Learned recognition of maternal signature odors mediates the first suckling episode in mice
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Background Soon after birth, all mammals must initiate milk suckling to survive. In rodents, this innate behavior is critically dependent on uncharacterized maternally derived chemosensory ligands. Recently, the first pheromone sufficient to initiate suckling was isolated from the rabbit. Identification of the olfactory cues that trigger first suckling in the mouse would provide the means to determine the neural mechanisms that generate innate behavior.Results Here we use behavioral analysis, metabolomics, and calcium imaging of primary sensory neurons and find no evidence of ligands with intrinsic bioactivity, such as pheromones, acting to promote first suckling in the mouse. Instead, we find that the initiation of suckling is dependent on variable blends of maternal "signature odors" that are learned and recognized prior to first suckling.Conclusions As observed with pheromone-mediated behavior, the response to signature odors releases innate behavior. However, this mechanism tolerates variability in both the signaling ligands and sensory neurons, which may maximize the probability that this first essential behavior is successfully initiated. These results suggest that mammalian species have evolved multiple strategies to ensure the onset of this critical behavior.
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A neutral odor can acquire the valence of a maternal odor if placed into the amniotic fluid a few days before birth, suggesting the odor itself is arbitrary for both rats and mice.
“Even a neutral odor can acquire the valence of a maternal odor if placed into the amniotic fluid a few days before birth, suggesting the odor itself is arbitrary for both rats and mice (Hepper and Cleland, 1998, Leon, 1992, Logan et al., 2012, Pedersen and Blass, 1982, Smotherman and Robinson, 1987, Sullivan and Leon, 1986, Sullivan and Wilson, 1991).”
From Early life adversity during the infant sensitive period for attachment: Programming of behavioral neurobiology of threat processing and social behavior (2017) · cites this paper as Logan et al., 2012
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Smith, C. A., Want, E. J., O’Maille, G., Abagyan, R. A., & Siuzdak, G. E. (2006) · Analytical Chemistry · doi:10.1021/ac051437y · Cited by 5,296 · see citing works
Combinatorial Receptor Codes for Odors
Malnic, B., Hirono, J., Sato, T., & Buck, L. B. (1999) · Cell · doi:10.1016/s0092-8674(00)80581-4 · Cited by 2,302 · see citing works
‘Pheromones’: a New Term for a Class of Biologically Active Substances
KARLSON, P., & LÜSCHER, M. (1959) · Nature · doi:10.1038/183055a0 · Cited by 1,364 · cited 2× · see citing works
“We perform in utero alteration of native amniotic fluid and find that the bioactivity is inconsistent with that expected of a classic pheromone [41].”
Rheingold, H. L. (1963) · Medical Entomology and Zoology · Cited by 886 · see citing works
Loss of Sex Discrimination and Male-Male Aggression in Mice Deficient for TRP2
Stowers, L., Holy, T. E., Meister, M., Dulac, C. G., & Koentges, G. (2002) · Science · doi:10.1126/science.1069259 · Cited by 880 · see citing works
Self-citationInnate versus learned odour processing in the mouse olfactory bulb
Kobayakawa, K., Kobayakawa, R., Matsumoto, H., Oka, Y., Imai, T., Ikawa, M., Okabe, M., Ikeda, T., Itohara, S., Kikusui, T., et al. (2007) · Nature · doi:10.1038/nature06281 · Cited by 659 · see citing works
Dhallan, R. S., Yau, K., Schrader, K. A., & Reed, R. R. (1990) · Nature · doi:10.1038/347184a0 · Cited by 652 · see citing works
MHC Class I Peptides as Chemosensory Signals in the Vomeronasal Organ
Leinders‐Zufall, T., Brennan, P., Widmayer, P., Prashanth Chandramani, S., Maul‐Pavicic, A., Jäger, M., Li, X.-H., Breer, H., Zufall, F., & Boehm, T. L. J. (2004) · Science · doi:10.1126/science.1102818 · Cited by 608 · see citing works
Representations of Odor in the Piriform Cortex
Stettler, D. D., & Axel, R. (2009) · Neuron · doi:10.1016/j.neuron.2009.09.005 · Cited by 583 · see citing works
Altered sexual and social behaviors in trp2 mutant mice
Leypold, B. G., Yu, C., Leinders‐Zufall, T., Kim, M. M., Zufall, F., & Axel, R. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.082127599 · Cited by 572 · see citing works
Mice Deficient in Golf Are Anosmic
Belluscio, L., Gold, G. H., Nemes, A., & Axel, R. (1998) · Neuron · doi:10.1016/s0896-6273(00)80435-3 · Cited by 563 · see citing works
Identification of protein pheromones that promote aggressive behaviour
Chamero, P., Marton, T. F., Logan, D. W., Flanagan, K. A., Cruz, J. R., Saghatelian, A., Cravatt, B. F., & Stowers, L. (2007) · Nature · doi:10.1038/nature05997 · Cited by 529 · see citing works
Self-citationBrunet, L. J., Gold, G. H., & Ngai, J. (1996) · Neuron · doi:10.1016/s0896-6273(00)80200-7 · Cited by 510 · see citing works
Self-citationWong, S. T., Trinh, K., Hacker, B., Chan, G. C. K., Lowe, G., Gaggar, A., Xia, Z., Gold, G. H., & Storm, D. R. (2000) · Neuron · doi:10.1016/s0896-6273(00)00060-x · Cited by 470 · see citing works
TRP2: A candidate transduction channel for mammalian pheromone sensory signaling
Liman, E. R., Corey, D. P., & Dulac, C. G. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.10.5791 · Cited by 445 · see citing works
Encoding social signals in the mouse main olfactory bulb
Lin, D., Zhang, S., Block, E., & Katz, L. C. (2005) · Nature · doi:10.1038/nature03414 · Cited by 444 · see citing works
Sex-specific peptides from exocrine glands stimulate mouse vomeronasal sensory neurons
Kimoto, H., Haga‐Yamanaka, S., Sato, K., & Touhara, K. (2005) · Nature · doi:10.1038/nature04033 · Cited by 378 · see citing works
Haga‐Yamanaka, S., Hattori, T., Sato, T., Sato, K., Matsuda, S., Kobayakawa, R., Sakano, H., Yoshihara, Y., Kikusui, T., & Touhara, K. (2010) · Nature · doi:10.1038/nature09142 · Cited by 376 · see citing works
Wyatt, T. (2010) · Journal of Comparative Physiology · doi:10.1007/s00359-010-0564-y · Cited by 365 · see citing works
Papes, F., Logan, D. W., & Stowers, L. (2010) · Cell · doi:10.1016/j.cell.2010.03.037 · Cited by 360 · see citing works
Self-citationChemical and behavioural characterization of the rabbit mammary pheromone
Schaal, B., Coureaud, G., Langlois, D., Ginies, C., Sémon, E., & Perrier, G. (2003) · Nature · doi:10.1038/nature01739 · Cited by 351 · see citing works
Subsystem Organization of the Mammalian Sense of Smell
Munger, S. D., Leinders‐Zufall, T., & Zufall, F. (2008) · Annual Review of Physiology · doi:10.1146/annurev.physiol.70.113006.100608 · Cited by 317 · see citing works
Good memories of bad events in infancy
Sullivan, R. M., Landers, M., Yeaman, B., & Wilson, D. A. (2000) · Nature · doi:10.1038/35024156 · Cited by 315 · see citing works
Garlic Ingestion by Pregnant Women Alters the Odor of Amniotic Fluid
Mennella, J. A., Johnson, A., & Beauchamp, G. K. (1995) · Chemical Senses · doi:10.1093/chemse/20.2.207 · Cited by 314 · see citing works
Spehr, M., Kelliher, K. R., Li, X., Boehm, T. L. J., Leinders‐Zufall, T., & Zufall, F. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4939-05.2006 · Cited by 301 · see citing works
Loss-of-function mutations in sodium channel Nav1.7 cause anosmia
Weiss, J., Pyrski, M. M., Jacobi, E., Bufe, B., Willnecker, V., Schick, B., Zizzari, P., Gossage, S. J., Greer, C. A., Leinders‐Zufall, T., et al. (2011) · Nature · doi:10.1038/nature09975 · Cited by 297 · see citing works
First Suckling Response of the Newborn Albino Rat: The Roles of Olfaction and Amniotic Fluid
Teicher, M. H., & Blass, E. M. (1977) · Science · doi:10.1126/science.918660 · Cited by 282 · see citing works
Prenatal and postnatal determinants of the 1st suckling episode in albino rats
Pedersen, P. E., & Blass, E. M. (1982) · Developmental Psychobiology · doi:10.1002/dev.420150407 · Cited by 280 · see citing works
Deficits in sexual and aggressive behaviors in Cnga2 mutant mice
Mandiyan, V. S., Coats, J., & Shah, N. M. (2005) · Nature Neuroscience · doi:10.1038/nn1589 · Cited by 270 · 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
Changes in the sensory processing of olfactory signals induced by birth in sleep
Kendrick, K., Levy, F., & Keverne, E. (1992) · Science · doi:10.1126/science.1589766 · Cited by 244 · see citing works
Driving Opposing Behaviors with Ensembles of Piriform Neurons
Choi, G. B., Stettler, D. D., Kallman, B. R., Bhaskar, S., Fleischmann, A., & Axel, R. (2011) · Cell · doi:10.1016/j.cell.2011.07.041 · Cited by 232 · see citing works
Leinders‐Zufall, T., Cockerham, R. E., Michalakis, S., Biel, M., Garbers, D. L., Reed, R. R., Zufall, F., & Munger, S. D. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0704965104 · Cited by 228 · see citing works
Does the newborn baby find the nipple by smell?
Varendi, H., Porter, R. H., & Winberg, J. (1994) · The Lancet · doi:10.1016/s0140-6736(94)91645-4 · Cited by 224 · see citing works
Neurobiology of associative learning in the neonate: Early olfactory learning
Wilson, D. A., & Sullivan, R. M. (1994) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(05)80039-1 · Cited by 206 · see citing works
Pheromones, binding proteins and receptor responses in rodents
Novotný, M. V. (2003) · Biochemical Society Transactions · doi:10.1042/bst0310117 · Cited by 203 · see citing works
Suckling in Newborn Rats: Eliminated by Nipple Lavage, Reinstated by Pup Saliva
Teicher, M. H., & Blass, E. M. (1976) · Science · doi:10.1126/science.935878 · Cited by 200 · see citing works
Sullivan, R. M., Stackenwalt, G., Nasr, F., Lemon, C. H., & Wilson, D. A. (2000) · Behavioral Neuroscience · doi:10.1037/0735-7044.114.5.957 · Cited by 169 · see citing works
High-throughput microarray detection of olfactory receptor gene expression in the mouse
Zhang, X., Rogers, M. E., Tian, H., Zhang, X., Zou, D., Liu, J., Ma, M., Shepherd, G. M., & Firestein, S. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0405350101 · Cited by 168 · see citing works
Teicher, M. H., Stewart, W., Kauer, J., & Shepherd, G. (1980) · Brain Research · doi:10.1016/0006-8993(80)91237-8 · Cited by 165 · see citing works
Pheromonal release of suckling in rabbits does not depend on the vomeronasal organ
Hudson, R., & Distel, H. (1986) · Physiology & Behavior · doi:10.1016/0031-9384(86)90394-x · Cited by 163 · see citing works
Elemental representations of stimuli in associative learning.
Harris, J. A. (2006) · Psychological Review · doi:10.1037/0033-295x.113.3.584 · Cited by 158 · see citing works
Activation and odor conditioning of suckling behavior in 3-day-old albino rats.
Pedersen, P. E., Williams, C. L., & Blass, E. M. (1982) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.8.4.329 · Cited by 149 · see citing works
Unique neural circuitry for neonatal olfactory learning
Moriceau, S., & Sullivan, R. M. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.4578-03.2004 · Cited by 141 · see citing works
Functional development of the olfactory bulb and a unique glomerular complex in the neonatal rat
Greer, C. A., Stewart, W., Teicher, M. H., & Shepherd, G. M. (1982) · Journal of Neuroscience · doi:10.1523/jneurosci.02-12-01744.1982 · Cited by 140 · see citing works
Franks, K. M., & Isaacson, J. S. (2005) · Neuron · doi:10.1016/j.neuron.2005.05.024 · Cited by 138 · see citing works
Mice with a “Monoclonal Nose”: Perturbations in an Olfactory Map Impair Odor Discrimination
Fleischmann, A., Shykind, B., Sosulski, D. L., Franks, K. M., Glinka, M. E., Mei, D. F., Sun, Y., Kirkland, J., Mendelsohn, M. M., Albers, M. W., et al. (2008) · Neuron · doi:10.1016/j.neuron.2008.10.046 · Cited by 129 · see citing works
Maternal Behavior in the Laboratory Rat
Rosenblatt, J. S., & Siegel, H. I. (1980) · Springer eBooks · doi:10.1007/978-94-011-6287-6_7 · Cited by 118 · see citing works
Evidence for Olfactory Function in Utero
Pedersen, P. E., Stewart, W. B., Jr., Greer, C. A., & Shepherd, G. M. (1983) · Science · doi:10.1126/science.6867725 · Cited by 117 · see citing works
Effects of nasal ZnSO4 irrigation and olfactory bulbectomy on rat pups
Singh, P. J., Tucker, A. M., & Hofer, M. A. (1976) · Physiology & Behavior · doi:10.1016/0031-9384(76)90094-9 · Cited by 108 · see citing works
Todrank, J., Heth, G., & Restrepo, D. (2010) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2010.2314 · Cited by 104 · see citing works
Chemical Signals in Vertebrates 9
(2001) · Springer eBooks · doi:10.1007/978-1-4615-0671-3 · Cited by 104 · see citing works
A Pheromone That Rapidly Promotes Learning in the Newborn
Coureaud, G., Moncomble, A.-S., Montigny, D., Dewas, M., Perrier, G., & Schaal, B. (2006) · Current Biology · doi:10.1016/j.cub.2006.08.030 · Cited by 102 · see citing works
Jastreboff, P. J., Pedersen, P. E., Greer, C. A., Stewart, W. B., Jr., Kauer, J. S., Benson, T. E., & Shepherd, G. M. (1984) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.81.16.5250 · Cited by 77 · see citing works
Mammary Odor Cues and Pheromones
Schaal, B. (2010) · Vitamins and hormones · doi:10.1016/s0083-6729(10)83004-3 · Cited by 64 · see citing works
Garlic in the ovine fetal environment
Nolte, D. L., Provenza, F. D., Callan, R. J., & Panter, K. E. (1992) · Physiology & Behavior · doi:10.1016/0031-9384(92)90464-d · Cited by 63 · see citing works
Schaal, B., Coureaud, G., Doucet, S., Allam, M. D., Moncomble, A.-S., Montigny, D., Patris, B., & Holley, A. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.02.008 · Cited by 61 · see citing works
Molecular Biology Of Early Olfactory Memory: Figure 1.Preprint
Sullivan, R. M., & Wilson, D. A. (2003) · Learning & Memory · doi:10.1101/lm.58203 · Cited by 56 · see citing works
Maternal pheromone: A demonstration of its existence in the mouse (Mus musculus)☆
BREEN, M., & Leshner, A. I. (1977) · Physiology & Behavior · doi:10.1016/0031-9384(77)90269-4 · Cited by 51 · see citing works
Perception of odor blending mixtures in the newborn rabbit
Coureaud, G., Thomas‐Danguin, T., Berre, E. L., & Schaal, B. (2008) · Physiology & Behavior · doi:10.1016/j.physbeh.2008.05.018 · Cited by 49 · see citing works
Individual olfactory signatures as major determinants of early maternal discrimination in sheep
Porter, R. H., Lévy, F., Poindron, P., Litterio, M., Schaal, B., & Beyer, C. (1991) · Developmental Psychobiology · doi:10.1002/dev.420240302 · Cited by 47 · see citing works
Changes in the sensory processing of olfactory signals induced by birth in sleep
Kendrick, K. M., Lévy, F., & Keverne, E. B. (1992) · Science · doi:10.1126/science.256.5058.833 · Cited by 46 · see citing works
Nipple attachment and survival in neonatal olfactory bulbectomized rats
Risser, J. M., & Slotnick, B. M. (1987) · Physiology & Behavior · doi:10.1016/0031-9384(87)90042-4 · Cited by 45 · see citing works
Anatomic mapping of neuronal odor responses in the developing rat olfactory bulb
Guthrie, K. M., & Gall, C. M. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10452 · Cited by 32 · see citing works
Brain processing of the mammary pheromone in newborn rabbits
Charra, R., Datiche, F., Casthano, A., Gigot, V., Schaal, B., & Coureaud, G. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.09.008 · Cited by 27 · see citing works
Coureaud, G., Languille, S., Schaal, B., & Hars, B. (2009) · Learning & memory (Cold Spring Harbor, N.Y.) · doi:10.1101/lm.1434009 · Cited by 22 · see citing works
Aïn, S. A., Chraïti, A., Schaal, B., & Patris, B. (2011) · Developmental Psychobiology · doi:10.1002/dev.21003 · Cited by 19 · see citing works
The Role of the Main and Accessory Olfactory Systems in Prenatal Olfaction
Coppola, D. M. (2001) · Springer eBooks · doi:10.1007/978-1-4615-0671-3_25 · Cited by 7 · see citing works
Flagged first, then by citations
1 of the 69 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Liberles, S. D. (2013) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021113-170334 · Cited by 292 · see citing works
The perception of odor objects in everyday life: a review on the processing of odor mixtures
Thomas‐Danguin, T., Sinding, C., Romagny, S., Mountassir, F. E., Atanasova, B., Berre, E. L., Bon, A. L., & Coureaud, G. (2014) · Frontiers in Psychology · doi:10.3389/fpsyg.2014.00504 · Cited by 295 · see citing works
Kaur, A. W., Ackels, T., Kuo, T.-H., Cichy, A., Dey, S., Hays, C. K., Kateri, M., Logan, D. W., Marton, T. F., Spehr, M., et al. (2014) · Cell · doi:10.1016/j.cell.2014.02.025 · Cited by 207 · see citing works
Self-citationAversion and Attraction through Olfaction
Li, Q., & Liberles, S. D. (2015) · Current Biology · doi:10.1016/j.cub.2014.11.044 · Cited by 200 · see citing works
Neural circuits of social behaviors: Innate yet flexible
Wei, D., Talwar, V., & Lin, D. (2021) · Neuron · doi:10.1016/j.neuron.2021.02.012 · Cited by 185 · see citing works
Olfactory Circuitry and Behavioral Decisions
Mori, K., & Sakano, H. (2020) · Annual Review of Physiology · doi:10.1146/annurev-physiol-031820-092824 · Cited by 120 · see citing works
Olfaction scaffolds the developing human from neonate to adolescent and beyond
Schaal, B., Saxton, T. K., Loos, H. M., Soussignan, R., & Durand, K. (2020) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2019.0261 · Cited by 109 · see citing works
Female chemical signalling underlying reproduction in mammals
Coombes, H. A., Stockley, P., & Hurst, J. L. (2018) · Journal of Chemical Ecology · doi:10.1007/s10886-018-0981-x · Cited by 98 · see citing works
Variation in olfactory neuron repertoires is genetically controlled and environmentally modulated
Ibarra-Soria, X., Nakahara, T. S., Lilue, J., Jiang, Y., Trimmer, C., Souza, M. A. A., Netto, P. H. M., Ikegami, K., Murphy, N. R., Kusma, M., et al. (2017) · eLife · doi:10.7554/elife.21476 · Cited by 95 · see citing works
Self-citationOpendak, M., Gould, E., & Sullivan, R. (2017) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2017.02.002 · Cited by 94 · see citing works
Semin (2017) · doi:10.1177/1745691616676599 · Cited by 86 · see citing works
The genomic basis of vomeronasal-mediated behaviour
Ibarra-Soria, X., Levitin, M. O., & Logan, D. W. (2013) · Mammalian Genome · doi:10.1007/s00335-013-9463-1 · Cited by 85 · see citing works
Self-citationIntroduction to Chemical Signaling in Vertebrates and Invertebrates
Mucignat-Caretta, C. (2014) · CRC Press eBooks · doi:10.1201/b16511-6 · Cited by 86 · see citing works
Are mammal olfactory signals hiding right under our noses?
Apps, P. (2013) · Die Naturwissenschaften · doi:10.1007/s00114-013-1054-1 · Cited by 79 · see citing works
Development of the mammalian main olfactory bulb
Tufo, C., Poopalasundaram, S., Dorrego-Rivas, A., Ford, M. C., Graham, A., & Grubb, M. S. (2022) · Development · doi:10.1242/dev.200210 · Cited by 75 · see citing works
Raineki, C., Opendak, M. M., Sarro, E. C., Showler, A., Bui, K., McEwen, B. S., Wilson, D. A., & Sullivan, R. M. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1907170116 · Cited by 76 · see citing works
State-dependent responses to sex pheromones in mouse
Stowers, L., & Liberles, S. D. (2016) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2016.04.001 · Cited by 75 · see citing works
Self-citationPerry, R. E., Finegood, E. D., Braren, S. H., DeJoseph, M. L., Putrino, D. F., Wilson, D. A., Sullivan, R. M., Raver, C. C., Blair, C., & Family Life Project Key Investigators (2018) · Development and Psychopathology · doi:10.1017/s095457941800007x · Cited by 74 · see citing works
Processing by the main olfactory system of chemosignals that facilitate mammalian reproduction
Baum, M. J., & Cherry, J. A. (2014) · Hormones and Behavior · doi:10.1016/j.yhbeh.2014.06.003 · Cited by 73 · see citing works
Chemosensory signals and their receptors in the olfactory neural system
Ihara, S., Yoshikawa, K., & Touhara, K. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.08.063 · Cited by 70 · see citing works
Olfaction: An Overlooked Sensory Modality in Applied Ethology and Animal Welfare
Nielsen, B. L., Jezierski, T. A., Bolhuis, J. E., Amo, L., Rosell, F., Oostindjer, M., Christensen, J. W., McKeegan, D. E. F., Wells, D. L., & Hepper, P. G. (2015) · Frontiers in Veterinary Science · doi:10.3389/fvets.2015.00069 · Cited by 67 · see citing works
Aïn, S. A., Perry, R. E., Nuñez, B. S., Kayser, K. E., Hochman, C., Brehman, E., LaComb, M., Wilson, D. A., & Sullivan, R. M. (2016) · Social Neuroscience · doi:10.1080/17470919.2016.1159605 · Cited by 63 · see citing works
Early handling and repeated cross-fostering have opposite effect on mouse emotionality
Luchetti, A., Oddi, D., Lampis, V., Centofante, E., Felsani, A., Battaglia, M., & D'Amato, F. R. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00093 · Cited by 61 · see citing works
Mutual mother-infant recognition in mice: The role of pup ultrasonic vocalizations
Mogi, K., Takakuda, A., Tsukamoto, C., Ooyama, R., Okabe, S., Koshida, N., Nagasawa, M., & Kikusui, T. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.08.044 · Cited by 54 · see citing works
FitzGerald, B. J., Richardson, K., & Wesson, D. W. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00081 · Cited by 51 · see citing works
Innate and learned aspects of pheromone-mediated social behaviours
Beny, Y., & Kimchi, T. (2014) · Animal Behaviour · doi:10.1016/j.anbehav.2014.09.014 · Cited by 49 · see citing works
The odour of human milk: Its chemical variability and detection by newborns
Loos, H. M., Reger, D., & Schaal, B. (2018) · Physiology & Behavior · doi:10.1016/j.physbeh.2018.11.008 · Cited by 49 · see citing works
Olfactory Stimulation Regulates the Birth of Neurons That Express Specific Odorant Receptors
van der Linden, C. J., Gupta, P., Bhuiya, A. I., Riddick, K. R., Hossain, K., & Santoro, S. W. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108210 · Cited by 49 · see citing works
Newborn mice form lasting CA2-dependent memories of their mothers
Laham, B. J., Diethorn, E. J., & Gould, E. (2021) · Cell Reports · doi:10.1016/j.celrep.2020.108668 · Cited by 45 · see citing works
Prenatal and Postnatal Human Olfactory Development: Influences on Cognition and Behavior
Schaal, B. (2015) · doi:10.1002/9781118971758.ch14 · Cited by 48 · see citing works
Developmental regulation of olfactory circuit formation in mice
Sakano, H. (2020) · Development Growth & Differentiation · doi:10.1111/dgd.12657 · Cited by 47 · see citing works
Gretenkord, S., Kostka, J. K., Hartung, H., Watznauer, K., Fleck, D., Minier-Toribio, A. M., Spehr, M., & Hanganu‐Opatz, I. L. (2019) · PLoS Biology · doi:10.1371/journal.pbio.2006994 · Cited by 44 · see citing works
Suckling, Feeding, and Swallowing: Behaviors, Circuits, and Targets for Neurodevelopmental Pathology
Maynard, T. M., Zohn, I. E., Moody, S. A., & LaMantia, A. (2020) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-100419-100636 · Cited by 44 · see citing works
CD36 is involved in oleic acid detection by the murine olfactory system
Oberland, S., Ackels, T., Gaab, S., Pelz, T., Spehr, J., Spehr, M., & Neuhaus, E. M. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00366 · Cited by 43 · see citing works
Selective Attention Controls Olfactory Decisions and the Neural Encoding of Odors
Carlson, K. S., Gadziola, M. A., Dauster, E. S., & Wesson, D. W. (2018) · Current Biology · doi:10.1016/j.cub.2018.05.011 · Cited by 44 · see citing works
Bryche, B., Baly, C., & Meunier, N. (2021) · Cell and Tissue Research · doi:10.1007/s00441-021-03467-y · Cited by 43 · see citing works
Sensory factors involved in mother-young bonding in sheep: a review
Mora‐Medina, P., Orihuela, A., Arch-Tirado, E., Roldán-Santiago, P., Terrazas, A., & Mota‐Rojas, D. (2016) · Veterinární Medicína · doi:10.17221/255/2014-vetmed · Cited by 43 · see citing works
Loss of transient receptor potential channel 5 causes obesity and postpartum depression
Li, Y., Cacciottolo, T. M., Yin, N., He, Y., Liu, H., Liu, H., Yang, Y., Henning, E., Keogh, J. M., Lawler, K., et al. (2024) · Cell · doi:10.1016/j.cell.2024.06.001 · Cited by 41 · see citing works
Nielsen, B. L. (2018) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2018.04.013 · Cited by 39 · see citing works
Green, W. W., Uytingco, C. R., Ukhanov, K., Kolb, Z., Moretta, J. C., McIntyre, J. C., & Martens, J. R. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.0084-18.2018 · Cited by 36 · see citing works
The role of the NMD factor UPF3B in olfactory sensory neurons
Tan, K., Jones, S. H., Lake, B. B., Chousal, J. N., Shum, E. Y., Zhang, L., Chen, S., Sohni, A., Pandya, S., Gallo, R. L., et al. (2020) · eLife · doi:10.7554/elife.57525 · Cited by 36 · see citing works
Chen, Y.-N., Kostka, J. K., Bitzenhofer, S. H., & Hanganu‐Opatz, I. L. (2023) · Current Biology · doi:10.1016/j.cub.2023.08.072 · Cited by 36 · see citing works
The Nipple: A Simple Intersection of Mammary Gland and Integument, but Focal Point of Organ Function
小山, 幸., Wu, H.-J., Easwaran, T. P., Thopady, S., & Foley, J. (2013) · Journal of Mammary Gland Biology and Neoplasia · doi:10.1007/s10911-013-9289-1 · Cited by 37 · see citing works
Inoue, N., Nishizumi, H., Ooyama, R., Mogi, K., Nishimori, K., Kikusui, T., & Sakano, H. (2021) · eLife · doi:10.7554/elife.65078 · Cited by 35 · see citing works
Nielsen, B., Rampin, O., Meunier, N., & Bombail, V. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00226 · Cited by 33 · see citing works
Neurobiology of secure infant attachment and attachment despite adversity: a mouse model
Roth, T. L., Raineki, C., Salstein, L., Perry, R. E., Sullivan-Wilson, T., Sloan, A., Lalji, B., Hammock, E. A. D., Wilson, D. A., Levitt, P. R., et al. (2013) · Genes Brain & Behavior · doi:10.1111/gbb.12067 · Cited by 32 · see citing works
Introduction to Chemical Signaling in Vertebrates and Invertebrates
Wyatt, T. D. (2014) · Frontiers in neuroscience · doi:10.1201/b16511-2 · Cited by 32 · see citing works
Chemical signals ‘selected for’ newborns in mammals
Schaal, B., & Aïn, S. A. (2014) · Animal Behaviour · doi:10.1016/j.anbehav.2014.08.022 · Cited by 30 · see citing works
Dinçkol, Ö., Fuentes, B., Tartaglione, A. M., Pino, A., Calamandrei, G., & Ricceri, L. (2022) · NeuroToxicology · doi:10.1016/j.neuro.2022.05.007 · Cited by 25 · see citing works
Defining immediate effects of sensitive periods on infant neurobehavioral function
Sullivan, R. M., & Opendak, M. M. (2020) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2020.08.006 · Cited by 23 · see citing works
Mazorra-Alonso, M., Tomás, G., & Soler, J. J. (2021) · Biology · doi:10.3390/biology10040274 · Cited by 24 · see citing works
How the sense of smell influences cognition throughout life
Kostka, J. K., & Bitzenhofer, S. H. (2022) · e-Neuroforum · doi:10.1515/nf-2022-0007 · Cited by 23 · see citing works
Maurya, D. K., & Menini, A. (2013) · Developmental Neurobiology · doi:10.1002/dneu.22159 · Cited by 24 · see citing works
Visualizing the Engram: Learning Stabilizes Odor Representations in the Olfactory Network
Shakhawat, A. M., Gheidi, A., Hou, Q., Dhillon, S. K., Marrone, D. F., Harley, C. W., & Yuan, Q. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.3396-14.2014 · Cited by 24 · see citing works
Maternal Olfactory Cues Synchronize the Circadian System of Artificially Raised Newborn Rabbits
Montúfar‐Chaveznava, R., Trejo-Muñoz, L., Hernández-Campos, O., Navarrete, E., & Caldelas, I. (2013) · PLoS ONE · doi:10.1371/journal.pone.0074048 · Cited by 21 · see citing works
Dynamic developmental changes in neurotransmitters supporting infant attachment learning
Colombel, N., Ferreira, G., Sullivan, R. M., & Coureaud, G. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105249 · Cited by 20 · see citing works
Myelination of the developing lateral olfactory tract and anterior commissure
Collins, L. N., Hill, D. L., & Brunjes, P. C. (2018) · The Journal of Comparative Neurology · doi:10.1002/cne.24452 · Cited by 19 · see citing works
Klaey‐Tassone, M., Durand, K., Damon, F., Heyers, K., Mezraï, N., Patris, B., Sagot, P., Soussignan, R., & Schaal, B. (2020) · American Journal of Human Biology · doi:10.1002/ajhb.23521 · Cited by 19 · see citing works
Epac activation initiates associative odor preference memories in the rat pupPreprint
Grimes, M. T., Powell, M. F., Gutierrez, S. M., Darby‐King, A., Harley, C. W., & McLean, J. H. (2015) · Learning & Memory · doi:10.1101/lm.037101.114 · Cited by 18 · see citing works
Olfactory‐driven beta band entrainment of limbic circuitry during neonatal development
Kostka, J. K., & Hanganu‐Opatz, I. L. (2023) · The Journal of Physiology · doi:10.1113/jp284401 · Cited by 15 · see citing works
A nasal chemosensation–dependent critical window for somatosensory development
Cai, L., Argunşah, A. Ö., Damilou, A., & Karayannis, T. (2024) · Science · doi:10.1126/science.adn5611 · Cited by 17 · see citing works
Lam, R. S., & Mombaerts, P. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12240 · Cited by 17 · see citing works
Cerebellar contribution to locomotor behavior: A neurodevelopmental perspective
Sathyanesan, A., & Gallo, V. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.04.016 · Cited by 15 · see citing works
Aïn, S. A., Mingioni, M., Patris, B., & Schaal, B. (2014) · Developmental Psychobiology · doi:10.1002/dev.21220 · Cited by 15 · see citing works
Cullere, M., Macchione, A. F., Haymal, B., Paradelo, M., Langer, M. D., Spear, N. E., & Molina, J. C. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.10.017 · Cited by 15 · see citing works
Neural representations of kinship
Clemens, A. M., & Brecht, M. (2021) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2021.02.007 · Cited by 15 · see citing works
Deconstructing the mouse olfactory percept through an ethological atlas
Manoel, D., Makhlouf, M., Arayata, C. J., Sathappan, A., Da'as, S. I., Abdelrahman, D., Selvaraj, S., Hasnah, R., Mainland, J. D., Gerkin, R. C., et al. (2021) · Current Biology · doi:10.1016/j.cub.2021.04.020 · Cited by 15 · see citing works
Flavors mothers taught us in the womb and in milk
Schaal, B. (2022) · Elsevier eBooks · doi:10.1016/b978-0-323-89903-1.00025-6 · Cited by 14 · see citing works
Wang, D. C., Santos-Valencia, F., Song, J. H., Franks, K. M., & Luo, L. (2024) · Neuron · doi:10.1016/j.neuron.2024.06.007 · Cited by 14 · see citing works
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Li, R., Diao, H., Zhao, F., Xiao, S., Zowalaty, A. E. E., Dudley, E. A., Mattson, M. P., & Ye, X. (2015) · Endocrinology · doi:10.1210/en.2015-1389 · Cited by 14 · see citing works
Behavioral Assays in the Study of Olfaction: A Practical Guide
Papes, F., Nakahara, T. S., & Camargo, A. P. (2018) · Methods in molecular biology · doi:10.1007/978-1-4939-8609-5_21 · Cited by 13 · see citing works
Functional development of olfactory tubercle domains during weaning period in mice
Murofushi, W., Mori, K., Murata, K., & Yamaguchi, M. (2018) · Scientific Reports · doi:10.1038/s41598-018-31604-1 · Cited by 14 · see citing works
Olfaction and olfactory-mediated behaviour in psychiatric disease models
Huckins, L. M., Logan, D. W., & Sánchez-Andrade, G. (2013) · Cell and Tissue Research · doi:10.1007/s00441-013-1617-7 · Cited by 14 · see citing works
Self-citationCircuit formation and sensory perception in the mouse olfactory system
Mori, K., & Sakano, H. (2024) · Frontiers in Neural Circuits · doi:10.3389/fncir.2024.1342576 · Cited by 13 · see citing works
Sampling, identification and sensory evaluation of odors of a newborn baby’s head and amniotic fluid
Uebi, T., Hariyama, T., Suzuki, K., Kanayama, N., Nagata, Y., Ayabe‐Kanamura, S., Yanase, S., Ohtsubo, Y., & Ozaki, M. (2019) · Scientific Reports · doi:10.1038/s41598-019-49137-6 · Cited by 13 · see citing works
Caballero, I., Mbouamboua, Y., Weise, S., López-Gálvez, R., Couralet, M., Fleurot, I., Pons, N., Barrera-Conde, M., Playan, N. Q., Keller, M., et al. (2025) · Science Advances · doi:10.1126/sciadv.ads1568 · Cited by 12 · see citing works
Chang, H., Pan, Y., Landrette, S. F., Ding, S., Dong, Y., Liu, L., Tian, L., Chai, H., Li, P., Li, D., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1906354116 · Cited by 12 · see citing works
Dewaele, A., Persuy, M., Badonnel, K., Meunier, N., Durieux, D., Castille, J., Favreau-Peigné, A., & Baly, C. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.02.026 · Cited by 12 · see citing works
Perrone, S., Beretta, V., Tataranno, M. L., Tan, S., Shi, Z., Scarpa, E., Dell’Orto, V., Ravenda, S., Petrolini, C., Brambilla, M., et al. (2025) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2025.106029 · Cited by 11 · see citing works
How amniotic fluid shapes early odor-guided responses to colostrum and milk (and more)
Schaal, B. (2016) · Elsevier eBooks · doi:10.1016/b978-0-08-100295-7.00002-5 · Cited by 11 · see citing works
Uncovering the mouse olfactory long non-coding transcriptome with a novel machine-learning model
Camargo, A. P., Nakahara, T. S., Firmino, L. E. R., Netto, P. H. M., do Nascimento, J. B. P., Donnard, E. R., Galante, P. A. F., Carazzolle, M. F., Malnic, B., & Papes, F. (2019) · DNA Research · doi:10.1093/dnares/dsz015 · Cited by 11 · see citing works
Aïn, S. A., Goudet, C., Schaal, B., & Patris, B. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2015.04.035 · Cited by 11 · see citing works
Preconfigured architecture of the developing mouse brain
Chini, M., Hnida, M., Kostka, J. K., Chen, Y., & Hanganu‐Opatz, I. L. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114267 · Cited by 10 · see citing works
The Evolution of Kin Discrimination Across the Tree of Life
Green, J. P., Biernaskie, J. M., Mee, M., & Leedale, A. E. (2024) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev-ecolsys-102221-051057 · Cited by 10 · see citing works
Lévy, F., Badonnel, K., Bertin, A., Cornilleau, F., Durieux, D., Meurisse, M., Nowak, R., Parias, C., Persuy, M. A., & Baly, C. (2020) · Physiology & Behavior · doi:10.1016/j.physbeh.2020.113166 · Cited by 10 · see citing works
Neurodevelopment and phenotype-modulating functions of S100B protein: A pilot study
Davydov, D. M., Av, L., Morozov, S., Gribova, I., & Murashev, A. N. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.12.037 · Cited by 11 · see citing works
Role of Olfaction for Eating Behavior
Fadool, D. A., & Kolling, L. J. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.23770-x · Cited by 9 · see citing works
The underexplored role of chemical communication in the domestic horse, Equus caballus
Guarneros, M., Sánchez‐García, O., Martı́nez–Gómez, M., & Arteaga, L. (2020) · Journal of Veterinary Behavior · doi:10.1016/j.jveb.2020.05.008 · Cited by 10 · see citing works
Stowers, L., & Spehr, M. (2015) · doi:10.1002/9781118971758.ch51 · Cited by 10 · see citing works
Self-citationThe complexity of pheromone-mediated behaviour in mammals
Logan, D. (2015) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2014.10.011 · Cited by 8 · see citing works
Self-citationPostnatal Development of Centrifugal Inputs to the Olfactory Bulb
Kostka, J. K., & Bitzenhofer, S. H. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.815282 · Cited by 9 · see citing works
de Vallière, A., Lopes, A. C., Addorisio, A., Gilliand, N., Nenniger-Tosato, M., Wood, D., Brechbühl, J., & Broillet, M.-C. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.1026373 · Cited by 8 · see citing works
Chemical Identification of “Maternal Signature Odors” in Rat
Sréng, L., Temime‐Roussel, B., Wortham, H., & Mourre, C. (2016) · Chemical Senses · doi:10.1093/chemse/bjw124 · Cited by 8 · see citing works
Nielsen, B. L., Jérôme, N., Saint-Albin, A., Joly, F., Rabot, S., & Meunier, N. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.09.018 · Cited by 8 · see citing works
The mouse olfactory peduncle 4: Development of synapses, perineuronal nets, and capillaries
Collins, L. N., & Brunjes, P. C. (2019) · The Journal of Comparative Neurology · doi:10.1002/cne.24778 · Cited by 8 · see citing works
Odor and Pheromone Molecules, Receptors, and Behavioral Responses
Touhara, K. (2014) · Springer eBooks · doi:10.1007/978-4-431-54376-3_2 · Cited by 4 · see citing works
Kostka, J. K., Gretenkord, S., Spehr, M., & Hanganu‐Opatz, I. L. (2020) · The Journal of Physiology · doi:10.1113/jp280131 · Cited by 7 · see citing works
Gretenkord, S., Kostka, J. K., Hartung, H., Watznauer, K., Fleck, D., Minier-Toribio, A. M., Spehr, M., & Hanganu‐Opatz, I. L. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/352054 · Cited by 7 · see citing works
Developmental Olfactory Dysfunction and Abnormal Odor Memory in Immune-Challenged Disc1 +/− Mice
Parbst, F., Kostka, J. K., Günther, A., Chen, Y., Hanganu‐Opatz, I. L., & Bitzenhofer, S. H. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.1007-24.2025 · Cited by 6 · see citing works
Nutrient-dependent/pheromone-controlled adaptive evolution: a model
Kohl, J. (2013) · Socioaffective Neuroscience & Psychology · doi:10.3402/snp.v3i0.20553 · Cited by 7 · see citing works
- Authors
- Logan, D. W., Brunet, L. J., Webb, W. R., Cutforth, T., Ngai, J., & Stowers, L.
- Affiliations
- Scripps Research Institute (US)
- University of California, Berkeley (US)
- University of California, Irvine (US)
- Corresponding author
- Stowers, Lisa
- Venue
- Current Biology
- Publisher
- Elsevier BV
- Published
- 2012-11
- Volume
- 22
- Issue
- 21
- Pages
- 1998-2007
- ISSN
- 0960-9822 (ISSN-L)
- PMC
- PMC3494771
- OpenAlex
- W2131074370
- Cited by
- 148
- References
- 69
- Citations by year
- 2026: 4 · 2025: 11 · 2024: 10 · 2023: 6 · 2022: 6 · 2021: 8 · 2020: 15 · 2019: 10 · 2018: 17 · 2017: 5 · 2016: 11 · 2015: 14 · 2014: 16 · 2013: 14 · 2012: 1
- FWCI
- 8.03
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Current Biology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Wellcome Trust (098051)
- National Institute on Deafness and Other Communication Disorders (R01DC009413, R01DC006885)
- Topics
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Keywords
- innate behavior, pheromones, neonatal behavior, sensory neurons, olfactory signaling
- MeSH terms
- Amniotic Fluid, Animals, Animals, Suckling, Behavior, Animal, Cesarean Section, Cues, Female, Lactation, Learning, Mice, Inbred BALB C, Mice, Inbred C57BL, Odorants, Pheromones, Sensory Receptor Cells, Smell, Mice, Knockout, Recognition, Psychology, Mice, Cyclic Nucleotide-Gated Cation Channels, Metabolomics
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