How does a newly born mouse get to the nipple? Odor substrates eliciting first nipple grasping and sucking responses

Developmental Psychobiology

Volumn 55, Issue 8, 2013, Pages 888-901

  Al Aïn, Syrina ^a   Belin, Laurine ^a   Schaal, Benoist ^a   Patris, Bruno ^a  

^a UNIVERSITÉ DE BOURGOGNE   (France)

Author keywords

Amniotic fluid; Colostrum; Milk; Mother infant interactions; Mouse (Mus musculus); Newborn; Olfaction; Saliva; Urine

Indexed keywords

MAMMALIA; MURINAE; MUS; MUS MUSCULUS;

AMNION FLUID; ANIMAL; ARTICLE; ASSOCIATION; COLOSTRUM; FEMALE; LACTATION; MILK; MOTHER-INFANT INTERACTIONS; MOUSE; MOUSE (MUS MUSCULUS); NEWBORN; NIPPLE; ODOR; PHYSIOLOGY; SALIVA; SMELLING; SPRAGUE DAWLEY RAT; SUCKING; SUCKLING ANIMAL; URINE;

AMNIOTIC FLUID; COLOSTRUM; MILK; MOTHER-INFANT INTERACTIONS; MOUSE (MUS MUSCULUS); NEWBORN; OLFACTION; SALIVA; URINE;

ANIMALS; ANIMALS, NEWBORN; ANIMALS, SUCKLING; CUES; FEMALE; LACTATION; MICE; MILK; NIPPLES; ODORS; RATS, SPRAGUE-DAWLEY; SMELL; SUCKING BEHAVIOR;

EID: 84886095436     PISSN: 00121630     EISSN: 10982302     Source Type: Journal    
DOI: 10.1002/dev.21082     Document Type: Article

References (82)

1. Al Aïn, S., Chraïti, A., Schaal, B., & Patris, B. (in press). Orientation of newborn mice to lactating females: Biological substrates of semiochemical interest. Developmental Psychobiology, DOI: 10.1002/dev.21003
2. Alberts, J. R., & Ronca, A. E. (in press). The experience of being born: A natural context for learning to suck. International Journal of Pediatrics.
3. Arias, C., & Chotro, M. G. (2007). Amniotic fluid can act as an appetitive unconditioned stimulus in preweanling rats. Developmental Psychobiology, 49, 139-149.
4. Armstrong, C. M., DeVito, L. M., & Cleland, T. A. (2006). One-trial associative odor learning in neonatal mice. Chemical Senses, 31, 343-349.
5. Blass, E. M. (1990). Suckling: Determinants, changes, mechanisms, and lasting impressions. Developmental Psychology, 26, 520-533.
6. Blass, E. M., & Teicher, M. H. (1980). Suckling. Science, 210, 15-22.
7. Bouslama, M., Durand, E., Chauviere, L., Van den Bergh, O., & Gallego, J. (2005). Olfactory classical conditioning in newborn mice. Behavioural Brain Research, 161, 102-106.
8. Brake, S. C. (1981). Suckling infant rats learn a preference for a novel olfactory stimulus paired with milk delivery. Science, 211, 506-508.
9. Büttner, A. (2002). Influence of human saliva on odorant concentrations. 2. Aldehydes, alcohols, 3-alkyl-2-methoxypyrazines, methoxyphenols, and 3-hydroxy-4, 5-dimethyl-2(5H)-furanone. Journal of Agricultural and Food Chemistry, 50, 7105-7110.
10. Cheslock, S. J., Varlinskaya, E. I., Petrov, E. S., & Spear, N. E. (2000). Rapid and robust olfactory conditioning with milk before suckling experience: Promotion of nipple attachment in the newborn rat. Behavioral Neuroscience, 114, 484-495.
11. Coppola, D. M., & Millar, L. C. (1997). Olfaction in utero: Behavioral studies of the mouse fetus. Behavioural Processes, 39, 53-68.
12. Coppola, D. M., & O'Connell, R. J. (1989). Stimulus access to olfactory and vomeronasal receptors in utero. Neuroscience Letters, 106, 241-248.
13. Coureaud, G., Schaal, B., Langlois, D., & Perrier, G. (2001). Orientation response of newborn rabbits to odours of lactating females: Relative effectiveness of surface and milk cues. Animal Behaviour, 61, 153-162.
14. Coureaud, G., Schaal, B., Hudson, R., Orgeur, P., & Coudert, P. (2002). Transnatal olfactory continuity in the rabbit: Behavioral evidence and short-term consequence of its disruption. Developmental Psychobiology, 40, 372-390.
15. Coureaud, G., Charra, R., Datiche, F., Sinding, C., Thomas-Danguin, T., Languille, S., ... Schaal, B. (2010). A pheromone to behave, a pheromone to learn: The rabbit mammary pheromone. Journal of Comparative Physiology A, 196, 779-790.
16. Dollinger, M. J., Holloway, W. R., & Denenberg, V. H. (1978). Nipple attachment in rats during the first 24 hours of life. Journal of Comparative and Physiological Psychology, 92, 619-626.
17. Doucet, S., Soussignan, R., Sagot, P., & Schaal, B. (2007). The "smellscape" of mother's breast: Effects of odor masking and selective unmasking on neonatal arousal, oral and visual responses. Developmental Psychobiology, 49, 129-138.
18. Doucet, S., Soussignan, R., Sagot, P., & Schaal, B. (2009). The secretion of areolar (Montgomery's) glands from lactating women elicits selective, unconditional responses in neonates. PLoS ONE, 4, e7579.
19. Dragatsis, I., Scott, Z., & Dietrich, P. (2004). Huntingtin-associated protein 1 (Hap1) mutant mice bypassing the early postnatal lethality are neuroanatomically normal and fertile but display growth retardation. Human Molecular Genetics, 13, 3115-3125.
20. Durand, E., Dauger, S., Vardon, G., Gressens, P., Gaultier, C., De Schonen, S., & Gallego, J. (2003). Classical conditioning of breathing pattern after two acquisition trials in 2-day-old mice. Journal of Applied Physiology, 94, 812-818.
21. Gabe, M. (1956). Contribution à l'histogénèse des glandes salivaires chez la souris. Cell and Tissue Research, 45, 74-95.
22. Harvey, P. J., & Mann, M. A. (1987). Pregnancy-induced autogrooming in mice: The effects of nipple removal. Developmental Psychobiology, 20, 593-602.
23. Hedrich, H. J., & Bullock, G. (Ed.) (2004). The laboratory mouse. New York, CA: Elsevier-Academic Press.
24. Hongo, T., Hakuba, A., Shiota, K., & Naruse, I. (2000). Suckling dysfunction caused by defects in the olfactory system in genetic arhinencephaly mice. Biology of the Neonate, 78, 293-299.
25. Hofer, M. A., Shair, H., & Singh, P. (1976). Evidence that maternal ventral skin substances promote suckling in infant rats. Physiology & Behavior, 17, 131-136.
26. Hudson, R., & Distel, H. (1983). Nipple location by newborn rabbits: Behavioural evidence for pheromonal guidance. Behaviour, 82, 260-275.
27. Hurst, J. L. (2009). Female recognition and assessment of males through scent. Behavioural Brain Research, 200, 295-303.
28. Johanson, I. B., & Hall, W. G. (1979). Appetitive learning in 1-day-old rat pups. Science, 205, 419-421.
29. Johanson, I. B., & Teicher, M. H. (1980). Classical conditioning of an odor preference in 3-day-old rats. Behavioral and Neural Biology, 29, 132-136.
30. Keil, W., von Stralendorff, F., & Hudson, R. (1990). A behavioral bioassay for analysis of rabbit nipple-search pheromone. Physiology & Behavior, 47, 525-529.
31. Keller, M., Baum, M. J., & Bakker, J. (2008). Olfactory control of sex-recognition and sexual behavior in mice. In J. L. Hurst, R. J. Beynon, S. C. Roberts, & T. D. Wyatt (Eds.), Chemical signals in vertebrates, Vol. 11 (pp. 241-250). Berlin: Springer Verlag.
32. Keller, M., Baum, M. J., Brock, O., Brennan, P. A., & Bakker, J. (2009). The main and accessory olfactory systems interact in the control of mate recognition and sexual behavior. Behavioural Brain Research, 200, 268-276.
33. Kodama, N. (1990). Preference for amniotic fluid in newborn mice. Annual Meeting of the International Society for Developmental Psychobiology, Cambridge, UK.
34. Koizumi, M., Horiguchi, K., Tomita, Y., Kato, Y., & Harigaya, T. (2003). Prolactin gene expression in the mouse nipple. The Journal of Reproduction and Development, 49, 465-472.
35. König, B., & Markl, H. (1987). Maternal care in house mice. Behavioral Ecology and Sociobiology, 20, 1-9.
36. Korthank, A. J., & Robinson, S. R. (1998). Effects of amniotic fluid on opioid activity and fetal responses to chemosensory stimuli. Developmental Psychobiology, 33, 235-248.
37. Laska, M., Hudson, R., & Distel, H. (1990). Sensitivity to biologically relevant odours may exceed the sum of component thresholds. ChemoEcology, 1, 651-662.
38. Marlier, L., & Schaal, B. (2005). Human newborns prefer human milk: Conspecific milk odor is attractive without postnatal exposure. Child Development, 76, 155-168.
39. Martinez-Garcia, F., Martinez-Ricos, J., Augustin-Pavon, C., Martinez-Hernandez, J., Novejarque, A., & Lanuza, E. (2009). Refining the dual olfactory hypothesis: Pheromone reward and odour experience. Behavioural Brain Research, 200, 277-286.
40. Mendez-Gallardo, V., & Robinson, S. R. (2011). Amniotic fluid and milk odor evoke crawling locomotion in the newborn rat. Presented at 44th Annual Meeting of the International Society for Developmental Psychobiology, Washington, USA.
41. Miller, S. S., & Spear, N. E. (2009). Olfactory learning in the rat immediately after birth: Unique salience of first odors. Developmental Psychobiology, 51, 488-504.
42. Moncho-Bogani, J., Lanuza, E., Hernandez, A., Novejarque, A., & Martinez-Gomez, F. (2002). Attractive properties of sexual pheromones in mice: Innate or learned ? Physiology and Behavior, 77, 167-176.
43. Moncomble, A. S., Coureaud, G., Quennedey, B., Langlois, D., Perrier, G., Brossut, R., & Schaal, B. (2005). The mammary pheromone of the rabbit: Where does it come from? Animal Behaviour, 69, 29-38.
44. Müller-Schwarze, D. (2006). Chemical ecology of vertebrates. Cambridge, UK: Cambridge University Press.
45. Müller-Schwarze, D. M., & Houlihan, D. (1991). Pheromonal activity of single castoreum constituents in Beaver, Castor Canadensis. Journal of Chemical Ecology, 17, 715-734.
46. Nien, C. J., Paugh, J. R., Massei, S., Wahlert, A. J., Kao, W. W., & Jester, J. V. (2009). Age-related changes in the meibomian gland. Experimental Eye Research, 89, 1021-1027.
47. Nejsum, L. N., Praetorius, J., & Nielsen, S. (2005). NKCC1 and NHE1 are abundantly expressed in the basolateral plasma membrane of secretory coil cells in rat, mouse, and human sweat glands. American Journal of Physiology, Cell Physiology, 289, C333-C340.
48. Nolte, D. L., & Mason, J. R. (1995). Maternal ingestion of ortho-aminoacetophenone during gestation affects intake by offspring. Physiology & Behavior, 58, 925-928.
49. Oostindjer, M., Al Aïn, S., Patris, B., Cadiou, H., Grosmaître, X., & Schaal, B. (2011). Psychobiological effects of perinatal exposure to odorants in mice. Part II: Behavioural alterations Chemical Senses, 36, E76-E77.
50. Patris, B., Lesimple, C., & Schaal, B. (2009). Perinatal odour learning in mice: Impact on odour preference and intake. Presented at the 31st International Ethological Conference, Rennes, France.
51. Pedersen, P. E., & Blass, E. M. (1981). Olfactory control over suckling in albino rats. In R. N. Aslin, J. R. Alberts, & M. R. Pedersen (Eds.), The development of perception: Psychobiological perspectives (pp. 359-381). New York: Academic Press.
52. Pedersen, P. A., & Blass, E. M. (1982). Prenatal and postnatal determinants of the 1st suckling episode in albino rats. Developmental Psychobiology, 15, 349-355.
53. Pedersen, P. E., Williams, C. L., & Blass, E. M. (1982). Activation and odor conditioning of suckling behavior in 3-day-old albino rats. Journal of Experimental Psychology: Animal Behavior Processes, 8, 329-341.
54. Putter, J., & Sagner, C. (1973). Chemical studies to detect residues of xylazine hydrochloride. Veterinary Medical Review 2, 145-159.
55. Raimbault, C., Saliba, E., & Porter, R. H. (2007). The effect of the odor of mother's milk on breastfeeding behaviour of premature infants. Acta Paediatrica, 96, 368-371.
56. Roberts, S. A., Simpson, D. M., Armstrong, S. D., Davidson, A. J., Robertson, D. H., McLean, L., ... Hurst, J. L. (2010). Darcin: A male pheromone that stimulates female memory and sexual attraction to an individual male's odour. BMC Biology, 8, 75.
57. Robinson, S. R., & Mendez-Gallardo, V. (2010). Amniotic fluid as an extended milieu intérieur. In K. E. Hood, C. T. Halper, G. Greenberg, & R. M. Lerner (Eds.), Handbook of developmental science, behavior, and genetics (pp. 234-284). New York: Blackwell.
58. Ronca, A. E., & Alberts, J. R. (1994). Sensory factors associated with gestation and parturition evoke cardiac and behavioral responses in fetal rats. Psychobiology, 55, 270-282.
59. Ronca, A. E., & Alberts, J. R. (1995). Maternal contributions to fetal experience and the transition from prenatal to postnatal life. In J.-P. Lecanuet, N. Krasnegor, & W. P. Smotherman (Eds.), Fetal behavior: A psychobiological perspective (pp 331-351). Hillsdale, NJ: Lawrence Erlbaum Associates.
60. Rosenblatt, J. S. (1983). Olfaction mediates developmental transitions in the altricial newborn of selected species of mammals. Developmental Psychobiology, 16, 347-375.
61. Schaal, B. (2005). From amnion to colostrum to milk: Bridging in early developmental transitions. In B. Hopkins & S. Johnson (Eds.), Prenatal development of postnatal functions (pp. 52-102). Westport, CT: Praeger.
62. Schaal, B. (2010). Mammary odor cues and pheromones: Mammalian infant-directed communication about Maternal State, Mammae and Milk. Vitamins & Hormones, 83, 83-136.
63. Schaal, B., & Orgeur, P. (1992). Olfaction in utero: Can the rodent model be generalized? Quarterly Journal of Experimental Psychology, 44B, 245-278.
64. Schaal, B., Coureaud, G., Langlois, D., Ginies, C., Sémon, E., & Perrier, G. (2003). The mammary pheromone of the rabbit: Chemical and behavioural characterisation. Nature, 424, 68-72.
65. Schaal, B., Doucet, S., Sagot, P., Hertling, E., & Soussignan, R. (2006). Human breast areolae as scent organs: Morphological data and possible involvement in maternalneonatal coadaptation. Developmental Psychobiology, 48, 100-110.
66. Schaal, B., Doucet, S., Soussignan, R., Rietdorf, M., Weibchen, G., & Francke, W. (2008). The human breast as a scent organ: Exocrine structures, secretions, volatile components, and possible functions in breastfeeding interactions. In J. L. Hurst, R. J. Beynon, S. C. Roberts, & T. D. Wyatt (Eds.), Chemical signals in vertebrates, Vol. 11. (pp. 325-335). Berlin: Springer Verlag.
67. Schaal, B., Coureaud, G., Moncomble, A. S., Langlois, D., & Perrier, G. (2008). Many common odour cues and (at least) one pheromone shaping the behaviour of young rabbits. In P. C. Alves, N. Ferr, & K. Hackländer (Eds.), Lagomorph biology: Evolution, ecology and conservation (pp. 189-209). Berlin: Springer Verlag.
68. Schaal, B., Coureaud, G., Doucet, S., Delaunay-El Allam, M., Moncomble, A. S., Montigny, D., ... Holley, A. (2009). Olfactory mammary signalisation in females and neonatal odour processing: Ways evolved in rabbit and human. Behavioural Brain Research, 200, 346-358.
69. Sellers, G., Lin, H. C., Riddell, M. G., Ravis, W. R., Lin, Y. J., Duran, S. H., & Givens, M. D. (2010). Pharmacokinetics of ketamine in plasma and milk of mature Holstein cows. Journal of Veterinary Pharmacology and Therapeutics, 33, 480-484.
70. Shahan, K., Denaro, M., Gilmartin, M., Shi, Y., & Derman, E. (1987). Expression of six mouse major urinary protein genes in the mammary, parotid, sublingual, submaxillary, and lachrymal glands and in the liver. Molecular and Cellular Biology, 7, 1947-1954.
71. Singh, P. J., & Hofer, M. A. (1978). Oxytocin reinstates maternal olfactory cues for nipple orientation and attachment in rat pups. Physiology & Behavior, 20, 385-389.
72. Small, W. S. (1899). Notes on the psychic development of the albino rat. American Journal of Psychology, 11, 80-100.
73. Smotherman, W. P., Richards, L. S., & Robinson, S. R. (1984). Techniques for observing fetal behavior in utero: A comparison of chemomyelotomy and spinal transection. Developmental Psychobiology, 17, 661-674.
74. Stevens, L. M., & Landis, S. C. (1987). Development and properties of the secretory response in rat sweat glands: Relationship to the induction of cholinergic function in sweat gland innervation. Developmental Biology, 123, I79-I90.
75. Sullivan, R. M., Hofer, M. A., & Brake, S. C. (1986). Olfactory-guided orientation in neonatal rats is enhanced by a conditioned change in behavioral state. Developmental Psychobiology, 19, 615-623.
76. Teicher, M. H., & Blass, E. M. (1976). Suckling in newborn rats: Eliminated by nipple lavage, reinstated by pup saliva. Science, 193, 422-425.
77. Teicher, M. H., & Blass, E. M. (1977). First suckling response of the newborn albino rat: The roles of olfaction and amniotic fluid. Science, 198, 635-636.
78. Todrank, J., Busquet, N., Baudoin, C., & Heth, G. (2005). Preferences of newborn mice for odours indicating closer genetic relatedness: Is experience necessary? Proceeding of the Royal Society B, 272, 2083-2088.
79. Todrank, J., Heth, G., & Restrepo, D. (2011). Effects of in utero odorant exposure on neuroanatomical development of the olfactory bulb and odor preferences. Proceeding of the Royal Society B, 278, 1949-1955.
80. Vilches, J. J., Ceballos, D., Verdu, E., & Navarro, X. (2002). Changes in mouse sudomotor function and sweat gland innervation with ageing. Autonomic Neuroscience: Basic and Clinical, 95, 80-87.
81. Weber, E. M., & Olsson, I. A. S. (2008). Maternal behaviour in Mus musculus sp.: An ethological review. Applied Animal Behaviour Science, 114, 1-22.
82. Youngentob, S. L., & Glendinning, J. I. (2009). Fetal ethanol exposure increases ethanol intake by making it smell and taste better. Proceedings of the National Academy of Science of the USA, 106, 5359-5364.