Abstract
New neurons are continuously added to the main olfactory bulb (MOB) of the mammalian brain. While their function has been demonstrated in olfactory learning, it is less known in an ethological context such as mothering. We addressed this question by investigating whether in sheep mothers the adult-generated olfactory neurons contribute to the processing of odors involved in attraction to lambs and in memorization of its individual signature. Parturient ewes, after having 2 days of contact with their lamb and being separated from them for 3 h, were exposed for 2 h either to their own lamb, an unfamiliar lamb or a familiar adult sheep and then sacrificed. A control group was composed of mothers not exposed to any lambs for 5 h before sacrifice. Bromodeoxyuridine, a marker of cell division, was injected 3 months before parturition and revealed through immunocytochemistry in combination with markers of activation or neuronal maturation. The percentage of adult-born cells activated in the granular layer of the MOB was compared between the four groups. Results show that the whole population of olfactory neuroblasts and in particular the 3-month-old neuroblasts, are preferentially activated by lamb exposure and that the preferential activation is specific to olfactory neurogenesis since no activation was observed in newborn neurons of the dentate gyrus. However, neither neuroblasts nor mature neurons of the MOB differentiate between familiar and unfamiliar lamb exposure. Therefore, our data shows that adult-born neurons contribute to the processing of infantile odors which are determinant for maternal behavior.
Similar content being viewed by others
References
Abrous D, Koehl M, Le Moal M (2005) Adult neurogenesis: from precursors to network and physiology. Physiol Rev 85:523–569
Alonso M, Lepousez G, Sebastien W, Bardy C, Gabellec MM, Torquet N, Lledo PM (2012) Activation of adult-born neurons facilitates learning and memory. Nat Neurosci 15:897–904. doi:10.1038/nn.3108
Belnoue L, Grosjean N, Abrous DN, Koehl M (2011) A critical time window for the recruitment of bulbar newborn neurons by olfactory discrimination learning. J Neurosci 31:1010–1016. doi:10.1523/jneurosci.3941-10.2011
Brown JP, Couillard-Despres S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG (2003) Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467:1–10. doi:10.1002/cne.10874
Brus M, Meurisse M, Gheusi G, Keller M, Lledo PM, Lévy F (2013) Dynamics of olfactory and hippocampal neurogenesis in adult sheep. J Comp Neurol 521:169–188. doi:10.1002/cne.23169
Brus M, Meurisse M, Keller M, Lévy F (2014) Interactions with the young down-regulate adult olfactory neurogenesis and enhance the maturation of olfactory neuroblasts in sheep mothers. Front Behav Neurosci 8:53. doi:10.3389/fnbeh.2014.00053
Corona R, Lévy F (2015) Chemical olfactory signals and parenthood in mammals. Horm Behav 68:77–90. doi:10.1016/j.yhbeh.2014.06.018
Dardou D, Datiche F, Cattarelli M (2006) Fos and Egr1 expression in the rat brain in response to olfactory cue after taste-potentiated odor aversion retrieval. Learn Mem 13:150–160. doi:10.1101/lm.148706
Feierstein CE et al (2010) Disruption of adult neurogenesis in the olfactory bulb affects social interaction but not maternal behavior. Front Behav Neurosci 4:176. doi:10.3389/fnbeh.2010.00176
Garrett L et al (2015) Conditional reduction of adult born doublecortin-positive neurons reversibly impairs selective behaviours. Front Behav Neurosci 9:302. doi:10.3389/fnbeh.2015.00302
Huang L, Bittman EL (2002) Olfactory bulb cells generated in adult male golden hamsters are specifically activated by exposure to estrous females. Horm Behav 41:343–350. doi:10.1006/hbeh.2002.1767
Keller M, Perrin G, Meurisse M, Ferreira G, Lévy F (2004) Cortical and medial amygdala are both involved in the formation of olfactory offspring memory in sheep. Eur J Neurosci 20:3433–3441
Keller M, Meurisse M, Levy F (2005) Mapping of brain networks involved in consolidation of lamb recognition memory. Neuroscience 133:359–369
Kendrick KM, Lévy F, Keverne EB (1992) Changes in the sensory processing of olfactory signals induced by birth in sheep. Science 256:833–836
Keverne EB, Lévy F, Guevara-Guzman R, Kendrick KM (1993) Influence of birth and maternal experience on olfactory bulb neurotransmitter release. Neuroscience 56:557–565
Larsen CM, Grattan DR (2010) Prolactin-induced mitogenesis in the subventricular zone of the maternal brain during early pregnancy is essential for normal postpartum behavioral responses in the mother. Endocrinology 151:3805–3814. doi:10.1210/en.2009-1385
Lazarini F, Lledo P-M (2011) Is adult neurogenesis essential for olfaction? Trends Neurosci 34:20–30
Lazarini F et al (2009) Cellular and behavioral effects of cranial irradiation of the subventricular zone in adult mice. PLoS One 4:e7017
Lepousez G, Nissant A, Lledo P-M (2015) Adult neurogenesis and the future of the rejuvenating brain circuits. Neuron 86:387–401. doi:10.1016/j.neuron.2015.01.002
Lévy F, Keller M (2009) Olfactory mediation of maternal behavior in selected mammalian species. Behav Brain Res 200:336–345
Lévy F, Poindron P (1987) The importance of amniotic fluids for the establishment of maternal behavior in experienced and non-experienced ewes. Anim Behav 35:1188–1192
Lévy F, Guevara-Guzman R, Hinton MR, Kendrick KM, Keverne EB (1993) Effects of parturition and maternal experience on noradrenaline and acetylcholine release in the olfactory bulb of sheep. Behav Neurosci 107:662–668
Lévy F, Kendrick KM, Goode JA, Guevara-Guzman R, Keverne EB (1995a) 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
Lévy F, Locatelli A, Piketty V, Tillet Y, Poindron P (1995b) Involvement of the main but not the accessory olfactory system in maternal behavior of primiparous and multiparous ewes. Physiol Behav 57:97–104
Lévy F, Keller M, Poindron P (2004) Olfactory regulation of maternal behavior in mammals. Horm Behav 46:284–302
Lévy F, Gheusi G, Keller M (2011) Plasticity of the parental brain: a case for neurogenesis. J Neuroendocrinol 23:984–993. doi:10.1111/j.1365-2826.2011.02203.x
Lledo PM, Alonso M, Grubb MS (2006) Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci 7:179–193
Lonergan ME, Gafford GM, Jarome TJ, Helmstetter FJ (2010) Time-dependent expression of Arc and zif268 after acquisition of fear conditioning. Neural Plast 2010:139891. doi:10.1155/2010/139891
Magavi SSP, Mitchell BD, Szentirmai O, Carter BS, Macklis JD (2005) Adult-born and preexisting olfactory granule neurons undergo distinct experience-dependent modifications of their olfactory responses in vivo. J Neurosci 25:10729–10739. doi:10.1523/jneurosci.2250-05.2005
Mak GK, Weiss S (2010) Paternal recognition of adult offspring mediated by newly generated CNS neurons. Nat Neurosci 13:753–758. doi:10.1038/nn.2550
Mak GK, Enwere EK, Gregg C, Pakarainen T, Poutanen M, Huhtaniemi I, Weiss S (2007) Male pheromone-stimulated neurogenesis in the adult female brain: possible role in mating behavior. Nat Neurosci 10:1003–1011
Ming GL, Song H (2005) Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28:223–250
Mouret A, Gheusi G, Gabellec MM, de Chaumont F, Olivo-Marin JC, Lledo PM (2008) Learning and survival of newly generated neurons: when time matters. J Neurosci 28:11511–11516
Nissant A, Bardy C, Katagiri H, Murray K, Lledo P-M (2009) Adult neurogenesis promotes synaptic plasticity in the olfactory bulb. Nat Neurosci 12:728–730
Numan M, Fleming AS, Lévy F (2006) Maternal Behavior. In: Neill JD (ed) Knobil and Neill’s physiology of reproduction. Elsevier, Amsterdam, pp 1921–1994
Oboti L et al (2011) Newborn interneurons in the accessory olfactory bulb promote mate recognition in female mice. Front Neurosci 5:113. doi:10.3389/fnins.2011.00113
Sakamoto M, Imayoshi I, Ohtsuka T, Yamaguchi M, Mori K, Kageyama R (2011) Continuous neurogenesis in the adult forebrain is required for innate olfactory responses. Proc Natl Acad Sci USA 108:8479–8484. doi:10.1073/pnas.1018782108
Schmidt-Hieber C, Jonas P, Bischofberger J (2004) Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 429:184–187. doi:10.1038/nature02553
Sultan S, Mandairon N, Kermen F, Garcia S, Sacquet J, Didier A (2010) Learning-dependent neurogenesis in the olfactory bulb determines long-term olfactory memory. FASEB J 24:2355–2363. doi:10.1096/fj.09-151456
Yamaguchi M, Mori K (2005) Critical period for sensory experience-dependent survival of newly generated granule cells in the adult mouse olfactory bulb. Proc Natl Acad Sci USA 102:9697–9702. doi:10.1073/pnas.0406082102
Zangenehpour S, Chaudhuri A (2002) Differential induction and decay curves of c-fos and zif268 revealed through dual activity maps. Mol Brain Res 109:221–225 (pii:S0169328X02005569)
Acknowledgments
The authors would like to acknowledge the financial support of the Agence Nationale de Recherches programme blanc (2013–2016) PLASTMATBEHAV. We particularly thank (1) N. Jouaneau and T. Delpuech for histological preparation; (2) J.-P. Dubois and A. Arnould for killing of animals; (3) the staff of the UEPAO of INRA Centre Nouzilly for animal breeding; (4) the cellular imaging platform (PIC) of UMR PRC, Nouzilly; (5) J. Lonstein for comments and English corrections.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Corona, R., Meurisse, M., Cornilleau, F. et al. Exposure to young preferentially activates adult-born neurons in the main olfactory bulb of sheep mothers. Brain Struct Funct 222, 1219–1229 (2017). https://doi.org/10.1007/s00429-016-1272-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-016-1272-3