Abstract
Humans’ early olfactory perception has been studied mainly within the framework of mother–offspring interactions and only a few studies have focused on newborns’ abilities to discriminate body odors per se. The aim of this study was to develop a method to evaluate olfactory social preferences of infants at term-equivalent age. Twenty dyads of infants (10 born preterm and 10 born at term) at term-equivalent age and their mothers were included. We analyzed the behavioral reactions of infants to their mother's upper-chest odor (that bears social, non-food related information). The two impregnated gauzes and a control gauze were presented to the infants for 10 s each, in a random order. We compared two durations of gauze impregnation: 30 min and 12 h. This study reveals that mothers’ upper chest emits sufficient olfactory information to induce reactions in infants born full-term or born preterm and that a short impregnation is preferable to evaluate their perception of body odors, notably for those born preterm.
Similar content being viewed by others
References
Ackerl K, Atzmueller M, Grammer K (2002) The scent of fear. Neuroendocrinol Lett 23:79–84
André V, Durier V, Beuchée A, Roué J-M, Lemasson A, Hausberger M, Sizun J, Henry S (2020) Higher tactile sensitivity in preterm infants at term-equivalent age: a pilot study. PLoS One 15:e0229270
Andrews K, Fitzgerald M (1994) The cutaneous withdrawal reflex in human neonates: sensitization, receptive fields, and the effects of contralateral stimulation. Pain 56:95–101
Balogh RenéD, Porter RH (1986) Olfactory preferences resulting from mere exposure in human neonates. Infant Behav Dev 9:395–401
Barbu-Roth M, Anderson DI, Desprès A, Provasi J, Cabrol D, Campos JJ (2009) Neonatal stepping in relation to terrestrial optic flow. Child Dev 80:8–14
Bartocci M, Winberg J, Papendieck G, Mustica T, Serra G, Lagercrantz H (2001) Cerebral hemodynamic response to unpleasant odors in the preterm newborn measured by near-infrared spectroscopy. Pediatr Res 50:324–330
Cernoch JM, Porter RH (1985) Recognition of maternal axillary odors by infants. Child Dev 56:1593–1598
Chen D, Haviland-Jones J (2000) Human olfactory communication of emotion. Percept Mot Skills 91:771–781
Chen E-M, Gau M-L, Liu C-Y, Lee T-Y (2017) Effects of father-neonate skin-to-skin contact on attachment: a randomized controlled trial. Nurs Res Pract 2017:8612024
DeCasper AJ, Fifer WP (1980) Of human bonding: newborns prefer their mothers’ voices. Science 208:1174–1176
Delaunay-El Allam M, Marlier L, Schaal B (2006) Learning at the breast: preference formation for an artificial scent and its attraction against the odor of maternal milk. Infant Behav Dev 29:308–321
Dormont L, Bessière J-M, Cohuet A (2013) Human skin volatiles: a review. J Chem Ecol 39:569–578
Doty RL (1981) Olfactory communication in humans. Chem Senses 6:351–376
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
Erlandsson K, Dsilna A, Fagerberg I, Christensson K (2007) Skin-to-skin care with the father after cesarean birth and its effect on newborn crying and prefeeding behavior. Birth 34:105–114
Faas AE, Spontón ED, Moya PR, Molina JC (2000) Differential responsiveness to alcohol odor in human neonates: effects of maternal consumption during gestation. Alcohol 22:7–17
Frie J, Bartocci M, Lagercrantz H, Kuhn P (2018) Cortical responses to alien odors in newborns: an fNIRS study. Cereb Cortex 28:3229–3240
Ganchrow JR, Steiner JE, Daher M (1983) Neonatal facial expressions in response to different qualities and intensities of gustatory stimuli. Infant Behav Dev 6:189–200
Gauthaman G, Jayachandran L, Prabhakar K (1984) Olfactory reflexes in newborn infants. Indian J Pediatr 51:397–399
Goubet N, Rattaz C, Pierrat V, Allémann E, Bullinger A, Lequien P (2002) Olfactory familiarization and discrimination in preterm and full-term newborns. Infancy 3:53–75
Goubet N, Rattaz C, Pierrat V, Bullinger A, Lequien P (2003) Olfactory experience mediates response to pain in preterm newborns. Dev Psychobiol 42:171–180
Goubet N, Strasbaugh K, Chesney J (2007) Familiarity breeds content? Soothing effect of a familiar odor on full-term newborns. J Dev Behav Pediatr 28:189–194
Grunau RE, Holsti L, Haley DW, Oberlander T, Weinberg J, Solimano A, Whitfield MF, Fitzgerald C, Yu W (2005) Neonatal procedural pain exposure predicts lower cortisol and behavioral reactivity in preterm infants in the NICU. Pain 113:293–300
Havlicek J, Lenochova P (2008) Environmental effects on human body odour. In: Hurst JL, Beynon RJ, Roberts SC, Wyatt TD (eds) Chemical signals in vertebrates 11. Springer, New York, pp 199–210
Keller WD, Hildebrandt KA, Richards ME (1985) Effects of extended father-infant contact during the newborn period. Infant Behav Dev 8:337–350
Kippenberger S, Havlíček J, Bernd A, Thaçi D, Kaufmann R, Meissner M (2012) ’Nosing around’the human skin: What information is concealed in skin odour? Exp Dermatol 21:655–659
Macfarlane A (1975) Olfaction in the development of social preferences in the human neonate. Parent Infant Interact 33:103–113
Makin JW, Porter RH (1989) Attractiveness of lactating females’ breast odors to neonates. Child Dev 60:803–810
Marlier L, Schaal B, Soussignan R (1998a) Bottle-fed neonates prefer an odor experienced in utero to an odor experienced postnatally in the feeding context. Dev Psychobiol 33:133–145
Marlier L, Schaal B, Soussignan R (1998b) Neonatal responsiveness to the odor of amniotic and lacteal fluids: a test of perinatal chemosensory continuity. Child Dev 69:611–623
Marlier L, Schaal B, Gaugler C, Messer J (2001) Olfaction in premature human newborns: detection and discrimination abilities two months before gestational term. Chemical signals in vertebrates 9. Springer, Berlin, pp 205–209
Mitchell A, Boss BJ (2002) Adverse effects of pain on the nervous systems of newborns and young children: a review of the literature. J Neurosci Nurs 34:228–236
Pascalis O, de Schonen S, Morton J, Deruelle C, Fabre-Grenet M (1995) Mother’s face recognition by neonates: a replication and an extension. Infant Behav Dev 18:79–85
Penn DJ, Oberzaucher E, Grammer K, Fischer G, Soini HA, Wiesler D, Novotny MV, Dixon SJ, Xu Y, Brereton RG (2007) Individual and gender fingerprints in human body odour. J R Soc Interface 4:331–340
Pihet S, Mellier D, Bullinger A, Schaal B (1997) Réponses comportementales aux odeurs chez le nouveau-né prématuré: étude préliminaire. Enfance 50:33–46
Prechtl HFR (1974) The behavioural states of the newborn infant (a review). Brain Res 76:185–212
Prehn A, Ohrt A, Sojka B, Ferstl R, Pause BM (2006) Chemosensory anxiety signals augment the startle reflex in humans. Neurosci Lett 394:127–130
Quinn PC, Yahr J, Kuhn A, Slater AM, Pascalils O (2002) Representation of the gender of human faces by infants: a preference for female. Perception 31:1109–1121
Rattaz C, Goubet N, Bullinger A (2005) The calming effect of a familiar odor on full-term newborns. J Dev Behav Pediatr 26:86–92
Sarnat HB (1978) Olfactory reflexes in the newborn infant. J Pediatr 92:624–626
Schaal B (1986) Presumed olfactory exchanges between mother and neonate in humans. In: Le Camus J, Cosnier J (eds) Ethology and Psychology. Privat, Toulouse, pp 101–110
Schaal B, Marlier L, Soussignan R (1995) Responsiveness to the odour of amniotic fluid in the human neonate. Neonatology 67:397–406
Schaal B, Marlier L, Soussignan R (1998) Olfactory function in the human fetus: evidence from selective neonatal responsiveness to the odor of amniotic fluid. Behav Neurosci 112:1438–1449
Schaal B, Marlier L, Soussignan R (2000) Human foetuses learn odours from their pregnant mother’s diet. Chem Senses 25:729–737
Schaal B, Hummel T, Soussignan R (2004) Olfaction in the fetal and premature infant: functional status and clinical implications. Clin Perinatol 31:261–285
Schleidt M, Hold B, Attili G (1981) A cross-cultural study on the attitude towards personal odors. J Chem Ecol 7:19–31
Soussignan R, Schaal B, Marlier L, Jiang T (1997) Facial and autonomic responses to biological and artificial olfactory stimuli in human neonates: re-examining early hedonic discrimination of odors. Physiol Behav 62:745–758
Steiner JE (1979) Human facial expressions in response to taste and smell stimulation. Adv Child Dev Behav 13:257–295
Sullivan RM, Toubas P (1998) Clinical usefulness of maternal odor in newborns: soothing and feeding preparatory responses. Neonatology 74:402–408
Troccaz M, Borchard G, Vuilleumier C, Raviot-Derrien S, Niclass Y, Beccucci S, Starkenmann C (2009) Gender-specific differences between the concentrations of nonvolatile (R)/(S)-3-methyl-3-sulfanylhexan-1-Ol and (R)/(S)-3-hydroxy-3-methyl-hexanoic acid odor precursors in axillary secretions. Chem Sens 34:203–210
Wallace P (1977) Individual discrimination of humans by odor. Physiol Behav 19:577–579
Young G, Décarie TG (1977) An ethology-based catalogue of facial/vocal behaviour in infancy. Anim Behav 25(Part 1):95–107
Acknowledgements
We are grateful to the hospital staff and especially Dr A. de La Pintière, the nursing staff S. le Gall and I. Paire, the team members of the NIDCAP program S. Bleunven, I. Olivard, B. Kerleroux, N. Ratynski and the research nurse S. Roudaut, for their help during this research. We are also very grateful to all the participants, and their parents, for volunteering to be part of this study. We thank also Ann Cloarec for correcting the English. The study resulted from collaborations within the interdisciplinary Group of Scientific Interest GIS “Cerveau-Comportement-Société”.
Funding
This work was supported by the University of Rennes 1 and the CNRS and a doctoral fellowship from the French research ministry to V. André.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflicts of interest.
Ethical approval
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.
Informed consent
Informed consent was obtained from the parents of all individual participants included in the study.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
André, V., Henry, S., Vuillemin, A. et al. A novel, short and easy-to-perform method to evaluate newborns’ social olfactory preferences. Anim Cogn 23, 843–850 (2020). https://doi.org/10.1007/s10071-020-01397-w
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10071-020-01397-w