, Kalra, PS, Kalra, SP. Inhibition of neuropeptide Y (NPY)-induced feeding and c-Fos response in magnocellular paraventricular nucleus by a NPY receptor antagonist: a site of NPY action. Endocrinology. 1999; 140, 4494–4500.CrossRefGoogle ScholarPubMed
71. Zakrzewska, KE, Cusin, I, Stricker-Krongrad , A, et al. Induction of obesity and hyperleptinemia by central glucocorticoid infusion in the rat. Diabetes. 1999; 48, 365–370.CrossRefGoogle ScholarPubMed