Vaginocervical Stimulation of ewes induces the rapid formation of a new bond with an alien young without interfering with a previous bond

Developmental Psychobiology

Volumn 52, Issue 6, 2010, Pages 537-544

  Levy F ^a,b,c,d   Keller, M ^a,b,c,d   Cornilleau, F ^a,b,c,d   Moussu, C ^a,b,c,d   Ferreira, G ^a,b,c,d  

^a UMR85 PHYSIOLOGIE DE LA REPRODUCTION ET DES COMPORTEMENTS   (France)

^b CNRS   (France)

^c UNIVERSITÉ DE TOURS   (France)

^d Haras Nationaux   (France)

Author keywords

Individual recognition; Maternal behavior; Olfactory recognition; Ovis aries; Sheep

Indexed keywords

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; FEMALE; MATERNAL BEHAVIOR; NEWBORN; NONPARAMETRIC TEST; ODOR; PHYSIOLOGY; RECOGNITION; SHEEP; UTERINE CERVIX; VAGINA;

ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; CERVIX UTERI; FEMALE; MATERNAL BEHAVIOR; RECOGNITION (PSYCHOLOGY); SHEEP; SMELL; STATISTICS, NONPARAMETRIC; VAGINA;

ANIMALIA; OVIS ARIES;

EID: 77956899739     PISSN: 00121630     EISSN: 10982302     Source Type: Journal    
DOI: 10.1002/dev.20459     Document Type: Article

References (41)

1. da Costa, A. P., Guevara-Guzman, R. G., Ohkura, S., Goode, J. A., & Kendrick, K. M. (1996). The role of oxytocin release in the paraventricular nucleus in the control of maternal behaviour in the sheep. Journal of Neuroendocrinology, 8(3), 163-177.
2. Ferreira, G., Terrazas, A., Poindron, P., Nowak, R., Orgeur, P., & Lévy, F. (2000). Learning of olfactory cues is not necessary for early lamb recognition by the mother. Physiology and Behavior, 69(4-5), 405-412.
3. Hayes, U. L., & De Vries, G. J. (2007). Role of pregnancy and parturition in induction of maternal behavior in prairie voles (Microtus ochrogaster). Hormones and Behaviour, 51(2), 265-272.
4. Keller, M., Meurisse, M., & Lévy, F. (2004). Mapping the neural substrates involved in maternal responsiveness and lamb olfactory memory in parturient ewes using Fos imaging. Behavioral Neuroscience, 118(6), 1274-1284.
5. Keller, M., Meurisse, M., Poindron, P., Nowak, R., Ferreira, G., Shayit, M., et al. (2003). Maternal experience influences the establishment of visual/auditory, but not olfactory recognition of the newborn lamb by ewes at parturition. Dev Psychobiol, 43(3), 167-176.
6. Keller, M., Perrin, G., Meurisse, M., Ferreira, G., & Levy, F. (2004). Cortical and medial amygdala are both involved in the formation of olfactory offspring memory in sheep. European Journal of Neuroscience, 20(12), 3433-3441.
7. Kendrick, K. M., da Costa, A. P., Broad, K. D., Ohkura, S., Guevara, R., Lévy, F., et al. (1997). Neural control of maternal behaviour and olfactory recognition of offspring. Brain Research Bulletin, 44(4), 383-395.
8. Kendrick, K. M., da Costa, A. P., Hinton, M. R., & Keverne, E. B. (1992). A simple method for fostering lambs using anoestrus ewes with artificially induced lactation and maternal behaviour. Applied Animal Behaviour Science, 34, 345-357.
9. Kendrick, K. M., Guevara-Guzman, R., Zorrilla, J., Hinton, M. R., Broad, K. D., Mimmack, M., et al. (1997). Formation of olfactory memories mediated by nitric oxide. Nature, 388(6643), 670-674.
10. Kendrick, K. M., Haupt, M. A., Hinton, M. R., Broad, K. D., & Skinner, J. D. (2001). Sex differences in the influence of mothers on the sociosexual preferences of their offspring. Hormones and Behavior, 40, 322-338.
11. Kendrick, K. M., & Keverne, E. B. (1991). Importance of progesterone and estrogen priming for the induction of maternal behavior by vaginocervical stimulation in sheep: Effects of maternal experience. Physiology and Behavior, 49(4), 745-750.
12. Kendrick, K. M., Keverne, E. B., Hinton, M. R., & Goode, J. A. (1992). Oxytocin, amino acid and monoamine release in the region of the medial preoptic area and bed nucleus of the stria terminalis of the sheep during parturition and suckling. Brain Research, 569(2), 199-209.
13. Kendrick, K. M., Keverne, E. B., Shapman, C., & Baldwin, B. A. (1988). Microdialysis measurement of oxytocin, aspartate, gama-aminobutyric acid and glutamate release from the olfactory bulb of the sheep during vaginocervical stimulation. Brain Research, 442, 171-174.
14. Kendrick, K. M., Lévy, F., & Keverne, E. B. (1991). Importance of vaginocervical stimulation for the formation of maternal bonding in primiparous and multiparous parturient ewes. Physiology and Behavior, 50(3), 595-600.
15. Kendrick, K. M., Lévy, F., & Keverne, E. B. (1992). Changes in the sensory processing of olfactory signals induced by birth in sheep. Science, 256(5058), 833-836.
16. Keverne, E. B., Lévy, F., Poindron, P., & Lindsay, D. R. (1983). Vaginal stimulation: An important determinant of maternal bonding in sheep. Science, 219(4580), 81-83.
17. Krehbiel, D., Poindron, P., Lévy, F., & Prud'Homme, M. J. (1987). Peridural anesthesia disturbs maternal behavior in primiparous and multiparous parturient ewes. Physiology and Behavior, 40(4), 463-472.
18. Lévy, F., & Fleming, A. S. (2006). The neurobiology of maternal behavior in mammals. In P. J. Marshall, & N. A. Fox (Eds.), The development of social engagement- Neurobiological perspectives (pp. 197-246). New-York: Oxford University Press.
19. Lévy, F., Gervais, R., Kindermann, U., Orgeur, P., & Piketty, V. (1990). Importance of beta-noradrenergic receptors in the olfactory bulb of sheep for recognition of lambs. Behavioral Neuroscience, 104, 464-469.
20. Lévy, F., Guevara-Guzman, R., Hinton, M. R., Kendrick, K. M., & Keverne, E. B. (1993). Effects of parturition and maternal experience on noradrenaline and acetylcholine release in the olfactory bulb of sheep. Behavioral Neuroscience, 107, 662-668.
21. Lévy, F., & Keller, M., (2008). Neurobiology of maternal behavior in sheep. In H. J. Brockmann, T. J. Roper, M. Naguib, K. E. Wynne-Edwards, C. Barnard, & J. C. Mitani (Eds.), Advances in the study of behavior (Vol. 38, pp. 399- 437). Amsterdam: Elsevier.
22. Lévy, F. Kendrick, K. M., Goode, J. A., Guevara-Guzman, R., & Keverne, E. B. (1995). Oxytocin and vasopressin release in the olfactory bulb of parturient ewes: Changes with maternal experience and effects on acetylcholine, gamma-aminobutyric acid, glutamate and noradrenaline release. Brain Research, 669(2), 197-206.
23. Lévy, F., Kendrick, K. M., Keverne, E. B., Piketty, V., & Poindron, P. (1992). Intracerebral oxytocin is important for the onset of maternal behavior in inexperienced ewes delivered under peridural anesthesia. Behavioral Neuroscience, 106(2), 427-432.
24. Lévy, F., Keverne, E. B., Piketty, V., & Poindron, P. (1990). Physiological determinism of olfactory attraction for amniotic fluids in sheep. In D. W. MacDonald, D. Mü ller- Schwarze, & S. E. Natynczuck (Eds.), Chemical signals in vertebrates (Vol. 5, pp. 162-165). Oxford: Oxford University Press.
25. Lévy, F., Locatelli, A., Piketty, V., Tillet, Y., & Poindron, P. (1995). Involvement of the main but not the accessory olfactory system in maternal behavior of primiparous and multiparous ewes. Physiology and Behavior, 57(1), 97-104.
26. Lévy, F., & Poindron, P. (1987). The importance of amniotic fluids for the establishment of maternal behavior in experienced and non-experienced ewes. Animal Behaviour, 35, 1188-1192.
27. Lévy, F., Poindron, P., & Le Neindre, P. (1983). Attraction and repulsion by amniotic fluids and their olfactory control in the ewe around parturition. Physiology and Behavior, 31, 687-692.
28. Meurisse, M., Chaillou, E., & Levy, F. (2009). Afferent and efferent connections of the cortical and medial nuclei of the amygdala in sheep. Journal of Chemical Neuroanatomy, 37(2), 87-97.
29. Nathanielsz, P. W. (1978). Endocrine mechanisms of parturition. Annual Review of Physiology, 40, 411-445.
30. Numan, M., Fleming, A. S., & Lévy, F. (2006). Maternal behavior. In J. D. Neill (Ed.), Knobil and Neill's physiology of reproduction (pp. 1921-1994). Amsterdam: Elsevier.
31. Numan, M., & Insel, T. R. (2003). The neurobiology of parental behavior. New York: Springer.
32. Orpen, B. G., & Fleming, A. S. (1987). Experience with pups sustains maternal responding in postpartum rats. Physiology and Behavior, 40(1), 47-54.
33. Pissonnier, D., Thierry, J. C., Fabre-Nys, P., Poindron, P., & Keverne, E. B. (1985). The importance of olfactory bulb noradrenalin for maternal recognition in sheep. Physiology and Behavior, 35, 361-363.
34. Poindron, P. (1976). Effets de la suppression de l'odorat, sans lésion des bulbes olfactifs, sur la sélectivité du comportement maternel de la Brebis. Comptes Rendus Hebdomadaires Des Séances de l'Académie des Sciences de Paris. Série D: Sciences Naturelles, 282(5), 489-491.
35. Poindron, P., Martin, G.B., & Hooley, R.D. (1979). Effects of lambing induction on the sensitive period for the establishment of maternal behaviour in sheep. Physiology and Behavior, 23(6), 1081-1087.
36. Poindron, P., & Le Neindre, P. (1980). Endocrine and sensory regulation of maternal behavior in the ewe. In J. S. Rosenblatt, R. A. Hinde, & C. Beer (Eds.), Advances in the study of behavior (Vol. 11, pp. 75-119). New York: Academic Press.
37. Rosenblatt, R. A. Hinde, & C. Beer (Eds.), Advances in the study of behavior (Vol. 11, pp. 75-119). New York: Academic Press.
38. Poindron, P., Lévy, F., & Krehbiel, D. (1988). Genital, olfactory, and endocrine interactions in the development of maternal behaviour in the parturient ewe. Psychoneuroendocrinology, 13(1-2), 99-125.
39. Putu, I. G., Poindron, P., Oldham, C. M., Gray, S. J., & Ballard, M. (1986). Lamb desertion in primiparous and multiparous Merino ewes induced to lamb with dexamethasone. Proceedings of the Australian Society for Animal Production, 16, 315-318.
40. Yeo, J. A., & Keverne, E. B. (1986). The importance of vaginalcervical stimulation for maternal behaviour in the rat. Physiology and Behavior, 37(1), 23-26.
41. Yu, G. Z., Kaba, H., Okutani, F., Takahashi, S., Higuchi, T., & Seto, K. (1996). The action of oxytocin originating in the hypothalamic paraventricular nucleus on mitral and granule cells in the rat main olfactory bulb. Neuroscience, 72(4), 1073-1082.