Involvement of the main but not the accessory olfactory system in maternal behavior of primiparous and multiparous ewes
Abstract
The respective roles of the main and accessory olfactory systems in the development of maternal behavior and selective suckling were investigated in parturient primiparous and multiparous ewes. Vomeronasal nerve section before parturition did not disturb either maternal behavior or maternal selectivity at suckling. By contrast, anosmia induced by zinc sulphate infusion had significant effects on the onset of maternal behavior in primiparous ewes. The onset of licking and of suckling were delayed and licking times and maternal bleats were reduced. Such disturbances were not observed in multiparous anosmic ewes, indicating that experience can compensate for the loss of olfactory information. On the other hand, anosmia prevented selective care regardless of maternal experience. Our results underline the importance of the main olfactory system for the development of adequate maternal behavior in sheep.
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There is some evidence that OT may play a role in mediating the beneficial effects of social support on immune function and stress reactivity.
“There is some evidence that OT may play a role in mediating these effects but more research is needed in this area, particularly with respect to immune function (for a review see Neumann in this Issue [84]).”
From Oxytocin and the Neural Mechanisms Regulating Social Cognition and Affiliative Behavior (2009) · cites this paper as [84]
The recognition of newborn lambs by ewes also appears to depend on the main olfactory system, although a vomeronasal contribution has also been reported.
“The recognition of newborn lambs by ewes also appears to depend on the main olfactory system (Levy et al., 1995), although a vomeronasal contribution has also been reported (Booth and Katz, 2000).”
From Human Vomeronasal Organ Function: A Critical Review of Best and Worst Cases (2001) · cites this paper as Levy et al., 1995
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“Lesioning the main, but not the accessory olfactory bulb, disrupts lamb recognition so that any alien lamb is allowed to suckle (Lévy et al., 1995).”
BackgroundSelf-citationKeller, M., Meurisse, M., & Lévy, F. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.6.1274 · Cited by 41 · see citing works
Self-citationLesion of the main olfactory epithelium facilitates maternal behavior in virgin rabbits
Chirino, R., Beyer, C., & González‐Mariscal, G. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.02.039 · Cited by 40 · see citing works
Mapping of brain networks involved in consolidation of lamb recognition memory
Keller, M., Meurisse, M., & Lévy, F. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.02.027 · Cited by 39 · see citing works
Self-citationBiological complexity and adaptability of simple mammalian olfactory memory systems
Brennan, P., & Keverne, E. B. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.10.020 · Cited by 37 · see citing works
Medina, J., & Workman, J. L. (2018) · Journal of Neuroscience Research · doi:10.1002/jnr.24311 · Cited by 37 · see citing works
Oettl, L., & Kelsch, W. (2017) · Current topics in behavioral neurosciences · doi:10.1007/7854_2017_8 · Cited by 36 · see citing works
Afferent and efferent connections of the cortical and medial nuclei of the amygdala in sheep
Meurisse, M., Chaillou, É., & Lévy, F. (2008) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2008.09.001 · Cited by 36 · see citing works
Self-citationAlvarez, M. R. D. V., & Kravetz, F. O. (2006) · Animal Research · doi:10.1051/animres:2006005 · Cited by 34 · see citing works
Chapter 8 Neurobiology of Maternal Behavior in Sheep
Lévy, F., & Keller, M. (2008) · Advances in the study of behavior · doi:10.1016/s0065-3454(08)00008-9 · Cited by 31 · see citing works
Self-citationScopolamine impairs the ability of parturient ewes to learn to recognise their lambs
Lévy, F., Richard, P., Meurisse, M., & Ravel, N. (1997) · Psychopharmacology · doi:10.1007/s002130050166 · Cited by 31 · see citing works
“the olfactory recognition of the lamb because bulbectomy (Bouissou 1968; Baldwin and Shillito 1974) or anosmia induced peripherally during gestation (Poindron 1976; Lévy et al. 1995) results in a loss of selectivity.”
BackgroundSelf-citationNogueira, S. S. D. C., Nogueira-Filho, S. L. G., Otta, E., Dias, C. T. D. S., & Carvalho, A. (1999) · Applied Animal Behaviour Science · doi:10.1016/s0168-1591(98)00231-7 · Cited by 29 · see citing works
“In Mus musculus and sheep, studies suggest that the experience acquired with the . previous births is important for the maternal success Salmon, 1987; Levy et al., 1995 .”
BackgroundGurule, S. C., Tobin, C. T., Bailey, D. W., & Gifford, J. A. H. (2021) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2021.105296 · Cited by 29 · see citing works
Timing of the attraction towards the placenta and amniotic fluid by the parturient cow
F, L. C. P. M., Hurnik, J. F., & King, G. J. (1997) · Applied Animal Behaviour Science · doi:10.1016/s0168-1591(96)01158-6 · Cited by 29 · see citing works
Selection for easier managed sheep
Conington, J., Collins, J., & Dwyer, C. M. (2010) · Animal Welfare · doi:10.1017/s096272860000227x · Cited by 28 · see citing works
Poindron, P., Otal, J., Ferreira, G., Keller, M., Guesdon, V., Nowak, R., & Lévy, F. (2010) · animal · doi:10.1017/s1751731110001126 · Cited by 28 · see citing works
“On the one hand, AF possesses a general supraindividual attractive quality for all parturient mothers (Lévy et al., 1983 and 1996) and this facilitates the acceptance of any lamb, including aliens (Poindron et al., 1980; Lévy and Poindron, 1984 and 1987; Lévy et al., 1995).”
BackgroundSelf-citationBrus, M., Meurisse, M., Keller, M., & Lévy, F. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00053 · Cited by 26 · see citing works
Self-citationExtensive immunolesions of basal forebrain cholinergic system impair offspring recognition in sheep
Ferreira, G., Meurisse, M., Gervais, R., Ravel, N., & Lévy, F. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00265-2 · Cited by 26 · see citing works
Self-citationBrain Evolution and Human Neuropsychology: The Inferential Brain Hypothesis
Koscik, T. R., & Tranel, D. (2012) · Journal of the International Neuropsychological Society · doi:10.1017/s1355617712000264 · Cited by 24 · see citing works
Disruption of adult olfactory neurogenesis induces deficits in maternal behavior in sheep
Corona, R., Meurisse, M., Cornilleau, F., Moussu, C., Keller, M., & Lévy, F. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.02.043 · Cited by 24 · see citing works
“Indeed, primiparous mothers rendered anosmic before parturition show reduced maternal behavior [24] and removing amniotic fluid from the neonate’s coat prevents maternal acceptance behavior [25].”
BackgroundSelf-citationNeural Substrates Involved in the Onset of Maternal Responsiveness and Selectivity in Sheep
Lévy, F. (2008) · Elsevier eBooks · doi:10.1016/b978-0-12-374285-8.00002-0 · Cited by 20 · see citing works
Self-citationMother-young recognition in goitered gazelle during hiding period
Blank, D. A., & Yang, W. (2017) · Behavioural Processes · doi:10.1016/j.beproc.2017.05.016 · Cited by 20 · see citing works
“…of even follower ungulates nuzzle the fawns’ tail region compulsively before allowing them to suckle, and anosmia prevents selective care regardless of maternal experience and the mothers’ ability to distinguish their young through auditory or visual cues (Levy et al., 1995; Keller et al., 2003).”
Biostimulation and pheromones in livestock: A review
Landaeta-Hernández, A. J., Ungerfeld, R., & Chenoweth, P. J. (2022) · Animal Reproduction Science · doi:10.1016/j.anireprosci.2022.107154 · Cited by 20 · see citing works
Ferreira, G., Gervais, R., Durkin, T., & Lévy, F. (1999) · Behavioral Neuroscience · doi:10.1037//0735-7044.113.1.136 · Cited by 18 · see citing works
Self-citationHernández, H., Serafín, N., Vázquez, H. G., Delgadillo, J. A., & Poindron, P. (2001) · Behavioural Processes · doi:10.1016/s0376-6357(01)00144-9 · Cited by 18 · see citing works
Self-citationSocial recognition memory requires protein synthesis after reactivation.
Perrin, G., Ferreira, G., Meurisse, M., Verdin, S., Mouly, A., & Lévy, F. (2007) · Behavioral Neuroscience · doi:10.1037/0735-7044.121.1.148 · Cited by 18 · see citing works
Self-citationSegregated pathways in the vomeronasal system
Halpern, M., Jia, C., & Shapiro, L. S. (1998) · Microscopy Research and Technique · doi:10.1002/(sici)1097-0029(19980615)41:6 · Cited by 87 · see citing works
Breed differences in maternal behaviour in relation to lamb (Ovis orientalis aries) productivity
von Borstel, U. K., Moors, E., Schichowski, C., & Gauly, M. (2010) · Livestock Science · doi:10.1016/j.livsci.2010.09.028 · Cited by 16 · see citing works
Lévy, F. (2022) · Advances in neurobiology · doi:10.1007/978-3-030-97762-7_3 · Cited by 15 · see citing works
Self-citationIs intranasal zinc effective and safe for the common cold? A systematic review and meta-analysis
D'Cruze, H., Arroll, B., & Kenealy, T. (2009) · Journal of Primary Health Care · doi:10.1071/hc09134 · Cited by 15 · see citing works
Corona, R., Meurisse, M., Cornilleau, F., Moussu, C., Keller, M., & Lévy, F. (2016) · Brain Structure and Function · doi:10.1007/s00429-016-1272-3 · Cited by 14 · see citing works
Self-citationThe role of olfactory cues in the discrimination of agemates by lambs
Ligout, S., Keller, M., & Porter, R. H. (2004) · Animal Behaviour · doi:10.1016/j.anbehav.2004.01.008 · Cited by 14 · see citing works
“In domestic sheep, Ovis aries, the critical influence of olfaction on the establishment of the ewe’s bondwithher newborn offspringhas been particularlywell documented (Lindsay & Fletcher 1968; Baldwin & Shillito 1974; Morgan et al. 1975; Poindron 1976; Poindron et al. 1993; Lévy et al. 1995).”
BackgroundOtal, J., Lévy, F., Cornilleau, F., Moussu, C., Keller, M., & Poindron, P. (2009) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2009.07.003 · Cited by 14 · see citing works
“Thus, preventing the perception of olfactory cues from the neonateby removing all amniotic fluids (Lévy andPoindron, 1987) or by rendering the ewe anosmic before parturition (Lévy et al., 1995), has more adverse consequences on the display of maternal behaviour in primiparous than in multiparous experienced mothers.”
BackgroundSelf-citationInvolvement of central muscarinic receptors in social and nonsocial learning in sheep
Ferreira, G., Poindron, P., & Lévy, F. (2003) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(03)00018-2 · Cited by 10 · see citing works
Self-citationLe rôle de l’odorat dans les relations interindividuelles des animaux d’élevage
Signoret, J. P., Lévy, F., Nowak, R., Orgeur, P., & Schaal, B. (1997) · INRAE Productions Animales · doi:10.20870/productions-animales.1997.10.5.4009 · Cited by 9 · see citing works
Self-citationPetrulis, A. (2003) · CRC Press eBooks · doi:10.1201/9780203911457.ch20 · Cited by 8 · see citing works
Weston, C. S. E. (2018) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2018.00336 · Cited by 7 · see citing works
Lévy, F., Keller, M., Cornilleau, F., Moussu, C., & Ferreira, G. (2010) · Developmental Psychobiology · doi:10.1002/dev.20459 · Cited by 7 · see citing works
Self-citationRusso, C., & Senese, V. P. (2022) · European Journal of Neuroscience · doi:10.1111/ejn.15890 · Cited by 6 · see citing works
“In mammals, offspring represent a very salient stimulus for adults (Lévy et al., 1995; Numan, 2012; Numan & Insel, 2003).”
BackgroundHillerer, K. M., & Gimsa, U. (2024) · Frontiers in Neuroscience · doi:10.3389/fnins.2024.1493605 · Cited by 4 · see citing works
- Authors
- Lévy, F., Locatelli, A., Piketty, V., Tillet, Y., & Poindron, P.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Corresponding author
- Lévy, F.
- Venue
- Physiology & Behavior
- Publisher
- Elsevier BV
- Published
- 1995-01
- Volume
- 57
- Issue
- 1
- Pages
- 97-104
- ISSN
- 0031-9384 (ISSN-L)
- OpenAlex
- W2013679119
- Cited by
- 130
- References
- 31
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 3 · 2022: 5 · 2021: 1 · 2020: 16 · 2019: 1 · 2018: 5 · 2017: 3 · 2016: 3 · 2015: 2 · 2014: 5 · 2013: 2 · 2012: 3
- FWCI
- 8.54
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Physiology & Behavior (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Health Sciences › Veterinary › Small Animals › Animal Behavior and Welfare Studies
- Keywords
- maternal behavior, vomeronasal system, accessory olfactory system, main olfactory system, sheep, ewes, anosmia, zinc sulfate, primiparous ewes, multiparous ewes, maternal experience, childbirth
- MeSH terms
- Animals, Behavior, Animal, Female, Maternal Behavior, Olfactory Bulb, Olfactory Pathways, Parity, Pregnancy, Sheep, Smell
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