Abstract

The neuropeptide oxytocin (OT) promotes maternal care and social affiliation in adults but its importance in infant attachment still remains unknown. True animal models of infant attachment are extremely rare, and the sheep (in complement to non-human primates) is one of the few that provides the opportunity to investigate its neuroendocrinological basis. In the lamb, access to the udder has strong rewarding properties for the establishment of a preferential relationship with the mother. Therefore, the present study explored the possible involvement of OT through its release during close social contacts with the mother. The first experiment revealed that lambs having free access to the udder from birth onward developed, by 12 h of age, a clear preference for their mothers over another maternal ewe. Delaying access to the udder for six, four or even only 2 h starting at birth, by covering the ewe’s udder, resulted in the lack of such a preference without affecting general activity. These effects persisted in most cases at 24 h but by 72 h of age a bond with the mother was clearly expressed. Experiment two showed that social interactions with the mother were followed by a release of OT in the plasma when lambs had the possibility to suckle. Non-nutritive interactions were without effects. Preliminary data on two subjects suggested that OT might also increase in the cerebrospinal fluid after suckling. Finally, in the third experiment, oral administration of a non-peptide OT receptor antagonist (L-368-899, Merck) over the first 4 h after birth led to decreased exploration of the mother’s body compared to lambs receiving saline, and impaired the expression of a preference for the mother at 24 h. The effects were no longer observed at 48 h. Our findings demonstrate that both delayed access to the mother’s udder and OT receptor antagonist alter the onset of mother preference in newborn lambs. This suggests that central OT facilitates the development of filial attachment through its release during suckling.

Highlights

  • Preferential interactions and mutual bonding in mammals are usually linked to litter size, mobility of the infant, duration of parental care and sociality [1,2,3,4]

  • The development of a preference for the mother after birth is dependent on the success of the first suckling bouts during which colostrum, as an internal signal, plays a key role [30,31,32]

  • This is an initial and crucial step leading to infant attachment in sheep

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Summary

Introduction

Preferential interactions and mutual bonding in mammals are usually linked to litter size, mobility of the infant, duration of parental care and sociality [1,2,3,4]. Bonds are more likely to emerge in species raising only one or two young, highly mobile, and where the risk of misdirecting maternal care is high. Mothers recognise their young on individual features and develop selective care [5,6,7]. The newborn acquires a multisensory image of the mother that forges its behavior in a preferential manner towards her [8]. This relationship may give rise to an attachment bond which refers to an affectional tie that one individual forms to another. Elaborated in humans first [9], this concept was extended to other mammalian species [1]

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