Changes in responsiveness to kit odours across pregnancy: relevance for the onset of maternal behaviour
DOI:
https://doi.org/10.4995/wrs.2015.3134Keywords:
olfactory cues, pregnancy, maternal responsiveness, rabbit, parturitionAbstract
Virgin does are indifferent to foster kits but lesions to the main or accessory olfactory systems allow them to behave “maternally” (i.e., they crouch over the litter and allow suckling). This suggests that kit-derived olfactory cues are aversive to virgins but not to lactating does. We hypothesised that the valence of such olfactory cues changes throughout gestation so that, at parturition, does are attracted to the newborn and can then show placentophagia, clean the kits and nurse them. To explore this hypothesis we exposed does to 2 nest boxes containing a variety of pup-derived vs. “neutral” odours, quantifying the number of sniffs and entrances to each box over 60 min. Virgins, confronted with 2 different types of contrasts, showed no significant differences in the number of sniffs or entrances directed at any of the 2 boxes. Pregnant rabbits sniffed the “kit-odour” box significantly more than the “neutral” one as early as gestation day 7, depending on the animals’ experience with the experimental setup and kit odours as virgins. The number of sniffs declined in late pregnancy in all groups. Entrances into the “kit-odour” box were few and significantly higher than those shown towards the “neutral” box only in 1 group. Our findings agree with a correlation between a shift in the valence of kit-derived olfactory cues and the hormonal changes known to occur throughout pregnancy. The relevance of this phenomenon for the onset of maternal responsiveness at parturition is discussed.
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Bauer J.H. 1983. Effects of maternal state on the responsiveness to nest odors of hooded rats. Physiol. Behav., 30: 229-232. doi:10.1016/0031-9384(83)90010-0
Baum M.J., Keverne E.B. 2002. Sex difference in attraction thresholds for volatile odors from male and estrous female mouse urine. Horm. Behav., 41: 213-219. doi:10.1006/hbeh.2001.1749
Chirino R., Beyer C., González-Mariscal G. 2007. Lesion to the main olfactory epithelium facilitates maternal behavior in virgin rabbits. Behav. Brain Res., 180: 127-132. doi:10.1016/j.bbr.2007.02.039
Fleming A.S., Cheung U., Myhal N., Kessler Z. 1989. Effects of maternal hormones on 'timidity' and attraction to puprelated odors in female rats. Physiol. Behav., 46: 449-453. doi:10.1016/0031-9384(89)90019-X
González-Mariscal G., Chirino R., Beyer C., Rosenblatt J.S. 2004. Removal of the accessory olfactory bulbs facilitates maternal behavior in virgin rabbits. Behav. Brain Res., 152: 89-95. doi:10.1016/j.bbr.2003.09.036
González-Mariscal G., Díaz-Sánchez V., Melo A.I., Beyer C., Rosenblatt J.S. 1994. Maternal behavior in New Zealand white rabbits: quantification of somatic events, motor patterns and steroid plasma levels. Physiol. Behav., 55: 1081-1089. doi:10.1016/0031-9384(94)90391-3
González-Mariscal G., Gallegos J.A. 2007. New Zealand white rabbits show non-selective nursing in various types of nests. World Rabbit Sci. 15: 167-172. doi:10.4995/wrs.2007.592
González-Mariscal G., Jiménez A., Chirino R., Beyer C. 2009. Motherhood and nursing stimulate c-FOS expression in the rabbit forebrain. Behav. Neurosci., 123: 731-739. doi:10.1037/a0016487
González-Mariscal G., Lemus A.C., Vega-González A., Aguilar-Roblero A. 2013a. Litter size determines circadian periodicity of nursing in rabbits. Chronobiol. Int., 30: 711-718. doi:10.3109/07420528.2013.784769
González-Mariscal G., Melo A.I., Chirino R., Jiménez P., Beyer C., Rosenblatt J.S. 1998. Importance of mother/young contact at parturition and across lactation for the expression of maternal behavior in rabbits. Dev. Psychobiol., 32: 101-111. doi:10.1002/(SICI)1098-2302(199803)32:2<101::AIDDEV3>3.0.CO;2-T
González-Mariscal G., Melo A.I., Jiménez P., Beyer C., Rosenblatt J.S. 1996. Estradiol, progesterone, and prolactin regulate maternal nest-building in rabbits. J. Neuroendocrinol., 8: 901-907. doi:10.1111/j.1365-2826.1996.tb00818.x
González-Mariscal G., Toribio A., Gallegos J.A., Serrano-Meneses, M.A. 2013b. Characteristics of suckling stimulation determine the daily duration of mother-young contact and milk output in rabbits. Dev. Psychobiol., 55: 809-817. doi:10.1002/dev.21071
Halem H.A., Baum M.J., Cherry J.A. 2001. Sex difference and steroid modulation of pheromone-induced immediate early genes in the two zones of the mouse accessory olfactory system. J. Neurosci., 21: 2474-2480.
Halem H.A., Cherry J.A., Baum M.J. 1999. Vomeronasal neuroepithelium and forebrain FOS responses to male pheromones in male and female mice. J. Neurobiol., 39: 249-263. doi:10.1002/(SICI)1097-4695(199905)39:2<249::AIDNEU9>3.0.CO;2-R
Jilge B. 1993. The ontogeny of circadian rhythms in the rabbit. J. Biol. Rhythms, 8: 247-260. doi:10.1177/074873049300800307
Jilge B. 1995. Ontogeny of the rabbit's circadian rhythms without an external zeitgeber. Physiol. Behav., 58: 131-140. doi:10.1016/0031-9384(95)00006-5
Kelliher K.R., Chang Y.M., Wersinger S.R., Baum M.J. 1998. Sex difference and testosterone modulation of pheromoneinduced neuronal FOS in the ferret's main olfactory bulb and hypothalamus. Biol. Reprod., 59: 1454-1463. doi:10.1095/biolreprod59.6.1454
Kendrick K.M., Keverne E.B., Baldwin B.A. 1987. Intracerebroventricular oxytocin stimulates maternal behaviour in the sheep. Neuroendocrinology, 46: 56-61. doi:10.1159/000124796
Kinsley C.H., Bridges R.S. 1990. Morphine treatment and reproductive condition alter olfactory preferences for pup and adult male odors in female rats. Dev. Psychobiol., 23: 331-347. doi:10.1002/dev.420230405
Lévy F., Kendrick K.M., Goode J.A., Guevara-Guzmán 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 Res., 669: 197-206. doi:10.1016/0006-8993(94)01236-B
Mc Neilly A.S., Friessen H.G. 1978. Prolactin during pregnancy and lactation in the rabbit. Endocrinology, 102: 1548-1554. doi:10.1210/endo-102-5-1548
Melo A.I., González-Mariscal G. 2003. Placentophagia in rabbits: incidence across the reproductive cycle. Dev. Psychobiol., 43: 37-43. doi:10.1002/dev.10118
Moretto D., Paclik L., Fleming A. 1986. The effects of early rearing environment on maternal behavior in adult female rats. Dev. Psychobiol., 19: 581-591. doi:10.1002/dev.420190609
Pietras R.J., Moulton D.G. 1974. Hormonal influences on odor detection in rats: changes associated with the estrous cycle, pseudopregnancy, ovariectomy and administration of testosterone propionate. Physiol. Behav., 12: 475-491. doi:10.1016/0031-9384(74)90125-5
Siegel S., Castellan N.J. Jr. 1988. Non parametric statistics for the behavioral sciences. Mc Graw Hill, New York, USA.
Xiao K., Kondo Y., Sakuma Y. 2004. Sex-specific effects of gonadal steroids on conspecific odor preference in the rat. Horm. Behav., 46: 356-361. doi:10.1016/j.yhbeh.2004.05.008
Yu G.Z., Kaba H., Okutani F., Takahashi S., Higuchi T., Seto K. 1996a. The action of oxytocin originating in the hypothalamic paraventricular nucleus on mitral and granule cells in the rat main olfactory bulb. Neuroscience, 72: 1073-1082. doi:10.1016/0306-4522(95)00599-4
Yu G.Z., Kaba H., Okutani F., Takahashi S., Higuchi T. 1996b. The olfactory bulb: a critical site of action for oxytocin in the induction of maternal behaviour in the rat. Neuroscience, 72: 1083-1088. doi:10.1016/0306-4522(95)00600-1
Zarrow M.X., Denenberg V.H., Anderson C.O. 1965. Rabbit: frequency of suckling in the pup. Science, 150: 1835-1836. doi:10.1126/science.150.3705.1835
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