Artificial feeding synchronizes behavioral, hormonal, metabolic and neural parameters in mother-deprived neonatal rabbit pups

European Journal of Neuroscience

Volumn 34, Issue 11, 2011, Pages 1807-1816

  Morgado, Elvira ^a   Juárez, Claudia ^a   Melo, Angel I ^b   Domínguez, Belisario ^a   Lehman, Michael N ^c   Escobar, Carolina ^d   Meza, Enrique ^a   Caba, Mario ^a  

^a UNIVERSIDAD VERACRUZANA   (Mexico)

^b DEPARTAMENTO DE FÍSICA   (Mexico)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Anticipatory arousal; Clock genes; Corticosterone; FOS; Synchronization by food

Indexed keywords

CORTICOTROPIN; PER1 PROTEIN; PROTEIN C FOS;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ARTIFICIAL FEEDING; CELL SYNCHRONIZATION; CIRCADIAN RHYTHM; CONTROLLED STUDY; FEEDING BEHAVIOR; FEMALE; FOOD INTAKE; GLUCOSE BLOOD LEVEL; LOCOMOTION; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; RABBIT; SUPRACHIASMATIC NUCLEUS; SUPRAOPTIC NUCLEUS; TUBEROMAMMILLARY NUCLEUS;

ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; BLOOD GLUCOSE; CIRCADIAN RHYTHM; CORTICOSTERONE; FEEDING BEHAVIOR; FEMALE; HYPOTHALAMUS; LACTATION; MATERNAL DEPRIVATION; MOTOR ACTIVITY; PERIOD CIRCADIAN PROTEINS; PROTO-ONCOGENE PROTEINS C-FOS; RABBITS;

EID: 82455212796     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2011.07898.x     Document Type: Article

References (59)

1. Abe, M., Herzog, E.D., Yamazaki, S., Straume, M., Tei, H., Sakaki, Y., Menaker, M. & Block, G.D. (2002) Circadian rhythms in isolated brain regions. J. Neurosci., 22, 350-356.
2. Acosta-Galvan, G., Yi, C.X., van der Vliet, J., Jhamandas, J.H., Panula, P., Angeles-Castellanos, M., Basualdo, M.d.C., Escobar, C. & Buijs, R.M. (2011) Interaction between hypothalamic dorsomedial nucleus and the suprachiasmatic nucleus determines intensity of food anticipatory behavior. Proc. Natl. Acad. Sci. USA, 108, 5813-5818.
3. Allingham, K., von Salderm, C., Brennan, P.A., Distel, H. & Hudson, R. (1998) Endogenous expression of c-Fos in hypothalamic nuclei of neonatal rabbits coincides with their circadian pattern of suckling-associated arousal. Brain Res., 783, 210-218.
4. Angeles-Castellanos, M., Aguilar-Roblero, R. & Escobar, C. (2003) c-Fos expression in hypothalamic nuclei of food-entrained rats. Am. J. Physiol. Regul. Integr. Comp. Physiol., 286, R158-R165.
5. Antle, M.C. & Silver, R. (2009) Neural basis of timing and anticipatory behaviors. Eur. J. Neurosci., 30, 1643-1649.
6. Beierle, E.A., Chen, M.K., Hartwich, J.E., Iyengar, M., Dai, W., Li, N., Demarco, V. & Neu, J. (2004) Artificial rearing of mouse pups: development of a mouse pup in a cup model. Pediatr. Res., 56, 250-255.
7. Brecchia, G., Bonanno, A., Dall'Aglio, C., Mercati, F., Zerani, M., DiGrigoli, A. & Boiti, C. (2009) Neuroendocrine responses in neonatal mother-deprived rabbits. Brain Res., 1304, 105-112.
8. Broekhuizen, S. & Mulder, J.L. (1983) Differences and similarities in nursing behaviour of hares and rabbits. Acta Zool. Fenn., 174, 61-63.
9. Brummelte, S., Schmidt, K.L., Taves, M.D., Soma, K.K. & Galea, L.A. (2010) Elevated corticosterone levels in stomach milk, serum, and brain of male and female offspring after maternal corticosterone treatment in the rat. Dev. Neurobiol., 70, 714-725.
10. Caba, M. & González-Mariscal, G. (2009) The rabbit pup, a natural model of nursing anticipatory activity. Eur. J. Neurosci., 30, 1697-1706.
11. Caba, M., Rovirosa, M.J. & Silver, R. (2003) Suckling and genital stroking induces Fos expresion in hypothalamic oxytocinergic neurons of rabbit pups. Brain Res. Dev. Brain Res., 143, 119-128.
12. Caba, M., Tovar, A., Silver, R., Morgado, E., Meza, E., Zavaleta, Y. & Juárez, C. (2008) Nature's food anticipatory experiment: entrainment of locomotor behavior, suprachiasmatic and dorsomedial hypothalamic nuclei by suckling in rabbit pups. Eur. J. Neurosci., 27, 432-443.
13. Caldelas, I., González, B., Montúfar-Chaveznava, R. & Hudson, R. (2009) Endogenous clock gene expression in the suprachiasmatic nuclei of previsual newborn rabbits is entrained by nursing. Dev. Neurobiol., 69, 47-59.
14. Catalani, A., Marinelli, M., Scaccianoce, S., Nicolai, R., Muscolo, L.A., Porcu, A., Korányi, L., Piazza, P.V. & Angelucci, L. (1993) Progeny of mothers drinking corticosterone during lactation has lower stress-induced corticosterone secretion and better cognitive performance. Brain Res., 624, 209-215.
15. Chatterjee, D., Chatterjee-Chakraborty, M., Rees, S., Cauchi, J., de Medeiros, C.B. & Fleming, A.S. (2007) Maternal isolation alters the expression of neural proteins during development: 'stroking' stimulation reverses these effects. Brain Res., 1158, 11-27.
16. Conover, W.J. & Iman, R.L. (1981) Rank transformation as a bridge between parametric and nonparametric statistics. Am. Stat., 35, 132-133.
17. Damiola, F., Minh, N.L., Preitner, N., Kornmann, B., Fleury-Olela, F. & Schibler, U. (2000) Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev., 14, 2950-2961.
18. Díaz-Muñoz, M., Vázquez-Martínez, O., Aguilar-Roblero, R. & Escobar, C. (2000) Anticipatory changes in liver metabolism and entrainment of insulin, glucagon and corticosterone in food-restricted rats. Am. J. Physiol. Regul. Integr. Comp. Physiol., 279, 2048-2056.
19. Flanagan, L.M., Olson, B.R., Sved, A.F., Verbalis, J.G. & Stricker, E.M. (1992) Gastric motility in conscious rats given oxytocin and an oxytocin antagonist centrally. Brain Res., 578, 256-260.
20. Gerhard, L. (1968) Atlas of the Mes- and Diencephalon of the Rabbit. Springer-Verlag, Berlín.
21. Girgis, M. & Shih-Chang, W. (1981) A New Stereotaxic Atlas of the Rabbit Brain. W. H. Green, St Louis.
22. Granados-Fuentes, D., Tseng, A. & Herzog, E.D. (2006) A circadian clock in the olfactory bulb controls olfactory responsivity. J. Neurosci., 26, 12219-12225.
23. Grosvenor, C.E., Picciano, M.F. & Baumrucker, C.R. (1993) Hormones and growth factors in milk. Endocr. Rev., 14, 710-728.
24. Hara, R., Wan, K., Wakamatsu, H., Aida, R., Moriya, T., Akiyama, M. & Shibata, S. (2001) Restricted feeding entrains liver clock without participation of the suprachiasmatic nucleus. Genes Cells, 6, 269-278.
25. Hernández-Campos, O., Montúfar-Chaveznava, R. & Caldelas, I.. (2011). Do newborn rabbits bearing suprachiasmatic nuclei lesions anticipate to nursing? 3rd World Congress of Chronobiology. Puebla, México.
26. Honma, K., Noe, Y., Honma, S., Katsuno, Y. & Hiroshighe, T. (1992) Roles of paraventricular catecholamines in feeding-associated corticosterone rhythm in rats. Am. J. Physiol., 25, E948-E965.
27. Hudson, R. & Distel, H. (1989) Temporal pattern of suckling in rabbit pups: a model of circadian synchrony between mother and young. In Reppert, S.M. (Ed.), Development of Circadian Rhythmicity and Photoperiodism in Mammals. Perinatology Press, Ithaca, NY, pp. 83-102.
28. Inzunza, O., Serón-Ferré, M.J., Bravo, H. & Torrealba, F. (2000) Tuberoammillary nucleus activation anticipates feeding under a restricted schedule in rats. Neurosci. Lett., 293, 139-142.
29. Jilge, B. (1993) The ontogeny of circadian rhythms in the rabbit. J. Biol. Rhythms, 8, 247-260.
30. Jilge, B. (1995) Ontogeny of the rabbit's rhythms without an external zeitgeber. Physiol. Behav., 58, 131-140.
31. Jilge, B., Kuhnt, B., Landerer, W. & Rest, S. (2000) Circadian thermoregulation in suckling rabbit pups. J. Biol. Rhythms, 15, 329-335.
32. Krieger, D. (1974) Food and water restriction shifts corticosterone, temperature, activity and brain amine periodicity. Endocrinology, 95, 1195-1201.
33. Kriegsfeld, L.J. & Silver, R. (2006) The regulation of neuroendocrine function: timing is everything. Horm. Behav., 49, 557-574.
34. Kriegsfeld, L.J., Korets, R. & Silver, R. (2003) Expression of the circadian clock gene Period1 in neuroendocrine cells: an investigation using mice with a Per1::GFP transgene. Eur. J. Neurosci., 17, 212-220.
35. Ladd, C.O., Huot, R.L., Thrivikraman, K.V., Nemeroff, C.B. & Plotsky, P.M. (2004) Long term adaptations in glucocorticoid receptor and mineralocorticoid receptor mRNA and negative feedback on the hypothalamo-pituitary-adrenal axis following neonatal maternal separation. Biol. Psychiatry, 55, 367-375.
36. Melo, A.I., Hernández-Curiel, M. & Hoffman, K.L. (2009) Maternal and peer contact during the postnatal period participate in the normal development of maternal aggression, maternal behavior, and the behavioral response to novelty. Behav. Brain Res., 201, 14-21.
37. Messer, M., Thoman, E.B., Galofre, A., Dallman, T. & Dallman, P.R. (1969) Artificial feeding of infant rats by continuous infusion. J. Nutr., 98, 404-410.
38. Meza, E., Juárez, C., Morgado, E., Zavaleta, Y. & Caba, M. (2008) Brief daily suckling shifts locomotor behavior and induces PER1 protein in paraventricular and supraoptic nuclei, but not in the suprachiasmatic nucleus, of rabbit does. Eur. J. Neurosci., 28, 1394-1403.
39. Meza, E., Waliszewski, S.M. & Caba, M. (2011) Circadian nursing induces PER1 protein in neuroendocrine tyrosine hydroxylase neurons in the rabbit doe. J. Neuroendocrinol., 23, 472-480.
40. Mistlberger, R.E. (1994) Circadian food-anticipatory activity: formal models and physiological mechanisms. Neurosci. Biobehav. Rev., 18, 171-195.
41. Moberg, G.P., Bellinger, L.L. & Mendel, V.E. (1975) Effect of meal feeding on daily rhythms of plasma corticosterone and growth hormone in the rat. Neuroendocrinology, 19, 160-169.
42. Morgado, E., Gordon, M.K., Minana-Solis, M.d.C., Meza, E., Levine, S., Escobar, C. & Caba, M. (2008) Hormonal and metabolic rhythms associated with the daily scheduled nursing in rabbit pups. Am. J. Physiol. Regul. Integr. Comp. Physiol., 295, R690-R695.
43. Morgado, E., Meza, E., Gordon, M.K., Pau, K.Y., Juárez, C. & Caba, M. (2010) Persistence of hormonal and metabolic rhythms during fasting in 7-to 9-day-old rabbits entrained by nursing during night. Horm. Behav., 58, 465-472.
44. Olszewski, P.K., Klockars, A., Schiöth, H.B. & Levine, A.S. (2010) Oxytocin as feeding inhibitor: maintaining homeostasis in consumatory behavior. Pharmacol. Biochem. Behav., 97, 47-54.
45. Pongrácz, P. & Altbäcker, V. (2003) Arousal, but not nursing, is necessary to elicit a decreased fear reaction toward humans in rabbit pups. Dev. Psychobiol., 43, 192-199.
46. Renaud, L.P., Tang, M., McCann, M.J., Stricker, E.M. & Verbalis, J.G. (1987) Cholecystokinin and gastric distension activate oxytocinergic cells in rat hypothalamus. Am. J. Physiol., 253, R661-R665.
47. Rovirosa, M.J., Levine, S., Gordon, M.K. & Caba, M. (2005) Circadian rhythm of corticosterone secretion in the neonatal rabbit. Brain Res. Dev. Brain Res., 8, 92-96.
48. Rowe, S.A. & Kennaway, D.J. (2002) Melatonin in rat milk and the likelihood of its role in postnatal maternal entrainment of rhythms. Am. J. Physiol. Regul. Integr. Comp. Physiol., 282, R797-R804.
49. Schuh, D., Hoy, S. & Selzer, D.. (2004) Vocalization of rabbit pups in the mother-young relationship. Proceedings of 8th World Rabbit Congress, Puebla, México, pp. 1266-1270.
50. Stephan, F.K. (2002) The 'other' circadian system: food as a zeitgeber. J. Biol. Rhythms, 17, 284-292.
51. Stephan, F.K., Swann, J.M. & Sisk, C.L. (1979) Anticipation of 24hr feeding schedules in rats with lesions of the suprachiasmatic nucleus. Behav. Neural Biol., 25, 345-363.
52. Suckow, M.A. & Douglas, F.A. (1997) The Laboratory Rabbit, 2nd edn. CRC Press, Boca Raton, Florida.
53. Szeto, A., Gonzales, J.A., Spitzer, S.B., Levine, J.E., Zaias, P.G., Saab, N., Schneiderman, N. & McCabe, P.M. (2004) Circulating levels of glucocorticoid hormones in WHHL and NZW rabbits: circadian cycle and response to repeated social encounter. Psychoneuroendocrinology, 29, 861-866.
54. Valdés, J.L., Farías, P., Ocampo-Garcés, A., Cortés, N., Serón-Ferré, M. & Torrealba, F. (2005) Arousal and differential Fos expression in histaminergic neurons of the ascending arousal system during a feeding-related motivated behaviour. Eur. J. Neurosci., 21, 1931-1942.
55. Verbalis, J.G., Blackburn, R.E., Hoffman, G.E. & Stricker, E.M. (1995) Establishing behavioral and physiological functions of central oxytocin: insights from studies of oxytocin and ingestive behaviors. Adv. Exp. Med. Biol., 395, 209-225.
56. Verwey, M. & Amir, S. (2009) Food-entrainable circadian oscillators in the brain. Eur. J. Neurosci., 30, 1650-1657.
57. Wakamatsu, H., Yoshinobu, Y., Aida, R., Moriya, T., Akiyama, M. & Shibata, S. (2001) Restricted-feeding-induced anticipatory activity rhythm is associated with a phase-shift of the expression of mPer1 and mPer2 mRNA in the cerebral cortex and hippocampus but not in the suprachiasmatic nucleus of mice. Eur. J. Neurosci., 13, 1190-1196.
58. Withworth, N.S. & Grosvenor, C.E. (1978) Transfer of milk prolactin to the plasma of neonatal rats by intestinal absorption. J. Endocrinol., 79, 191-199.
59. Zarrow, M.X., Denenberg, V.H. & Anderson, C. (1965) Rabbit: frequency of suckling in the pup. Science, 150, 1835-1836.