Changes in the sensory processing of olfactory signals induced by birth in sleep
Abstract
After giving birth, sheep and many other species form a selective bond with their offspring based on the sense of smell. Processing of olfactory signals is altered to allow the animals to perform this selective recognition. Lamb odors have little effect on either neurotransmitter release or electrical activity of neurons in the olfactory bulb before birth. However, after birth there is an increase in the number of mitral cells, the principal cells of the olfactory bulb, that respond to lamb odors, which is associated with increased cholinergic and noradrenergic neurotransmitter release. Selective recognition of lambs is accompanied by increased activity of a subset of mitral cells and release of glutamate and γ-aminobutyric acid (GABA) from the dendrodendritic synapses between the mitral and granule cells. The relation between the release of each transmitter after birth also suggests an increased efficacy of glutamate-evoked GABA release.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Many sites of action have been implicated for OT in rat social recognition, including the ventral hippocampus, septum, medial preoptic area, and olfactory bulb.
“There have been many sites of action implicated for OT in rat social recognition, including the ventral hippocampus, septum, medial preoptic area, and olfactory bulb [71-74].”
From Oxytocin and the Neural Mechanisms Regulating Social Cognition and Affiliative Behavior (2009) · cites this paper as [72]
Cites
Morris, R. G. M., Anderson, E., Lynch, G. S., & Baudry, M. (1986) · Nature · doi:10.1038/319774a0 · Cited by 3,640 · see citing works
Two-stage model of memory trace formation: A role for “noisy” brain states
Buzsáki, G. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90423-5 · Cited by 1,709 · see citing works
Long-term potentiation and NMDA receptors in rat visual cortex
Artola, A., & Singer, W. (1987) · Nature · doi:10.1038/330649a0 · Cited by 966 · see citing works
Synaptic organization of the mammalian olfactory bulb
Shepherd, G. M. (1972) · Physiological Reviews · doi:10.1152/physrev.1972.52.4.864 · Cited by 697 · see citing works
Changes in Spatial Patterns of Rabbit Olfactory EEG with Conditioning to Odors
Freeman, W. J., & Schneider, W. (1982) · Psychophysiology · doi:10.1111/j.1469-8986.1982.tb02598.x · Cited by 447 · see citing works
Membrane and synaptic properties of identified neurons in the olfactory bulb
Mori, K. (1987) · Progress in Neurobiology · doi:10.1016/0301-0082(87)90024-4 · Cited by 320 · see citing works
Stanton, P. K., & Sarvey, J. M. (1985) · Journal of Neuroscience · doi:10.1523/jneurosci.05-08-02169.1985 · Cited by 314 · see citing works
Surprisingly rich projection from locus coeruleus to the olfactory bulb in the rat
Shipley, M. T., Halloran, F. J., & de la Torre, J. (1985) · Brain Research · doi:10.1016/0006-8993(85)90537-2 · Cited by 292 · see citing works
Norepinephrine and learning-induced plasticity in infant rat olfactory system
Sullivan, R., Wilson, D., & Leon, M. (1989) · The Journal of Neuroscience · doi:10.1523/jneurosci.09-11-03998.1989 · Cited by 261 · see citing works
Vaginal stimulation: an important determinant of maternal bonding in sheep
Keverne, E. B., Levy, F., Poindron, P., & Lindsay, D. R. (1983) · Science · doi:10.1126/science.6849123 · Cited by 230 · see citing works
Endocrine and Sensory Regulation of Maternal Behavior in the Ewe
Poindron, P., & Neindre, P. L. (1980) · Advances in the study of behavior · doi:10.1016/s0065-3454(08)60115-1 · Cited by 221 · see citing works
Kendrick, K. M., Keverne, E. B., Chapman, C., & Baldwin, B. A. (1988) · Brain Research · doi:10.1016/0006-8993(88)91455-2 · Cited by 175 · see citing works
Pheromones in mice: reciprocal interaction between the nose and brain
Keverne, E. B., & de la Riva, C. (1982) · Nature · doi:10.1038/296148a0 · Cited by 172 · see citing works
Kendrick, K. M., Keverne, E. B., Chapman, C., & Baldwin, B. A. (1988) · Brain Research · doi:10.1016/0006-8993(88)91447-3 · Cited by 168 · see citing works
Gray, C. M., Freeman, W. J., & Skinner, J. E. (1986) · Behavioral Neuroscience · doi:10.1037//0735-7044.100.4.585 · Cited by 162 · see citing works
Rosser, A., & Keverne, E. B. (1985) · Neuroscience · doi:10.1016/0306-4522(85)90258-1 · Cited by 156 · see citing works
The importance of olfactory bulb noradrenalin for maternal recognition in sheep
Pissonnier, D., Thiéry, J., Fabre‐Nys, C., Poindron, P., & Keverne, E. B. (1985) · Physiology & Behavior · doi:10.1016/0031-9384(85)90309-9 · Cited by 148 · see citing works
Gray, C. M., Freeman, W. J., & Skinner, J. E. (1986) · Behavioral Neuroscience · doi:10.1037/0735-7044.100.4.585 · Cited by 142 · see citing works
Lévy, F., Poindron, P., & Neindre, P. L. (1983) · Physiology & Behavior · doi:10.1016/s0031-9384(83)80004-3 · Cited by 127 · see citing works
The effects of ablation of the olfactory bulbs on parturition and maternal behaviour in soay sheep
Baldwin, B. A., & Shillito, E. E. (1974) · Animal Behaviour · doi:10.1016/s0003-3472(74)80072-2 · Cited by 109 · see citing works
Kendrick, K. M., Lévy, F., & Keverne, E. B. (1991) · Physiology & Behavior · doi:10.1016/0031-9384(91)90551-x · Cited by 107 · see citing works
The ‘critical period’ in the attachment of lambs and ewes
Smith, F. V., Van-Toller, C., & Boyes, T. (1966) · Animal Behaviour · doi:10.1016/s0003-3472(66)80019-2 · Cited by 92 · see citing works
Distribution and derivation of cholinergic elements in the rat olfactory bulb
Godfrey, D. A., Ross, C. D., Herrmann, A. D., & Matschinsky, F. M. (1980) · Neuroscience · doi:10.1016/0306-4522(80)90103-7 · Cited by 71 · see citing works
A defect in the cell cycle of neuroglia in the myelin deficient jimpy mouse
Knapp, P. E., & Skoff, R. P. (1987) · Developmental Brain Research · doi:10.1016/0165-3806(87)90055-1 · Cited by 57 · see citing works
Taylor, J. G., & Keverne, E. B. (1991) · Biological Cybernetics · doi:10.1007/bf00199593 · Cited by 27 · see citing works
Inhibitory processes in development of seizure activity in hippocampal slices
Higashima, M. (1988) · Experimental Brain Research · doi:10.1007/bf00248498 · Cited by 17 · see citing works
Gervais, R., Araneda, S., & Pujol, J. (1984) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(84)90076-2 · Cited by 12 · see citing works
Single-Unit Recording in Conscious Sheep
Kendrick, K. M., & Baldwin, B. A. (1991) · Methods in neurosciences · doi:10.1016/b978-0-12-185257-3.50006-9 · Cited by 8 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Oxytocin and the Neural Mechanisms Regulating Social Cognition and Affiliative Behavior
Ross, H. E., & Young, L. J. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.05.004 · Cited by 856 · see citing works
“After giving birth, there is a strengthening of the mitral to granule and periglomerular cell synapses to bias the network to respond to lamb odor, with a higher number of output mitral cells responding to the ewes own lamb odor [34-36].”
BackgroundModulation of Early Olfactory Processing by an Octopaminergic Reinforcement Pathway in the Honeybee
Farooqui, T., Robinson, K. O., Vaessin, H., & Smith, B. H. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-12-05370.2003 · Cited by 282 · see citing works
Maternal brain response to own baby‐cry is affected by cesarean section delivery
Swain, J. E., Tasgin, E., Mayes, L. C., Feldman, R., Todd Constable, R., & Leckman, J. F. (2008) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2008.01963.x · Cited by 206 · see citing works
Egger, V., Svoboda, K., & Mainen, Z. F. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-20-07551.2003 · Cited by 170 · see citing works
Impaired Maternal Behavior in Mice Lacking Norepinephrine and Epinephrine
THOMAS, S. A., & Palmiter, R. D. (1997) · Cell · doi:10.1016/s0092-8674(00)80446-8 · Cited by 167 · see citing works
Learned recognition of maternal signature odors mediates the first suckling episode in mice
Logan, D. W., Brunet, L. J., Webb, W. R., Cutforth, T., Ngai, J., & Stowers, L. (2012) · Current Biology · doi:10.1016/j.cub.2012.08.041 · Cited by 148 · see citing works
Jiang, M., Griff, E. R., Ennis, M. J., Zimmer, L. A., & Shipley, M. T. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-19-06319.1996 · Cited by 135 · see citing works
Activity-Dependent Changes to the Brain and Behavior of the Honey Bee,Apis mellifera(L.)
Sigg, D. P., Thompson, C. M., & Mercer, A. R. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-18-07148.1997 · Cited by 130 · see citing works
Acetylcholine and Olfactory Perceptual Learning: Figure 1Preprint
Wilson, D. A., Fletcher, M. L., & Sullivan, R. M. (2004) · Learning & Memory · doi:10.1101/lm.66404 · Cited by 127 · see citing works
Learning modulates the ensemble representations for odors in primary olfactory networks
Daly, K. C., Christensen, T. A., Lei, H., Smith, B. H., & Hildebrand, J. G. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0401902101 · Cited by 117 · see citing works
Synaptic circuitry of the retina and olfactory bulb
DeVries, S. H., & Baylor, D. A. (1993) · Cell · doi:10.1016/s0092-8674(05)80033-9 · Cited by 113 · see citing works
Colbert, H. A., & Bargmann, C. I. (1997) · Learning & Memory · doi:10.1101/lm.4.2.179 · Cited by 112 · see citing works
Fletcher, M. L., & Wilson, D. A. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-17-06946.2003 · Cited by 110 · see citing works
Detection, processing and reinforcement of social cues: regulation by the oxytocin system
Menon, R., & Neumann, I. D. (2023) · Nature Reviews Neuroscience · doi:10.1038/s41583-023-00759-w · Cited by 100 · see citing works
Neural correlates of olfactory learning: Critical role of centrifugal neuromodulationPreprint
Fletcher, M. L., & Chen, W. R. (2010) · Learning & Memory · doi:10.1101/lm.941510 · Cited by 106 · see citing works
Distinct neural mechanisms mediate olfactory memory formation at different timescalesPreprint
McNamara, A. M., Magidson, P. D., Linster, C., Wilson, D. A., & Cleland, T. A. (2008) · Learning & Memory · doi:10.1101/lm.785608 · Cited by 88 · see citing works
Noradrenergic Induction of Odor-Specific Neural Habituation and Olfactory Memories
Shea, S. D., Katz, L. C., & MOONEY, R. D. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.3853-08.2008 · Cited by 82 · see citing works
Yuan, Q., Harley, C. W., Darby‐King, A., Neve, R. L., & McLean, J. H. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-11-04760.2003 · Cited by 70 · see citing works
The DAF-7 TGF-β signaling pathway regulates chemosensory receptor gene expression in C. elegansPreprint
Nolan, K. M., Sarafi-Reinach, T. R., Horne, J. G., Saffer, A. M., & Sengupta, P. (2002) · Genes & Development · doi:10.1101/gad.1027702 · Cited by 68 · see citing works
Neurochemistry of the Main Olfactory System
Ennis, M. J., Hamilton, K. A., & Hayar, A. M. (2007) · Springer eBooks · doi:10.1007/978-0-387-30374-1_6 · Cited by 65 · see citing works
Enhanced Synaptic Integration of Adult-Born Neurons in the Olfactory Bulb of Lactating Mothers
Kopel, H., Schechtman, E., Groysman, M., & Mizrahi, A. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.6354-11.2012 · Cited by 64 · see citing works
The parental brain and behavior: A target for endocrine disruption
Keller, M., Vandenberg, L. N., & Charlier, T. D. (2019) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.100765 · Cited by 62 · see citing works
Second-order neurones and receptor mechanisms in visual- and olfactory-information processing
Nakanishi, S. (1995) · Trends in Neurosciences · doi:10.1016/0166-2236(95)93929-r · Cited by 58 · see citing works
Cesarean Section or Natural Childbirth? Cesarean Birth May Damage Your Health
Chen, H., & Tan, D. (2019) · Frontiers in Psychology · doi:10.3389/fpsyg.2019.00351 · Cited by 57 · see citing works
Noradrenergic Plasticity of Olfactory Sensory Neuron Inputs to the Main Olfactory Bulb
Eckmeier, D., & Shea, S. D. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0551-14.2014 · Cited by 47 · see citing works
Centrifugal Drive onto Local Inhibitory Interneurons of the Olfactory Bulb
Mouret, A., Murray, K., & Lledo, P. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.03913.x · Cited by 43 · see citing works
Lethbridge, R. L., Hou, Q., Harley, C. W., & Yuan, Q. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035024 · Cited by 42 · see citing works
Precise and Pervasive Phasic Bursting in Locus Coeruleus during Maternal Behavior in Mice
Dvorkin, R., & Shea, S. D. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.0938-21.2022 · Cited by 38 · see citing works
Molecular approaches to aggregation behavior and social attachment
de Bono, M. (2002) · Journal of Neurobiology · doi:10.1002/neu.10162 · Cited by 36 · see citing works
Wolf, D., Hartig, R., Zhuo, Y., Scheller, M. F., Articus, M., Moor, M., Grinevich, V., Linster, C., Russo, E., Weber‐Fahr, W., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-50113-6 · Cited by 21 · see citing works
Olfaction-Inspired MCs: Molecule Mixture Shift Keying and Cross-Reactive Receptor Arrays
Jamali, V., Loos, H. M., Buettner, A., Schober, R., & Poor, H. V. (2023) · IEEE Transactions on Communications · doi:10.1109/tcomm.2023.3242379 · Cited by 17 · see citing works
Lévy, F. (2022) · Advances in neurobiology · doi:10.1007/978-3-030-97762-7_3 · Cited by 15 · see citing works
Pinho, J., Cunliffe, V. T., Kareklas, K., Petri, G., & Oliveira, R. F. (2023) · Communications Biology · doi:10.1038/s42003-023-04999-5 · Cited by 16 · see citing works
Neuronal replacement in microcircuits of the adult olfactory system
Lledo, P., & Lazarini, F. (2007) · Comptes Rendus Biologies · doi:10.1016/j.crvi.2007.01.002 · Cited by 15 · see citing works
Evolutionary biological perspectives on current social issues of breastfeeding and weaning
Tsutaya, T., & 水島, 希. (2023) · American Journal of Biological Anthropology · doi:10.1002/ajpa.24710 · Cited by 11 · see citing works
Abellán‐Álvaro, M., Ayala, G., Barneo‐Muñoz, M., Martínez‐Garciá, F., Agustín‐Pavón, C., & Lanuza, E. (2021) · The FASEB Journal · doi:10.1096/fj.202100163rr · Cited by 10 · see citing works
Livingstone, M. S. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2212224119 · Cited by 8 · see citing works
Kepple, D. R., Cazakoff, B. N., Demmer, H. S., Eckmeier, D., Shea, S. D., & Koulakov, A. A. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/339689 · Cited by 7 · see citing works
Hillerer, K. M., & Gimsa, U. (2024) · Frontiers in Neuroscience · doi:10.3389/fnins.2024.1493605 · Cited by 4 · see citing works
Neuroendocrinology, Neurochemistry, and Molecular Neurobiology of Affiliative Behavior
Hammock, E. A. D., & Young, L. J. (2006) · Springer eBooks · doi:10.1007/978-0-387-30405-2_6 · Cited by 4 · see citing works
Stable clique membership in mouse societies requires oxytocin-enabled social sensory statesPreprint
Nelias, C., Ghanayem, S., Wolf, D., Moor, M., Scheller, M. F., Grinevich, V., Reinwald, J., & Kelsch, W. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.08.26.672298 · Cited by 3 · see citing works
Wang, T., & Wöhr, M. (2026) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2026.106747 · Cited by 2 · see citing works
Mammalian social memory relies on neuromodulation in the olfactory bulb
Suyama, H., Egger, V., & Lukas, M. (2022) · e-Neuroforum · doi:10.1515/nf-2022-0004 · Cited by 2 · see citing works
Precise and pervasive phasic bursting in locus coeruleus during maternal behaviorPreprint
Dvorkin, R., & Shea, S. D. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.03.31.437751 · Cited by 2 · see citing works
Stable clique membership in male mouse societies requires oxytocin-enabled social sensory states
Nelias, C., Ghanayem, S., Wolf, D., Moor, M., Nikolantonaki, D., Turgut, E. D., Scheller, M. F., Grinevich, V., Reinwald, J., & Kelsch, W. (2026) · Nature Communications · doi:10.1038/s41467-026-76841-5 · Cited by 1 · see citing works
Transition to motherhood, marial stability and divorce
Simonič, B. (2015) · The Pontifical University of John Paul II in Krakow Press eBooks · doi:10.15633/9788374384919.07
Freitas‐de‐Melo, A., Lévy, F., Meurisse, M., Casuriaga, D., Pérez-Clariget, R., & Ungerfeld, R. (2026) · Behavioural Brain Research · doi:10.1016/j.bbr.2026.116489
- Authors
- Kendrick, K. M., Lévy, F., & Keverne, E. B.
- Affiliations
- Biotechnology and Biological Sciences Research Council (GB)
- Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR)
- University of Cambridge (GB)
- Venue
- Science
- Published
- 1992-05-08
- Volume
- 256
- Issue
- 5058
- Pages
- 833-836
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W4236618601
- Cited by
- 46
- References
- 27
- Citations by year
- 2026: 3 · 2025: 1 · 2024: 2 · 2023: 4 · 2022: 4 · 2021: 2 · 2019: 2 · 2018: 1 · 2015: 1 · 2014: 1 · 2012: 3
- FWCI
- 0.44
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Science (publishedVersion)
- HAL (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- olfactory processing, births, sheep, mitral cells, olfactory bulb, cholinergic neurotransmission, noradrenergic neurotransmission, glutamate release, GABA release, dendrodendritic synapses, postnatal development
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review