Unique salience of maternal breast odors for newborn infants

Human infants are particularly responsive to olfactory cues emanating from their mother's nipple/areola region. Beginning within minutes after birth, maternal breast odors elicit preferential head orientation by neonates and help guide them to the nipple. Such odors also influence babies' general motor activity and arousal, which may contribute further to successful nipple localization and sucking. The role of maternal olfactory signals in the mediation of early breast-feeding is functionally analogous to that of nipple-search pheromone as described in nonhuman mammals. To some extent, the chemical profile of breast secretions overlaps with that of amniotic fluid. Therefore, early postnatal attraction to odors associated with the nipple/areola may reflect prenatal exposure and familiarization. Although newborns are generally attracted to breast odors produced by lactating women, breast-fed infants rapidly learn their mother's characteristic olfactory signature while sucking at her breasts and can subsequently recognize her by that unique scent alone. Early odor-based recognition may be an important factor in the development of the infant-mother bond.

[1]  P. Poindron,et al.  Endocrine and Sensory Regulation of Maternal Behavior in the Ewe , 1980 .

[2]  I. W. R. Bushneil,et al.  Neonatal recognition of the mother's face , 1989 .

[3]  D. Stoddart.  The scented ape , 1990 .

[4]  B. A. Baldwin,et al.  The effects of ablation of the olfactory bulbs on parturition and maternal behaviour in Soay sheep. , 1974, Animal behaviour.

[5]  R. Sullivan,et al.  Olfactory classical conditioning in neonates. , 1991, Pediatrics.

[6]  P. Orgeur,et al.  Recognition of Dizygotic and Monozygotic Twin Lambs By Ewes , 1993 .

[7]  M. Meredith.  8 – Sensory Physiology of Pheromone Communication , 1983 .

[8]  E. Keverne,et al.  Changes in the sensory processing of olfactory signals induced by birth in sheep. , 1992, Science.

[9]  H. Lagercrantz.  Stress, Arousal, and Gene Activation at Birth , 1996 .

[10]  K. Christensson,et al.  Gastric Suction in Healthy Newborn Infants Effects on Circulation and Developing Feeding Behaviour , 1987, Acta paediatrica Scandinavica.

[11]  K. Christensson,et al.  Soothing effect of amniotic fluid smell in newborn infants. , 1998, Early human development.

[12]  R. Porter,et al.  Odor signatures and kin recognition , 1985, Physiology & Behavior.

[13]  M. Hofer,et al.  Effects of nasal ZnSO4 irrigation and olfactory bulbectomy on rat pups , 1976, Physiology & Behavior.

[14]  N. Krasnegor,et al.  Mammalian parenting : biochemical, neurobiological, and behavioral determinants , 1990 .

[15]  B. Schaal,et al.  “Microsmatic Humans” Revisited: The Generation and Perception of Chemical Signals , 1991 .

[16]  R. Porter,et al.  Olfactory preferences resulting from mere exposure in human neonates , 1986 .

[17]  R. Hudson,et al.  Do newborn rabbits learn the odor stimuli releasing nipple-search behavior? , 1985, Developmental psychobiology.

[18]  K. Christensson,et al.  Separation distress call in the human neonate in the absence of maternal body contact , 1995, Acta paediatrica.

[19]  A. M. Miller,et al.  Sebaceous glands in the human nipple , 1926 .

[20]  R. Soussignan,et al.  Responsiveness to the odour of amniotic fluid in the human neonate. , 1995, Biology of the neonate.

[21]  B. Slotnick,et al.  Nipple attachment and survival in neonatal olfactory bulbectomized rats , 1987, Physiology & Behavior.

[22]  G. Beauchamp,et al.  Maternal diet alters the sensory qualities of human milk and the nursling's behavior. , 1991, Pediatrics.

[23]  I. Rogers,et al.  Association between breast feeding, child development and behaviour. , 1997, Early human development.

[24]  R. Soussignan,et al.  Neonatal responsiveness to the odor of amniotic and lacteal fluids: a test of perinatal chemosensory continuity. , 1998, Child development.

[25]  A. Decasper,et al.  Of Human Bonding: Newborns Prefer Their Mothers' Voices , 1980 .

[26]  M. Schleidt,et al.  The significance of mother's perfume for infants in the first weeks of their life , 1990 .

[27]  P. Poindron.  Mother-young relationships in intact or anosmic ewes at the time of sucking. , 1976 .

[28]  PG Hepper,et al.  Fetal memory: Does it exist? What does it do? , 1996, Acta paediatrica (Oslo, Norway : 1992). Supplement.

[29]  P. Eneroth,et al.  Short-term effects of early suckling and touch of the nipple on maternal behaviour. , 1990, Early human development.

[30]  D. Lehrman.  Ethology and psychology. , 1961, Recent advances in biological psychiatry.

[31]  R. Nowak,et al.  Development of exclusive mother-young bonding in sheep and goats. , 1993, Oxford reviews of reproductive biology.

[32]  H. Montagner,et al.  Les stimulations olfactives dans les relations entre l'enfant et la mère , 1980 .

[33]  G. Beauchamp,et al.  Garlic ingestion by pregnant women alters the odor of amniotic fluid. , 1995, Chemical senses.

[34]  Barbara A. Smith,et al.  Preference of Mongolian gerbils for salivary cues: a developmental analysis , 1990, Animal Behaviour.

[35]  G. Alexander,et al.  Odour cues to maternal recognition of lambs: an investigation of some possible sources. , 1982 .

[36]  M. Russell,et al.  Human olfactory communication , 1976, Nature.

[37]  A. Fleming,et al.  Postpartum factors related to mother's attraction to newborn infant odors. , 1993, Developmental psychobiology.

[38]  R. Porter,et al.  Attractiveness of lactating females' breast odors to neonates. , 1989, Child development.

[39]  J. McGlone,et al.  Sensory systems and nipple attachment behavior in neonatal pigs , 1990, Physiology & Behavior.

[40]  H. Moss,et al.  Patterns and determinants of maternal attachment. , 1970, The Journal of pediatrics.

[41]  H. Kalmus,et al.  The discrimination by the nose of the dog of individual human odours and in particular of the odours of twins , 1955 .

[42]  Leonard A. Rosenblum,et al.  The Effect of the Infant on Its Caregiver. Volume 1 in the Origins of Behavior Series. , 1974 .

[43]  B. Campbell,et al.  Ontogeny of behavioral arousal in rats: effect of maternal and sibling presence. , 1976, Journal of comparative and physiological psychology.

[44]  Martin H. Teicher,et al.  Suckling in newborn rats: eliminated by nipple lavage, reinstated by pup saliva. , 1976, Science.

[45]  R. Doty.  Mammalian olfaction, reproductive processes, and behavior. , 1977 .

[46]  P. Hepper,et al.  Newborn and fetal response to maternal voice , 1993 .

[47]  P. Hepper.  The Discrimination of Human Odour by the Dog , 1988, Perception.

[48]  E. Wilson,et al.  Sociobiology: The New Synthesis , 1975 .

[49]  Thomas V. Getchell,et al.  Smell and Taste in Health and Disease , 1992, Annals of Internal Medicine.

[50]  D. Krehbiel,et al.  Investigations of the nature of lambs' individual odour signatures , 1994, Behavioural Processes.

[51]  P. Hepper.  Human fetal "olfactory" learning , 1995 .

[52]  R. Porter,et al.  Temporal parameters of responsiveness to maternal pheromone in Acomys cahirinus , 1978, Physiology & Behavior.

[53]  J. Winberg,et al.  Does the newborn baby find the nipple by smell? , 1994, The Lancet.

[54]  A Macfarlane,et al.  Olfaction in the development of social preferences in the human neonate. , 2008, Ciba Foundation symposium.

[55]  B. Schaal,et al.  Familiarité et discrimination olfactive chez le nouveau-né : influence différentielle du mode d'alimentation ? , 1997 .

[56]  F. Lévy,et al.  Influence du liquide amniotique sur la manifestation du comportement maternel chez la brebis parturiente , 1984 .

[57]  M. Hofer.  Olfactory denervation: its biological and behavioral effects in infant rats. , 1976, Journal of Comparative and Physiological Psychology.

[58]  E. Keverne,et al.  Physiological, Sensory, and Experiential Factors of Parental Care in Sheep , 1996 .

[59]  Martin H. Teicher,et al.  Survival, growth and suckling behavior of neonatally bulbectomized rats , 1978, Physiology & Behavior.

[60]  G. Dryden,et al.  Lip-Licking Behavior in Captive Musk Shrews, Suncus Murinus , 1977 .

[61]  P. Poindron,et al.  Individual olfactory signatures as major determinants of early maternal discrimination in sheep. , 1991, Developmental psychobiology.

[62]  B. Nicholson.  DOES KISSING AID HUMAN BONDING BY SEMIOCHEMICAL ADDICTION? , 1984, The British journal of dermatology.

[63]  M. Hofer.  Hidden Regulatory Processes in Early Social Relationships , 1978 .

[64]  A. Fleming,et al.  Cortisol, Hedonics, and Maternal Responsiveness in Human Mothers , 1997, Hormones and Behavior.

[65]  S. Shuster,et al.  Lactation, Sebum Excretion and Melanocyte-stimulating Hormone , 1973, Nature.

[66]  C. Almli,et al.  Olfactory bulbectomy in infant rats: Survival, growth and ingestive behaviors , 1981, Physiology & Behavior.

[67]  M. Hofer,et al.  Evidence that maternal ventral skin substances promote suckling in infant rats , 1976, Physiology & Behavior.

[68]  D. Maurer,et al.  Developmental changes in the scanning of faces by young infants. , 1976, Child development.

[69]  G. Sharman,et al.  Reproductive behaviour in the Red Kangaroo, Megaleia rufa, in captivity , 1964 .

[70]  A. Eidelman,et al.  Mothers' recognition of their newborns by olfactory cues , 1987 .

[71]  M. Horning,et al.  Profiles of volatile metabolites in body fluids , 1976 .

[72]  R. Porter,et al.  Attractiveness of amniotic fluid odor: evidence of prenatal olfactory learning? , 1996, Acta paediatrica.

[73]  M. Salas,et al.  Behavioral response of infant rats to maternal odor. , 1970, Physiology & behavior.

[74]  J. Vandenbergh.  Pheromones and reproduction in mammals , 1983 .

[75]  R. Porter,et al.  Recognition of maternal axillary odors by infants. , 1985, Child development.

[76]  S. Sjölin,et al.  Studies on Perceived Breast Milk Insufficiency: III. Consequences for Breast Milk Consumption and Growth , 1991, Acta paediatrica Scandinavica.

[77]  T. Yanaihara,et al.  The effect of odors on human newborn infants under stress , 1997 .

[78]  A. Leshner,et al.  Maternal pheromone: A demonstration of its existence in the mouse (Mus musculus) , 1977, Physiology & Behavior.

[79]  H. Varendi,et al.  Natural odour preferences of newborn infants change over time , 1997, Acta paediatrica.

[80]  W. P. Smotherman.  Odor aversion learning by the rat fetus , 1982, Physiology & Behavior.

[81]  G. W. Arnold,et al.  THE ROLES PLAYED BY THE SENSES OF THE EWE IN THE LOCATION AND RECOGNITION OF LAMBS , 1975 .

[82]  R. Porter,et al.  The influence of maternal labels on dietary preferences of spiny mouse weanlings , 1990, Physiology & Behavior.

[83]  R. Porter,et al.  Maternal recognition of neonates through olfactory cues , 1983, Physiology & Behavior.

[84]  E. Tobach,et al.  Olfactory bulbectomy and nursing behavior in rat pups (Wistar DAB). , 1975, Developmental psychobiology.

[85]  W. Fifer,et al.  Psychobiology of newborn auditory preferences. , 1989, Seminars in perinatology.

[86]  R Gervais,et al.  Importance of beta-noradrenergic receptors in the olfactory bulb of sheep for recognition of lambs. , 1990, Behavioral neuroscience.

[87]  P. Poindron,et al.  Attraction and repulsion by amniotic fluids and their olfactory control in the ewe around parturition , 1983, Physiology & Behavior.

[88]  R. Sullivan,et al.  Norepinephrine and learning-induced plasticity in infant rat olfactory system , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[89]  R. Hudson,et al.  Nipple Location By Newborn Rabbits: Behavioural Evidence for Pheromonal Guidance , 1983 .

[90]  I. F. Roberts.  Human Lactation 4. Breastfeeding, Nutrition, Infection and Infant Growth in Developed and Emerging Countries , 1991 .

[91]  R. Porter,et al.  Breast-fed infants respond to olfactory cues from their own mother and unfamiliar lactating females☆ , 1992 .

[92]  P. Wallace.  Individual discrimination of humans by odor , 1977, Physiology & Behavior.

[93]  M. Leon,et al.  Neuroethology of olfactory preference development. , 1992, Journal of neurobiology.

[94]  P. Brennan,et al.  Olfactory recognition: a simple memory system. , 1990, Science.

[95]  M. Leon,et al.  Maternal pheromone: discrimination by pre-weanling albino rats. , 1971, Physiology & behavior.

[96]  H. Lagercrantz,et al.  The "stress" of being born. , 1986, Scientific American.

[97]  Persistent effects of early odor exposure on human neonates , 1991 .

[98]  R. Porter,et al.  The responses of one-day old Acomys cabirinus pups to naturally occurring chemical stimuli. , 2010, Zeitschrift fur Tierpsychologie.

[99]  D. Wilson,et al.  The role of olfactory bulb norepinephrine in early olfactory learning. , 1992, Brain research. Developmental brain research.

[100]  M. Russell,et al.  Mother's identification of their infant's odors , 1983 .

[101]  A. Decasper,et al.  Human newborns' perception of male voices: preference, discrimination, and reinforcing value. , 1984, Developmental psychobiology.

[102]  P. Poindron,et al.  The importance of amniotic fluids for the establishment of maternal behaviour in experienced and inexperienced ewes , 1987, Animal Behaviour.

[103]  Richard L. Doty,et al.  7 – The Pheromone Concept in Mammalian Chemical Communication: A Critique , 1976 .