Determining the period, phase and anticipatory component of activity and temperature patterns in newborn rabbits that were maintained under a daily nursing schedule and fasting conditions

Physiology and Behavior

Volumn 106, Issue 5, 2012, Pages 587-596

  Trejo Muñoz, Lucero ^a   Navarrete, Erika ^a   Montúfar Chaveznava, Rodrigo ^b   Caldelas, Ivette ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b Instituto de Ciencia y Tecnología Del Distrito Federal   (Mexico)

Author keywords

Anticipation of nursing; Body temperature; Circadian rhythms; Development; Locomotor activity; Time series analysis

Indexed keywords

ALGORITHM; ARTICLE; BODY TEMPERATURE; CIRCADIAN RHYTHM; FEMALE; LOCOMOTION; NEWBORN; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RABBIT; TEMPERATURE;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BODY TEMPERATURE; CIRCADIAN RHYTHM; FASTING; FEEDING BEHAVIOR; LACTATION; MOTOR ACTIVITY; RABBITS;

EID: 84860386101     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2012.04.005     Document Type: Article

References (70)

1. Pittendrigh C. Circadian systems: general perspective. Handbook of behavioral neurobiology: biological rhythms 1981, 57-80. Plenum Press, New York. J. Aschoff (Ed.).
2. Weaver D.R. The suprachiasmatic nucleus: a 25-year retrospective. J Biol Rhythms 1998, 13:100-112.
3. Reppert S.M., Weaver D.R. Molecular analysis of mammalian circadian rhythms. Annu Rev Physiol 2001, 63:647-676.
4. Reppert S.M., Weaver D.R. Coordination of circadian timing in mammals. Nature 2002, 418:935-941.
5. Reppert S.M., Schwartz W.J. Maternal coordination of the foetal biological clock in utero. Science 1983, 220:969-971.
6. Shibata S., Moore R.Y. Development of neuronal activity in the rat suprachiasmatic nucleus. Brain Res 1987, 431:311-315.
7. Reppert S.M., Uhl G.R. Vasopressin messenger ribonucleic acid in supraoptic and suprachiasmatic nuclei: appearance and circadian regulation during development. Endocrinology 1987, 120:2483-2487.
8. Shimomura H., Moriya T., Sudo M., Wakamatsu H., Akiyama M., Miyake Y., et al. Differential daily expression of Per1 and Per2 mRNA in the suprachiasmatic nucleus of foetal and early postnatal mice. Eur J Neurosci 2001, 13:687-693.
9. Sládek M., Sumová A., Kováčiková Z., Bendová Z., Laurinová K., Illnerová H. Insight into molecular core clock mechanism of embryonic and early postnatal rat suprachiasmatic nucleus. Proc Natl Acad Sci U S A 2004, 101:6231-6236.
10. Shibata S., Moore R.Y. Development of a foetal circadian rhythm after disruption of the maternal circadian system. Brain Res 1988, 469:313-317.
11. Reppert S.M. Interaction between the circadian clocks of mother and fetus. Ciba Found Symp 1995, 183:198-207.
12. Torres-Farfan C., Mendez N., Abarzua-Catalan L., Vilches N., Valenzuela G.J., Seron-Ferre M. A circadian clock entrained by melatonin is ticking in the rat fetal adrenal. Endocrinology 2011, 152:1891-1900.
13. Takahashi K., Deguchi T. Entrainment of the circadian rhythms of blinded infant rats by nursing mothers. Physiol Behav 1983, 31:373-378.
14. 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.
15. 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.
16. Ohta H., Xu S., Moriya T., Iigo M., Watanabe T., Nakahata N., et al. Maternal feeding controls fetal biological clock. PLoS One 2008, 3:e2601.
17. Hudson R., Distel H. Temporal pattern of suckling in rabbit pups: a model of circadian synchrony between mother and young. Research in perinatal medicine (IX), development of circadian rhythmicity and photoperiodism in mammals 1989, 83-102. Perinatology Press, New York. S.M. Reppert (Ed.).
18. Jilge B., Hudson R. Diversity and development of circadian rhythms in the European rabbit. Chronobiol Int 2001, 18:1-26.
19. Caldelas I., Chimal-Monroy J., Martínez-Gómez M., Hudson R. Non-photic circadian entrainment in mammals: a brief review and proposal for study during development. Biol Rhythm Res 2005, 36:23-37.
20. Caldelas I., Montúfar-Chaveznava R., Martínez-Gómez M., Hudson R. Non-photic entrainment of the circadian system in mammals: a developmental approach. Comparative aspects of circadian rhythms 2008, 143-158. Research Signpost, Kerala. M.L. Fanjul-Moles, R. Aguilar-Roblero (Eds.).
21. Deutsch J.A. Nest building behaviour of domestic rabbits under semi-natural conditions. Br J Anim Behav 1957, 5:53-54.
22. Zarrow M.X., Denenberg V.H., Anderson C.O. Rabbit: frequency of suckling in the pup. Science 1965, 150:1835-1836.
23. Lincoln D.W. Does a mechanism of negative feedback determine the intermittent release of oxytocin during suckling?. J Endocrinol 1974, 60:193-194.
24. Schley V.P. Die künstliche aufzucht von kaninchen unter verwendung von mittelkettigen trigliceriden (MKT) - erste ergebnisse. Berl Münch Tierärztl Wochenschr 1976, 89:32-35.
25. Hudson R., Distel H. The pattern of behaviour of rabbit pups in the nest. Behaviour 1982, 79:255-271.
26. Jilge B. The ontogeny of circadian rhythms in the rabbit. J Biol Rhythms 1993, 8:247-260.
27. Caba M., Tovar A., Silver R., Mogado E., Meza E., Zavaleta Y., et al. Nature's food anticipatory experiment: entrainment of locomotor behavior, suprachiasmatic and dorsomedial hypothalamic nuclei by suckling in rabbit pups. Eur J Neurosci 2008, 27:432-443.
28. Jilge B., Kuhnt B., Landerer W., Rest S. Circadian thermoregulation in suckling rabbit pups. J Biol Rhythms 2000, 15:329-335.
29. Jilge B., Kuhnt B., Landerer W., Rest S. Circadian temperature rhythms in rabbit pups and in their does. Lab Anim 2001, 35:364-373.
30. Caldelas I., González B., Montúfar-Chaveznava R., Hudson R. Endogenous clock gene expression in the suprachiasmatic nuclei of previsual newborn rabbits is entrained by nursing. Dev Neurobiol 2009, 69:47-59.
31. Escobar C., Hudson R., Martínez-Gómez M., Aguilar-Roblero R. Metabolic correlates of the circadian pattern of suckling-associated arousal in young rabbits. J Comp Physiol A 2000, 186:33-38.
32. Rovirosa M.J., Levine S., Gordon M.K., Caba M. Circadian rhythm of corticosterone secretion in the neonatal rabbit. Brain Res Dev Brain Res 2005, 158:92-96.
33. Caldelas I., Tejadilla D., González B., Montúfar R., Hudson R. Diurnal pattern of clock gene expression in the hypothalamus of the newborn rabbit. Neuroscience 2007, 144:395-401.
34. Mistlberger R.E. Circadian food-anticipatory activity: formal models and physiological mechanisms. Neurosci Biobehav Rev 1994, 18:171-195.
35. Moore-Ede M.C., Sulzman F.M., Fuller C.A. A physiological system measuring time. The clocks that time us. Physiology of the circadian timing system 1982, 21-39. Harvard University Press, Cambridge. M.C. Moore-Ede, F.M. Sulzman, C.A. Fuller (Eds.).
36. Johnston P.G., Zucker I. Lability and diversity of circadian rhythms of cotton rats Sigmodon hispidus. Am J Physiol 1983, 244:R338-R346.
37. Cohen R., Smale L., Kronfeld-Schor N. Plasticity of circadian activity and body temperature rhythms in golden spiny mice. Chronobiol Int 2009, 26:430-446.
38. Challet E., Pitrosky B., Sicard B., Malan A., Pévet P. Circadian organization in a diurnal rodent, Arvicanthis ansorgei Thomas 1910: chronotypes, responses to constant lighting conditions, and photoperiodic changes. J Biol Rhythms 2002, 17:52-64.
39. Enright J.T. Data analysis. Handbook of behavioural neurobiology. Vol. 4 Biological rhythms 1981, 21-39. Plenum Press, New York. J. Aschoff (Ed.).
40. Hull D. Oxygen consumption and body temperature of new-born rabbits and kittens exposed to cold. J Physiol 1965, 177:192-202.
41. Gilbert C., Blanc S., Giroud S., Trabalon M., Le Maho Y., Perret M., et al. Role of huddling on the energetic of growth in a newborn altricial mammal. Am J Physiol Regul Integr Comp Physiol 2007, 293:R867-R876.
42. Bautista A., Drummond H., Martínez-Gómez M., Hudson R. Thermal benefit of sibling presence in the newborn rabbit. Dev Psychobiol 2003, 43:208-215.
43. Tauber H., Waehneldt T.V., Neuhoff V. Myelination in rabbit optic nerves is accelerated by artificial eye opening. Neurosci Lett 1980, 16:235-238.
44. Donoho D.L. Wavelet shrinkage and W.V.D. - a ten-minute tour. Progress in wavelet analysis and applications 1993, 109-128. Editions Frontieres, Gif-sur-Yvette. Y. Meyer, Roques (Eds.).
45. Donoho D.L., Johnstone I.M. Ideal spatial adaptation via wavelet shrinkage. Biometrika 1994, 81:425-455.
46. Coifman R.R., Donoho D.L. Translation-invariant de-noising. Wavelets and statistics. Lecture Notes in Statistics 1995, 125-150. Springer Verlag, New York. A. Antoniadis, G. Oppenheim (Eds.).
47. Anscombe F.J. The transformation of Poisson, binomial and negative-binomial data. Biometrika 1948, 35:246-254.
48. Mallat S. A wavelet tour of signal processing 1999, Academic Press, San Diego. 2nd ed.
49. Ziemer R.E., Tranter W.H., Fannin D.R. Signals and systems: continuous and discrete 1998, Prentice Hall Press, New Jersey. 4th ed.
50. Savitzky A., Golay M.J.E. Smoothing and differentiation of data by simplified least squares procedures. Anal Chem 1964, 36:1627-1639.
51. Oakley D.A., Plotkin H.C. Ontogeny of spontaneous locomotor activity in rabbit, rat, and guinea pig. J Comp Physiol Psychol 1975, 89:267-273.
52. Smith G.K., Anderson V. Effects of maternal isolation on the development of activity rhythms in infant rats. Physiol Behav 1984, 33:751-756.
53. Anderson V.N., Smith G.K. Effects of feeding and light cycles on activity rhythms of maternally isolated rat pups. Physiol Behav 1987, 39:169-181.
54. Mirmiran M., Bernardo L., Jenkins S.L., Ma X.H., Brenna J.T., Nathanielsz P.W. Growth, neurobehavioral and circadian rhythm development in newborn baboons. Pediatr Res 2001, 49:673-677.
55. Spiers D.E., Adair E.R. Ontogeny of homeothermy in the immature rat: metabolic and thermal responses. J Appl Physiol 1986, 60:1190-1197.
56. Schmidt I., Barone A., Carlisle H.J. Diurnal cycle of core temperature in huddling, week-old rat pups. Physiol Behav 1986, 37:105-109.
57. Schmidt I., Kaul R., Heldmaier G. Thermoregulation and diurnal rhythms in 1-week-old rat pups. Can J Physiol Pharmacol 1987, 65:1355-1364.
58. Alberts J.R. Huddling by rat pups: ontogeny of individual and group behavior. Dev Psychobiol 2007, 49:22-32.
59. Kleitman N., Satinoff E. Thermoregulatory behavior in rat pups from birth to weaning. Physiol Behav 1982, 29:537-541.
60. Pacheco-Cobos L., Rosetti M., Distel H., Hudson R. To stay or not to stay: the contribution of tactile and thermal cues to coming to rest in newborn rabbits. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2003, 189:383-389.
61. Teicher M.H., Flaum L.E. Ontogeny of ultradian and nocturnal activity rhythms in the isolated albino rat. Dev Psychobiol 1979, 12:441-454.
62. Davis F.C., Reppert S.M. Development of mammalian rhythms. Handbook of behavioral neurobiology: circadian clocks 2001, 247-290. Plenum Publishing, New York. J.T. Takahashi, F.W. Turek, R.Y. Moore (Eds.).
63. Rivkees S.A. Developing circadian rhythmicity. Basic and clinical aspects. Pediatr Clin North Am 1997, 44:467-487.
64. Nuesslein-Hildesheim B., Imai-Matsumura K., Döring H., Schmidt I. Pronounced juvenile circadian core temperature rhythms exist in several strains of rats but not in rabbits. J Comp Physiol B 1995, 165:13-17.
65. Melanie E., Kittrell W., Satinoff E. Development of the circadian rhythm of body temperature in rats. Physiol Behav 1986, 38:99-104.
66. Jilge B. Ontogeny of the rabbit's circadian rhythms without an external zeitgeber. Physiol Behav 1995, 58:131-140.
67. Morgado E., Meza E., Gordon M.K., Pau F.K., Juárez C., Caba M. Persistence of hormonal and metabolic rhythms during fasting in 7- to 9-day-old rabbits entrained by nursing during the night. Horm Behav 2010, 58:465-472.
68. Escobar C., Salgado R., Rodriguez K., Blancas Vázquez A.S., Angeles-Castellanos M., Buijs R.M. Scheduled meals and scheduled palatable snacks synchronize circadian rhythms: consequences for ingestive behavior. Physiol Behav 2011, 104:555-561.
69. Schaal B., Coureaud G., Langlois D., Giniès C., Sémon E., Perrier G. Chemical and behavioural characterization of the rabbit mammary pheromone. Nature 2003, 424:68-72.
70. Montúfar-Chaveznava R., Hernández-Campos O., Hudson R., Caldelas I. Differential maturation of the molecular clockwork in the olfactory bulb and suprachiasmatic nucleus of the rabbit. Neuroscience 2012, 10.1016/j.neuroscience.2012.01.025.