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Home / Equine Research Bank / PLoS One / Neonatal handling affects durably bonding and social develop...
PloS one2009; 4(4); e5216; doi: 10.1371/journal.pone.0005216

Neonatal handling affects durably bonding and social development.

Abstract: The neonatal period in humans and in most mammals is characterized by intense mother-young interactions favoring pair bonding and the adaptation of neonates to their new environment. However, in many post-delivery procedures, human babies commonly experience combined maternal separation and intense handling for about one hour post-birth. Currently, the effects of such disturbances on later attachment and on the development of newborns are still debated: clearly, further investigations are required. As animals present good models for controlled experimentation, we chose domestic horses to investigate this issue. Horses, like humans, are characterized by single births, long lactating periods and selective mother-infant bonds. Routine postnatal procedures for foals, as for human babies, also involve intense handling and maternal separation. In the present study, we monitored the behavior of foals from early stages of development to "adolescence", in a normal ecological context (social groups with adults and peers). Experimental foals, separated from their mothers and handled for only 1 hour post-birth, were compared to control foals, left undisturbed after birth. Our results revealed short- and long-term effects of this unique neonatal experience on attachment and subsequent social competences. Thus, experimental foals presented patterns of insecure attachment to their mothers (strong dependence on their mothers, little play) and impaired social competences (social withdrawal, aggressiveness) at all ages. We discuss these results in terms of mother-young interactions, timing of interactions and relationships between bonding and subsequent social competences. Our results indicate that this ungulate species could become an interesting animal model. To our knowledge, this is the first clear demonstration that intervention just after birth affects bonding and subsequent social competences (at least until "adolescence"). It opens new research directions for studies on both humans and other animals.
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Publication Date: 2009-04-08 PubMed ID: 19352503PubMed Central: PMC2662428DOI: 10.1371/journal.pone.0005216Google Scholar: Lookup
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Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research paper explores how handling newborns immediately after birth and separating them from their mothers can have lasting effects on their bonding and social development, using foals as a model. The study found that foals that were separated and handled for an hour after birth showed insecure attachment to their mothers and poorer social competences.

Objective and Methodology

  • The research aimed to investigate the effects of immediate post-birth handling of newborns and their separation from mothers, on their bonding and social behavior in future. The focus was on whether such an experience could affect the newborn’s attachment to the mother and social abilities.
  • Domestic horses were chosen as models for this study due to their similarities with humans such as single births, lengthy lactation periods, and selective mother-infant bonds.
  • The researchers compared the behavior of two groups – one where foals were separated from their mothers and handled for an hour immediately after birth (experimental foals) and the other where foals were left undisturbed (control group).

Results

  • Both short-term and long-term effects of neonatal handling and separation were observed on the foals’ attachment to their mothers and their future social abilities.
  • The handled and separated foals displayed signs of insecure attachment to their mothers e.g., they were overly dependent on their mothers and played less.
  • These foals also showed reduced social abilities – they were less social and more aggressive, regardless of their age.

Discussion and Conclusion

  • The findings were discussed in terms of mother-offspring interaction, appropriate timing for interaction, and how bonding is related to subsequent social competences.
  • The researchers suggested that the domestic horse could serve as an interesting animal model to further investigate these effects.
  • This research is the first to definitively show that intervention just after birth can affect bonding and future social competence, at least until adolescence, thus opening new avenues for research in human and animal studies.

Cite This Article

APA
Henry S, Richard-Yris MA, Tordjman S, Hausberger M. (2009). Neonatal handling affects durably bonding and social development. PLoS One, 4(4), e5216. https://doi.org/10.1371/journal.pone.0005216

Publication

PloS one
ISSN: 1932-6203
NlmUniqueID: 101285081
Country: United States
Language: English
Volume: 4
Issue: 4
Pages: e5216
PII: e5216

Researcher Affiliations

Henry, Séverine
  • UMR CNRS 6552 Ethos, Ethologie animale et humaine, Université de Rennes 1, Rennes, France. severine.henry@univ-rennes1.fr
Richard-Yris, Marie-Annick
    Tordjman, Sylvie
      Hausberger, Martine

        MeSH Terms

        • Animals
        • Animals, Newborn
        • Horses / physiology

        Conflict of Interest Statement

        The authors have declared that no competing interests exist.

        References

        This article includes 110 references
        1. Hofer MA. Early social relationships: a psychobiologist's view.. Child Dev 1987 Jun;58(3):633-47.
          pubmed: 3608643
        2. Poindron P, Schaal PB. Parent-infant relationships in Mammals: factors of control and psychobiological implications. .
        3. Acolet D, Sleath K, Whitelaw A. Oxygenation, heart rate and temperature in very low birthweight infants during skin-to-skin contact with their mothers.. Acta Paediatr Scand 1989 Mar;78(2):189-93.
          pubmed: 2929342doi: 10.1111/j.1651-2227.1989.tb11055.xgoogle scholar: lookup
        4. Christensson K, Cabrera T, Christensson E, Uvnäs-Moberg K, Winberg J. Separation distress call in the human neonate in the absence of maternal body contact.. Acta Paediatr 1995 May;84(5):468-73.
          pubmed: 7633137doi: 10.1111/j.1651-2227.1995.tb13676.xgoogle scholar: lookup
        5. Christensson K, Siles C, Moreno L, Belaustequi A, De La Fuente P, Lagercrantz H, Puyol P, Winberg J. Temperature, metabolic adaptation and crying in healthy full-term newborns cared for skin-to-skin or in a cot.. Acta Paediatr 1992 Jun-Jul;81(6-7):488-93.
          pubmed: 1392359doi: 10.1111/j.1651-2227.1992.tb12280.xgoogle scholar: lookup
        6. Ferber SG, Makhoul IR. The effect of skin-to-skin contact (kangaroo care) shortly after birth on the neurobehavioral responses of the term newborn: a randomized, controlled trial.. Pediatrics 2004 Apr;113(4):858-65.
          pubmed: 15060238doi: 10.1542/peds.113.4.858google scholar: lookup
        7. Mooncey S, Giannakoulopoulos X, Glover V, Acolet D, Modi N. The effect of mother-infant skin-to-skin contact on plasma cortisol and β-endorphin concentrations in preterm newborns. Infant Behav Dev 1997;20:553–557.
        8. Klaus MH, Jerauld R, Kreger NC, McAlpine W, Steffa M, Kennel JH. Maternal attachment. Importance of the first post-partum days.. N Engl J Med 1972 Mar 2;286(9):460-3.
          pubmed: 5009748doi: 10.1056/nejm197203022860904google scholar: lookup
        9. Matthiesen AS, Ransjö-Arvidson AB, Nissen E, Uvnäs-Moberg K. Postpartum maternal oxytocin release by newborns: effects of infant hand massage and sucking.. Birth 2001 Mar;28(1):13-9.
          pubmed: 11264623doi: 10.1046/j.1523-536x.2001.00013.xgoogle scholar: lookup
        10. Winberg J. Mother and newborn baby: mutual regulation of physiology and behavior--a selective review.. Dev Psychobiol 2005 Nov;47(3):217-29.
          pubmed: 16252290doi: 10.1002/dev.20094google scholar: lookup
        11. Klaus MH, Kennell JH, Plumb N, Zuehlke S. Human maternal behavior at the first contact with her young.. Pediatrics 1970 Aug;46(2):187-92.
          pubmed: 5432150
        12. Als H. The newborn communicates.. J Commun 1977 Spring;27(2):66-73.
          pubmed: 853137doi: 10.1111/j.1460-2466.1977.tb01828.xgoogle scholar: lookup
        13. Varendi H, Porter RH, Winberg J. Does the newborn baby find the nipple by smell?. Lancet 1994 Oct 8;344(8928):989-90.
          pubmed: 7934434doi: 10.1016/s0140-6736(94)91645-4google scholar: lookup
        14. Blass EM, Teicher MH. Suckling.. Science 1980 Oct 3;210(4465):15-22.
          pubmed: 6997992doi: 10.1126/science.6997992google scholar: lookup
        15. Koepke JE, Bigelow AE. Observations of Newborn Suckling Behavior. Infant Behav Dev 1997;20:93–98.
        16. Klaus M. Mother and infant: early emotional ties.. Pediatrics 1998 Nov;102(5 Suppl E):1244-6.
          pubmed: 9794962
        17. Bystrova K, Widström AM, Matthiesen AS, Ransjö-Arvidson AB, Welles-Nyström B, Wassberg C, Vorontsov I, Uvnäs-Moberg K. Skin-to-skin contact may reduce negative consequences of "the stress of being born": a study on temperature in newborn infants, subjected to different ward routines in St. Petersburg.. Acta Paediatr 2003;92(3):320-6.
          pubmed: 12725547doi: 10.1080/08035250310009248google scholar: lookup
        18. Klaus M, Kennell J. Commentary: routines in maternity units: are they still appropriate for 2002?. Birth 2001 Dec;28(4):274-5.
          pubmed: 11903217doi: 10.1046/j.1523-536x.2001.00274.xgoogle scholar: lookup
        19. Klaus MH, Jerauld R, Kreger NC, McAlpine W, Steffa M, Kennel JH. Maternal attachment. Importance of the first post-partum days.. N Engl J Med 1972 Mar 2;286(9):460-3.
          pubmed: 5009748doi: 10.1056/nejm197203022860904google scholar: lookup
        20. Carlsson SG, Fagerberg H, Horneman G, Hwang CP, Larsson K, Rödholm M, Schaller J, Danielsson B, Gundewall C. Effects of amount of contact between mother and child on the mother's nursing behavior.. Dev Psychobiol 1978 Mar;11(2):143-50.
          pubmed: 640231doi: 10.1002/dev.420110206google scholar: lookup
        21. De Chateau P, Wiberg B. Long-term effect on mother-infant behaviour of extra contact during the first hour post partum. II. A follow-up at three months.. Acta Paediatr Scand 1977 Mar;66(2):145-51.
          pubmed: 842336doi: 10.1111/j.1651-2227.1977.tb07826.xgoogle scholar: lookup
        22. Righard L, Alade MO. Effect of delivery room routines on success of first breast-feed.. Lancet 1990 Nov 3;336(8723):1105-7.
          pubmed: 1977988doi: 10.1016/0140-6736(90)92579-7google scholar: lookup
        23. Svejda M, Carlsson SG, Larsson K. Effects of extended post-partum mother-child contact on the mother's behavior during nursing. Infant behav for dev 1979;2:319–324.
        24. Nyqvist KH, Ewald U. Successful breast feeding in spite of early mother-baby separation for neonatal care.. Midwifery 1997 Mar;13(1):24-31.
          pubmed: 9171586doi: 10.1016/s0266-6138(97)90029-2google scholar: lookup
        25. Renfrew MJ, Lang S, Woolridge MW. Early versus delayed initiation of breastfeeding.. Cochrane Database Syst Rev 2000;(2):CD000043.
          pubmed: 10796101doi: 10.1002/14651858.cd000043google scholar: lookup
        26. Hwang CP. Aspects of the mother-infant relationship during nursing, 1 and 6 weeks after early extended post-partum contact.. Early Hum Dev 1981 Jul;5(3):279-87.
          pubmed: 7261991doi: 10.1016/0378-3782(81)90035-9google scholar: lookup
        27. Hales DJ, Lozoff B, Sosa R, Kennell JH. Defining the limits of the maternal sensitive period.. Dev Med Child Neurol 1977 Aug;19(4):454-61.
          pubmed: 892242doi: 10.1111/j.1469-8749.1977.tb07938.xgoogle scholar: lookup
        28. Jansson UM, Mustafa T, Khan MA, Lindblad BS, Widström AM. The effects of medically-orientated labour ward routines on prefeeding behaviour and body temperature in newborn infants.. J Trop Pediatr 1995 Dec;41(6):360-3.
          pubmed: 8606445doi: 10.1093/tropej/41.6.360google scholar: lookup
        29. Long JG, Philip AG, Lucey JF. Excessive handling as a cause of hypoxemia.. Pediatrics 1980 Feb;65(2):203-7.
          pubmed: 7356847
        30. Ali Z, Lowry M. Early maternal-child contact: effects on later behaviour.. Dev Med Child Neurol 1981 Jun;23(3):337-45.
          pubmed: 7250542
        31. Buranasin B. The effects of rooming-in on the success of breastfeeding and the decline in abandonment of children.. Asia Pac J Public Health 1991;5(3):217-20.
          pubmed: 1823804doi: 10.1177/101053959100500305google scholar: lookup
        32. Lvoff NM, Lvoff V, Klaus MH. Effect of the baby-friendly initiative on infant abandonment in a Russian hospital.. Arch Pediatr Adolesc Med 2000 May;154(5):474-7.
          pubmed: 10807298doi: 10.1001/archpedi.154.5.474google scholar: lookup
        33. Widström AM, Thingström-Paulsson J. The position of the tongue during rooting reflexes elicited in newborn infants before the first suckle.. Acta Paediatr 1993 Mar;82(3):281-3.
          pubmed: 8495085doi: 10.1111/j.1651-2227.1993.tb12660.xgoogle scholar: lookup
        34. Sroufe LA, Fox NE, Pancake VR. Attachment and dependency in developmental perspective. Child development 1983;54:1615–1627.
        35. Sroufe LA. Attachment and development: a prospective, longitudinal study from birth to adulthood.. Attach Hum Dev 2005 Dec;7(4):349-67.
          pubmed: 16332580doi: 10.1080/14616730500365928google scholar: lookup
        36. Gottlieb G, Lickliter R. The various roles of animal models in understanding human development. Social development 2004;13:311–325.
        37. Harlow HF. The development of affectional patterns in infant monkeys. .
        38. Bowlby J. Attachment and Loss, volume 1, Attachment. .
        39. Denenberg VH. Effects of exposure to stressors in early life upon later behavioral and biological processes. .
        40. Plotsky PM, Meaney MJ. Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats.. Brain Res Mol Brain Res 1993 May;18(3):195-200.
          pubmed: 8497182doi: 10.1016/0169-328x(93)90189-vgoogle scholar: lookup
        41. Meaney MJ, Diorio J, Francis D, Widdowson J, LaPlante P, Caldji C, Sharma S, Seckl JR, Plotsky PM. Early environmental regulation of forebrain glucocorticoid receptor gene expression: implications for adrenocortical responses to stress.. Dev Neurosci 1996;18(1-2):49-72.
          pubmed: 8840086doi: 10.1159/000111395google scholar: lookup
        42. Liu D, Caldji C, Sharma S, Plotsky PM, Meaney MJ. Influence of neonatal rearing conditions on stress-induced adrenocorticotropin responses and norepinepherine release in the hypothalamic paraventricular nucleus.. J Neuroendocrinol 2000 Jan;12(1):5-12.
          pubmed: 10692138doi: 10.1046/j.1365-2826.2000.00422.xgoogle scholar: lookup
        43. Pryce CR, Bettschen D, Bahr NI, Feldon J. Comparison of the effects of infant handling, isolation, and nonhandling on acoustic startle, prepulse inhibition, locomotion, and HPA activity in the adult rat.. Behav Neurosci 2001 Feb;115(1):71-83.
          pubmed: 11256454doi: 10.1037/0735-7044.115.1.71google scholar: lookup
        44. Ladd CO, Huot RL, Thrivikraman KV, Nemeroff CB, Meaney MJ, Plotsky PM. Long-term behavioral and neuroendocrine adaptations to adverse early experience.. Prog Brain Res 2000;122:81-103.
          pubmed: 10737052doi: 10.1016/s0079-6123(08)62132-9google scholar: lookup
        45. Harlow HF, Dodsworth RO, Harlow MK. Total social isolation in monkeys.. Proc Natl Acad Sci U S A 1965 Jul;54(1):90-7.
          pmc: PMC285801pubmed: 4955132doi: 10.1073/pnas.54.1.90google scholar: lookup
        46. Champoux M, Coe CL, Schanberg S, Kuhn C, Suomi SJ. Hormonal effects of early rearing conditions in the infant rhesus monkey. Am J Primatol 1989;19:111–117.
        47. Kraemer GW. Psychobiology of early social attachment in rhesus monkeys. Clinical implications. Ann NY Acad Sci 2003;15:401–408.
        48. Hinde RA, Spencer-Booth Y, Bruce M. Effects of 6-day maternal deprivation on rhesus monkey infants.. Nature 1966 Jun 4;210(5040):1021-3.
          pubmed: 4958198doi: 10.1038/2101021a0google scholar: lookup
        49. Hinde RA, Spencer-Booth. Towards understanding individual differences in rhesus mother-infant interaction. Anim Behav 1971;19:165–173.
        50. Ainsworth MDS, Blehar MC, Waters E, Wall S. Patterns of attachment: a psychological study of the strange situation. .
        51. Stern JS. Somatosensation and maternal care in Norway rats. .
        52. Pryce CR. Socialization, hormones and the regulation of maternal behavior in nonhuman simian primates. .
        53. Crowell-Davis SL, Weeks J. Maternal behaviour and mare-foal interaction. .
        54. Moons CPH, Laughlin K, Zanella AJ. Effects of short-term maternal separations on weaning stress in foals. Appl Anim Behav Sci 2005;91:321–335.
        55. Sevi A, Caroprese M, Annicchiarico G, Albenzio M, Taibi L. The effect of a gradual separation from the mother on later behavioral, immune and endocrine alterations in artificially reared lambs. Appl Anim Behav Sci 2003;83:41–53.
        56. Goursaud AP, Nowak R. Colostrum mediates the development of mother preference by newborn lambs.. Physiol Behav 1999 Aug 1;67(1):49-56.
          pubmed: 10463628doi: 10.1016/s0031-9384(99)00037-2google scholar: lookup
        57. Nowak R, Murphy TM, Lindsay DR, Alster P, Andersson R, Uvnäs-Moberg K. Development of a preferential relationship with the mother by the newborn lamb: importance of the sucking activity.. Physiol Behav 1997 Oct;62(4):681-8.
          pubmed: 9284484doi: 10.1016/s0031-9384(97)00079-6google scholar: lookup
        58. Henry S, Richard-Yris MA, Hausberger M. Influence of various early human-foal interferences on subsequent human-foal relationship.. Dev Psychobiol 2006 Dec;48(8):712-8.
          pubmed: 17111402doi: 10.1002/dev.20189google scholar: lookup
        59. Hausberger M, Henry S, Larose C, Richard-Yris MA. First suckling: a crucial event for mother-young attachment? an experimental study in horses (Equus caballus).. J Comp Psychol 2007 Feb;121(1):109-12.
          pubmed: 17324081doi: 10.1037/0735-7036.121.1.109google scholar: lookup
        60. Carson K, Wood-Gush DGM. Equine behaviour: I. A review of the literature on social and dam foal behavior. Appl Anim Ethol 1983;10:165–178.
        61. Miller RM. Imprint training of the newborn foal. .
        62. Fairbanks LA. Individual differences in maternal style: cause and consequences for mothers and offspring. Advances in the study of behaviour 1996;25:579–611.
        63. Crowell-Davis SL. Spatial relations between mares and foals of the Welsh pony (Equus caballus). Anim Behav 1986;34:1007–1015.
        64. Wolff A, Hausberger M. Behaviour of foals before weaning may have some genetic basis. Ethology 1994;96:1–10.
        65. Waring GH. Horse behaviour. The behaviour traits and adaptations of domestic and wild horses, including ponies. .
        66. Seligman ME, Maier SF, Geer JH. Alleviation of learned helplessness in the dog.. J Abnorm Psychol 1968 Jun;73(3):256-62.
          pubmed: 5658526doi: 10.1037/h0025831google scholar: lookup
        67. Simpson BS. Neonatal foal handling. Appl Anim Behav Sci 2002;78:303–317.
        68. Lamb ME. Father-infant and mother-infant interaction in the first year of life. Child Dev 1977;48:167–181.
        69. Simons SH, van Dijk M, Anand KS, Roofthooft D, van Lingen RA, Tibboel D. Do we still hurt newborn babies? A prospective study of procedural pain and analgesia in neonates.. Arch Pediatr Adolesc Med 2003 Nov;157(11):1058-64.
          pubmed: 14609893doi: 10.1001/archpedi.157.11.1058google scholar: lookup
        70. Gray L, Watt L, Blass EM. Skin-to-skin contact is analgesic in healthy newborns.. Pediatrics 2000 Jan;105(1):e14.
          pubmed: 10617751doi: 10.1542/peds.105.1.e14google scholar: lookup
        71. Mörelius E, Hellström-Westas L, Carlén C, Norman E, Nelson N. Is a nappy change stressful to neonates?. Early Hum Dev 2006 Oct;82(10):669-76.
          pubmed: 16507341doi: 10.1016/j.earlhumdev.2005.12.013google scholar: lookup
        72. Anand KJ, Scalzo FM. Can adverse neonatal experiences alter brain development and subsequent behavior?. Biol Neonate 2000 Feb;77(2):69-82.
          pubmed: 10657682doi: 10.1159/000014197google scholar: lookup
        73. Caldji C, Francis D, Sharma S, Plotsky PM, Meaney MJ. The effects of early rearing environment on the development of GABAA and central benzodiazepine receptor levels and novelty-induced fearfulness in the rat.. Neuropsychopharmacology 2000 Mar;22(3):219-29.
          pubmed: 10693149doi: 10.1016/s0893-133x(99)00110-4google scholar: lookup
        74. Walker CD, Anand KJ, Plotsky PM. Development of the hypothalamic–pituitary–adrenal axis and the stress response. .
        75. Veissier I, Boissy A, Nowak R, Orgeur P, Poindron P. Ontogeny of social awareness in domestic herbivores. Appl Anim Behav Sci 1998;57:233–245.
        76. Blass EM, Shide DJ, Zaw-Mon C, Sorrentino J. Mother as shield: differential effects of contact and nursing on pain responsivity in infant rats--evidence for nonopioid mediation.. Behav Neurosci 1995 Apr;109(2):342-53.
          pubmed: 7619324doi: 10.1037//0735-7044.109.2.342google scholar: lookup
        77. Blass EM, Watt LB. Suckling- and sucrose-induced analgesia in human newborns.. Pain 1999 Dec;83(3):611-623.
          pubmed: 10568870doi: 10.1016/s0304-3959(99)00166-9google scholar: lookup
        78. Goldberg S, Grusec JE, Jenkins JM. Confidence in protection: Arguments for a narrow definition of attachment. J Family Psychol 1996;13:475–483.
        79. Nievar MA, Becker BJ. Sensitivity and attachment: A second perspective of De Wolff and van IJzendoorns meta-analysis. Social Development 2008;17:102–114.
        80. McElwain NL, Booth-Laforce C. Maternal sensitivity to infant distress and nondistress as predictors of infant-mother attachment security.. J Fam Psychol 2006 Jun;20(2):247-55.
          pubmed: 16756400doi: 10.1037/0893-3200.20.2.247google scholar: lookup
        81. Egeland B, Farber EA. Infant-mother attachment: factors related to its development and changes over time.. Child Dev 1984 Jun;55(3):753-71.
          pubmed: 6734316
        82. Goldberg S, Perrotta M, Minde K, Corter C. Maternal behavior and attachment in low-birth-weight twins and singletons.. Child Dev 1986 Feb;57(1):34-46.
          pubmed: 3948593doi: 10.1111/j.1467-8624.1986.tb00004.xgoogle scholar: lookup
        83. Pederson DR, Moran G, Sitko C, Campbell K, Ghesquire K, Acton H. Maternal sensitivity and the security of infant-mother attachment: a Q-sort study.. Child Dev 1990 Dec;61(6):1974-83.
          pubmed: 2083509doi: 10.1111/j.1467-8624.1990.tb03579.xgoogle scholar: lookup
        84. Rosenblum LA, Paully GS. The effects of varying environmental demands on maternal and infant behavior.. Child Dev 1984 Feb;55(1):305-14.
          pubmed: 6705632
        85. Lyons DM, Kim S, Schatzberg AF, Levine S. Postnatal foraging demands alter adrenocortical activity and psychosocial development.. Dev Psychobiol 1998 May;32(4):285-91.
          pubmed: 9589217
        86. Houpt C. Formation and dissolution of mare-foal bond. Appl Anim Behav Sci 2002;78:1–11.
        87. Schaal B, Marlier L. Maternal and paternal perception of individual odor signatures in human amniotic fluid--potential role in early bonding?. Biol Neonate 1998 Oct;74(4):266-73.
          pubmed: 9701648doi: 10.1159/000014033google scholar: lookup
        88. Levy F, Poindron P, Le Neindre P. Attraction and repulsion by amniotic fluids and their olfactory control in the ewe around parturition.. Physiol Behav 1983 Nov;31(5):687-92.
          pubmed: 6665057doi: 10.1016/s0031-9384(83)80004-3google scholar: lookup
        89. Poindron P, Nowak R, Lévy F, Porter RH, Schaal B. Development of exclusive mother-young bonding in sheep and goats.. Oxf Rev Reprod Biol 1993;15:311-64.
          pubmed: 8336980
        90. Schaal B, Orgeur P, Arnold C. Olfactory preferences in newborn lambs: possible influence of prenatal experience. Behaviour 1995;132:251–263.
        91. Polan HJ, Hofer MA. Maternally directed orienting behaviors of newborn rats.. Dev Psychobiol 1999 May;34(4):269-79.
          pubmed: 10331151doi: 10.1002/(sici)1098-2302(199905)34:2<269::aid-dev3>3.0.co;2-lgoogle scholar: lookup
        92. Michelsson K, Christensson K, Rothgänger H, Winberg J. Crying in separated and non-separated newborns: sound spectrographic analysis.. Acta Paediatr 1996 Apr;85(4):471-5.
          pubmed: 8740308doi: 10.1111/j.1651-2227.1996.tb14064.xgoogle scholar: lookup
        93. Schapiro S, Salas M. Behavioral response of infant rats to maternal odor.. Physiol Behav 1970 Jul;5(7):815-7.
          pubmed: 5522499doi: 10.1016/0031-9384(70)90285-4google scholar: lookup
        94. Oswalt GL, Meier GW. Olfactory, thermal, and tactual influences on infantile ultrasonic vocalization in rats.. Dev Psychobiol 1975 Mar;8(2):129-35.
          pubmed: 1225689doi: 10.1002/dev.420080205google scholar: lookup
        95. Noirot E, Alegria J. Neonate orientation towards human voice differs with type of feeding.. Behav Processes 1983 Mar;8(1):65-71.
          pubmed: 24923609doi: 10.1016/0376-6357(83)90044-xgoogle scholar: lookup
        96. Smotherman WP, Robinson SR. Rat fetuses respond to chemical stimuli in gas phase.. Physiol Behav 1990 May;47(5):863-8.
          pubmed: 2388943doi: 10.1016/0031-9384(90)90010-2google scholar: lookup
        97. Brake SC, Sager DJ, Sullivan R, Hofer M. The role of intraoral and gastrointestinal cues in the control of sucking and milk consumption in rat pups.. Dev Psychobiol 1982 Nov;15(6):529-41.
          pubmed: 7152120doi: 10.1002/dev.420150605google scholar: lookup
        98. Als H, Gilkerson L. Developmentally supportive care in the neonatal intensive care unit. Zero to Three 1995;15:1–10.
        99. Egeland B, Erickson M. Psychologically unavailable caregiving. .
        100. Feldman R. Parent-infant synchrony and the construction of shared timing; physiological precursors, developmental outcomes, and risk conditions.. J Child Psychol Psychiatry 2007 Mar-Apr;48(3-4):329-54.
          pubmed: 17355401doi: 10.1111/j.1469-7610.2006.01701.xgoogle scholar: lookup
        101. Jaffe J, Beebe B, Feldstein S, Crown CL, Jasnow MD. Rhythms of dialogue in infancy: coordinated timing in development.. Monogr Soc Res Child Dev 2001;66(2):i-viii, 1-132.
          pubmed: 11428150
        102. Pastor DL. The quality of mother-infant attachment and its relationship to toddlers' initial sociability with peers. Dev Psychol 1981;17:326–335.
        103. Waters E, Wippman J, Sroufe LA. Attachment, positive affect, and competence in the peer group: two studies in construct validation.. Child Dev 1979 Sep;50(3):821-9.
          pubmed: 498856
        104. Fleming AS, Li M. Psychobiology of maternal behavior and its early determinants in nonhuman mammals. .
        105. Fleming AS, O'Day DH, Kraemer GW. Neurobiology of mother-infant interactions: experience and central nervous system plasticity across development and generations.. Neurosci Biobehav Rev 1999 May;23(5):673-85.
          pubmed: 10392659doi: 10.1016/s0149-7634(99)00011-1google scholar: lookup
        106. Rosenblatt JS, Siegel HI, Mayer AD. Progress in the study of maternal behavior in the rat: Hormonal, nonhormonal, sensory, and developmental aspects. .
        107. Arnold JL, Siviy SM. Effects of neonatal handling and maternal separation on rough-and-tumble play in the rat.. Dev Psychobiol 2002 Nov;41(3):205-15.
          pubmed: 12325135doi: 10.1002/dev.10069google scholar: lookup
        108. Pryce CR, Rüedi-Bettschen D, Dettling AC, Weston A, Russig H, Ferger B, Feldon J. Long-term effects of early-life environmental manipulations in rodents and primates: Potential animal models in depression research.. Neurosci Biobehav Rev 2005;29(4-5):649-74.
          pubmed: 15925698doi: 10.1016/j.neubiorev.2005.03.011google scholar: lookup
        109. Bertin A, Hausberger M, Henry L, Richard-Yris MA. Adult and peer influences on starling song development.. Dev Psychobiol 2007 May;49(4):362-74.
          pubmed: 17455227doi: 10.1002/dev.20223google scholar: lookup
        110. Siegel S, Castellan NJ. Non parametric statistics for the behavioural sciences (2nd Edition). .

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