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Neonatal Handling Affects Durably Bonding and Social Development

By Séverine Henry, Marie-Annick Richard-Yris, Sylvie Tordjman and Martine Hausberger


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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    1. (2007). Adult and peer influences on starling song development.
    2. (1990). Alade OM
    3. (1968). Alleviation of learned helplessness in the dog.
    4. (1980). Aspects of the mother-infant relationship during nursing, 1 and 6 weeks after early extended post-partum contact.
    5. (1983). Attachment and dependency in developmental perspective.
    6. (2005). Attachment and development: a prospective, longitudinal study from birth to adulthood.
    7. (1969). Attachment and Loss,
    8. (1979). Attachment, positive affect, and competence in the peer group: Two studies in construct validation.
    9. (1983). Attraction and repulsion by amniotic fluids and their olfactory control in the ewe around parturition.
    10. (1970). Behavioral responses of infant rats to maternal odor.
    11. (1994). Behaviour of foals before weaning may have some genetic basis.
    12. (2000). Can adverse neonatal experiences alter brain development and subsequent behavior?
    13. (1999). Colostrum mediates the development of mother preference by newborn lambs.
    14. (2001). Commentary: Routines in Maternity Units: Are They Still Appropriate for
    15. (1977). Communication in infancy and early childhood: The newborn communicates. Journal of communication.
    16. (2001). Comparison of the effects of infant handling, isolation and non handling onacoustic startle, prepulse inhibition, locomotion and HPA activity in the adult rat.
    17. (1996). Confidence in protection: Arguments for a narrow definition of attachment.
    18. (1996). Crying in separated and non-separated newborns: Sound spectrographic analysis.
    19. (1977). Defining the limits of the maternal sensitive period.
    20. (1997). Development of a preferential relationship with the mother by the newborn lamb: importance of the sucking activity.
    21. (1993). Development of exclusive bonding in sheep and goats.
    22. (2001). Development of the hypothalamic– pituitary–adrenal axis and the stress response. In:
    23. (1995). Developmentally supportive care in the neonatal intensive care unit. Zero to Three 15:
    24. (2003). Do We Still Hurt Newborn Babies? A Prospective Study of Procedural Pain and Analgesia in Neonates.
    25. (1994). Does the newborn baby find the nipple by smell?
    26. (1996). Early environmental regulation of forebrain glucocorticoid receptor gene expression: implications for adrenocortical responses to stress.
    27. (1981). Early maternal-child contact: effects on later behaviour.
    28. (1993). Early postnatal experience alter hypothalamic corticotrophin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats.
    29. (1987). Early social relationships: A psychobiologist’s view.
    30. (2000). Early versus delayed initiation of breastfeeding.
    31. (2000). Effect of the Baby Friendly Initiative on infant abandonment in a Russian hospital.
    32. (1966). Effects of 6-day maternal deprivation on rhesus monkey infants.
    33. (1975). Effects of exposure to stressors in early life upon later behavioral and biological processes.
    34. (1979). Effects of extended post-partum mother-child contact on the mother’s behavior during nursing. Infant behav for dev 2:
    35. (2002). Effects of neonatal handling and maternal separation on rough-and-tumble play in the rat.
    36. (2005). Effects of short-term maternal separations on weaning stress in foals.
    37. (1978). Effects of various amounts of contact between mother and child on the mother’s nursing behavior: follow-up study.
    38. (1983). Equine behaviour: I. A review of the literature on social and dam foal behavior.
    39. (1980). Excessive handling as a cause of hypoxemia.
    40. (1977). Father-infant and mother-infant interaction in the first year of life.
    41. (2007). First suckling: a crucial event for mother-young attachment? An experimental study in horses (Equus caballus).
    42. (2002). Formation and dissolution of mare-foal bond.
    43. (1989). Hormonal effects of early rearing conditions in the infant rhesus monkey.
    44. (2003). Horse behaviour. The behaviour traits and adaptations of domestic and wild horses, including ponies. New Jersey: Noyes publ. (2d edition).
    45. (1970). Human maternal behaviour at the first contact with her young.
    46. (1991). Imprint training of the newborn foal. Colorado Springs:
    47. (1996). Individual differences in maternal style: cause and consequences for mothers and offspring. Advances in the study of behaviour 25:
    48. (1984). Infant-mother attachment: Factors related to its development and change over time.
    49. (2000). Influence of neonatal rearing conditions on stress-induced adrenocorticotropin responses and norepinephrine release in the hypothalamic paraventricular nucleus.
    50. (2006). Influence of various early human-foal interferences on subsequent human-foal relationship.
    51. (2006). Is a nappy change stressful to neonates? Early Human Development
    52. (1996). Long-term behavioral and neuroendocrine adaptations to adverse early experience.
    53. (1977). Long-term effect on mother-infant behaviour of extra contact during the first hour post partum. II. A follow-up at three months.
    54. (2005). Long-term effects of early-life environmental manipulations in rodents and primates: Potential animal models in depression research.
    55. (1998). Maternal and paternal perception of individual odour signatures in human amniotic fluid, potential role in early bonding?
    56. (1972). Maternal attachment: Importance of the first post-partum days.
    57. (1972). Maternal attachment: importance of the first postpartum days.
    58. (1986). Maternal behavior and attachment in low birthweight twins and singletons.
    59. (2005). Maternal behaviour and mare-foal interaction.
    60. (1990). Maternal sensitivity and the security of infant attachment: a Q-sort study.
    61. (2006). Maternal Sensitivity to Infant Distress and Nondistress as Predictors of Infant-Mother Attachment Security.
    62. (1999). Maternally directed orienting behaviors of newborn rats.
    63. (1998). Mother and infant: early emotional ties.
    64. (2005). Mother and newborn baby: mutual regulation of physiology and behavior. A selective review.
    65. (1995). Mother as a shield: differential effects of contact and nursing on pain responsivity in infant rats: evidence for nonopioid mediation.
    66. (2002). Neonatal foal handling.
    67. (1983). Neonate orientation towards human voice differs with type of feeding.
    68. (1999). Neurobiology of mother-infant interactions: experience and central nervous system plasticity across development and generations.
    69. (1988). Non parametric statistics for the behavioural sciences (2nd Edition).
    70. (1995). Olfactory preferences in newborn lambs: possible influence of prenatal experience.
    71. (1975). Olfactory, thermal and tactual influences on infantile ultrasonic vocalizations in rats.
    72. (1998). Ontogeny of social awareness in domestic herbivores.
    73. (1993). Parent-infant relationships in Mammals: factors of control and psychobiological implications.
    74. (2007). Parent-infant synchrony and the construction of shared timing: Physiological precursors, developmental outcomes, and risk conditions.
    75. (1978). Patterns of attachment: a psychological study of the strange situation. Hillsdale, NJ (USA): Lawrence Erlbaum Associates.
    76. (1998). Postnatal foraging demands alter adrenocortical activity and psychosocial development.
    77. (2001). Postpartum maternal oxytocin release by newborns: effects of infant hand massage and sucking.
    78. (1979). Progress in the study of maternal behavior in the rat: Hormonal, nonhormonal, sensory, and developmental aspects.
    79. (2003). Psychobiology of early social attachment in rhesus monkeys. Clinical implications.
    80. (2002). Psychobiology of maternal behavior and its early determinants in nonhuman mammals.
    81. (1987). Psychologically unavailable caregiving.
    82. (1989). Rat fetuses respond to chemical stimuli in gas phase.
    83. (2001). Rhythms of dialogue in infancy: coordinated timing in development.
    84. (2008). Sensitivity and attachment: A second perspective of De Wolff and van IJzendoorns meta-analysis.
    85. (1995). Separation distress call in the human neonate in the absence of maternal body contact.
    86. (2000). Skin-to-Skin Contact Is Analgesic in Healthy Newborns.
    87. (1996). Socialization, hormones and the regulation of maternal behavior in nonhuman simian primates.
    88. (1996). Somatosensation and maternal care in Norway rats.
    89. (1986). Spatial relations between mares and foals of the Welsh pony (Equus caballus).
    90. (1997). Successful breastfeeding in spite of early motherbaby separation for neonatal care.
    91. (1999). Suckling- and sucrose-induced analgesia in human newborns.
    92. (1992). Temperature, metabolic adaptation and crying in healthy full-term newborns cared for skin-to-skin or in a cot.
    93. (1961). The development of affectional patterns in infant monkeys.
    94. (2003). The effect of a gradual separation from the mother on later behavioral, immune and endocrine alterations in artificially reared lambs.
    95. (1997). The effect of mother-infant skin-to-skin contact on plasma cortisol and b-endorphin concentrations in preterm newborns.
    96. (2004). The effect of skin-to-skin contact (kangaroo care) shortly after birth on the neurobehavioral responses of the term newborn: a randomized, controlled trial.
    97. (2000). The effects of early rearing environment on the development of GABAA and central benzodiazepine receptor levels and novelty-induced fearfulness in the rat.
    98. (1991). The effects of rooming-in on the success of breastfeeding and the decline in abandonment of children.
    99. (1984). The effects of varying environmental demands on maternal and infant behavior.
    100. (1993). The position of the tongue during rooting reflexes elicited in newborn infants before the first suckle.
    101. (1981). The quality of mother-infant attachment and its relationship to toddlers’ initial sociability with peers.
    102. (1982). The role of intra-oral and gastro-intestinal cues in the control of sucing and milk consumption in rat pups.
    103. (2004). The various roles of animal models in understanding human development.
    104. (1971). Towards understanding individual differences in rhesus mother-infant interaction.
    105. (2003). Uvna ¨s-Moberg K
    106. (1989). Whitelaw A
    107. (1995). Widstro ¨m AM

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