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Pascal Poindron ´ ´ ´ Frederic Levy

Laboratoire de Comportement, Neurobiologie et Adaptation, UMR 6175 ´ INRA/CNRS/Universite de Tours/Haras Nationaux, 37380 Nouzilly, France E-mail: poindron@tours.inra.fr

Matthieu Keller
´ Centre de Neurobiologie Cellulaire et Moleculaire ´ ` Universite de Liege, Avenue de l’Hopital 1 ` B36, 4000 Liege, Belgique

Maternal Responsiveness and Maternal Selectivity in Domestic Sheep and Goats: The Two Facets of Maternal Attachment
ABSTRACT: Sheep and goats rapidly establish an exclusive relationship with their neonate following contact with it during a sensitive period of maternal responsiveness induced by the physiological events occurring at parturition. The data concerning the sensory, physiological, and neurobiological factors involved in the activation of both maternal responsiveness and the establishment of selective nursing indicates that these processes are activated simultaneously by the combined action of two main factors, the prepartum rise in circulating estrogen and the vaginocervical stimulation (VCS) caused by fetus expulsion. On the one hand, these two factors act on a neural network including the main olfactory system (MOB), the medial preoptic area (MPOA), and the paraventricular nucleus of the hypothalamus (PVN) to induce maternal responsiveness towards any neonate. The intracerebral release of oxytocin (OT) from the PVN, and the triggering of olfactory attraction for amniotic fluid (AF) are key elements in this process. On the other hand, VCS at birth also sets the MOB ready to memorize the individual odor of the neonate, through the release of peptides and neurotransmitters (noradrenaline and acetylcholine). In addition to the MOB, the network involved in recognition mainly includes the medial and cortical amygdala. Across consolidation processes, reorganization occurs in the network engaged in lamb recognition. Whether this memorization may be potentiated by other sensory cues is not known. The identification of the chemosensory compounds involved in the attraction for AF and in the recognition of the neonate is important for understanding the mechanisms of maternal attachment. ß 2006 Wiley Periodicals, Inc. Dev Psychobiol 49: 54–70, 2007. Keywords: maternal behavior; sensitive period; bonding; selective nursing; olfaction; recognition; neural network; neurobiology; social recognition

INTRODUCTION
Already in the early 60s, Hersher, Richmond, and Moore (1963a) had proposed a physiological control for the sensitive period of maternal bonding in sheep and goats. Nonetheless, after these early studies by their group and that of Klopfer, little was done for nearly two decades concerning the internal determinants of maternal behavior

Received 13 September 2006; Accepted 21 September 2006 Correspondence to: P. Poindron Published online in Wiley InterScience (www.interscience.wiley.com). DOI 10.1002/dev.20192 ß 2006 Wiley Periodicals, Inc.

in these two species. In that respect, the work of Rosenblatt, Siegel, and Mayer (1979) on rats was of utmost interest when we started to investigate the physiological factors activating maternal behavior in sheep (Le Neindre, Poindron, & Delouis, 1979). Some of ´ ´ us (Pierre Le Neindre, Pascal Poindron, and later Frederic ´ Levy) then had the good fortune to meet him, initiating a long lasting interaction which further stimulated our work. His genuine interest has always been for us very enriching and his ideas have been a guiding influence on our research. Therefore, it is a great pleasure and honor to write this review to acknowledge his esteemed contribution to the field of maternal behavior. Sheep and goats offer a unique opportunity to study the mechanisms by which a mother establishes an exclusive

Smith et al. Poindron & Le Neindre. In addition to selective nursing. Poindron et al... & Oddoye. & Boyes. Keller et al. mothers display a very strong but transient attraction for amniotic fluid (AF) and accept any neonate that is ´ presented to them (Levy. Also. Caba.. 1980. 1994. relationship with her young and thus to investigate how a selective emotional bond is formed in a mammal. Another feature of maternal care is that in both species. ewes and does become rapidly 1 Responsiveness is used in this review in the sense of immediate receptivity and display of maternal care in presence of a young. 1981. Indeed. Rosenblatt & Siegel. while the display of maternal responsiveness1 generally depends on physiological facilitation in laboratory species (e. 1993a). 1966).1002/dev Maternal Bonding in Sheep and Goats 55 FIGURE 1 Establishment of selective behavior after parturition in sheep and goats. 2000. attached exclusively to their neonate(s) and reject. parturient ewes and goats show an initial transitory period of maternal responsiveness controlled by physiological events related with parturition. Selective nursing is defined as acceptance of the own lamb and rejection of alien lambs (Adapted from Bordi et al.Developmental Psychobiology. Poindron. 2006. Bridges & Byrnes. mothers display a preference for their own young in a two-choice test within 4–6 hr after parturition. maternal selectivity in domestic sheep and goats has been regarded as a possible example of . Serafin. the maternal bond is not easily broken once it has been established and adoptions of alien young are quite difficult to perform. Fleming. Van-Toller. 1963a. any alien young that attempts to suckle (Hersher et al. rabbits. 1994. Fig. 2002.. & Moore. 2003. Raksanyi. & Terrazas. often with aggressive behavior. In contrast. with increased locomotor activity and emission of numerous high-pitched bleats (sheep: Poindron. 1979). Hernandez. 1966. 2003a). & Beyer. 1980. At this time.. and olfactory masking (Hersher. Romeyer et al. this exclusive care of the mother for her neonate is exhibited in several other ways. forced nursing... Smith. ´ Gonzalez-Mariscal & Poindron. 1980. Trillat. Rosenblatt et al.g. Krehbiel.. Le Neindre. & Orgeur. and adoption may necessitate 1 week or more of confinement.. Numan. Hence. The withdrawal of the own young induces a high state of agitation in the dam. Note the influence of the age of the young on its acceptance. Gilling. DOI 10. Oppong-Anane. 1983. 1). & Le Neindre. 1963b). & Levy. Richmond. Awotwi. Poindron. Spontaneous acceptance of lambs or kids have rarely been reported outside the period surrounding parturition (Hass. Thus. Gomora Arrati. in most domestic ungulates—with the exception of the swine—mothers rapidly develop exclusive care of the neonate they have been familiarized with from parturition. while maternal selectivity refers to exclusive care for the young the mother has bonded to. 2003. 2000). maternal care is rarely selective and mothers care for any young that is present in the nest. But contrary to most mothers of altricial young. 1990). rats. Poindron. goat: Addae. even though nursing is prevented (Keller et al. voles.

Piketty. if the neonate is removed at birth. 1975). without ´ developing an individual bond with their own (Levy. 1963b. Klopfer et al. let us see first what is the evidence that allows a distinction between these two aspects of maternal behavior. and how it relates to maternal responsiveness. 1975. should be of little consequence on its acceptance when reunited with its dam. & Lindsay. 1980. However.1002/dev imprinting in adulthood (Gubernick.. are seldom found outside the peripartum period. does the treatment allow the mother to remain responsive to any neonate?). Poindron. (2) exposure to the neonate during the sensitive period allows the mother to maintain maternal behavior towards this neonate for longer than if the contact occurs after the sensitive period has ended. assessed in most studies by the display of maternal care with a short latency (<30 min). Klopfer & Gamble. In the present review. Indeed. maternal responsiveness fades within a few hours in both species. focusing on three main questions: 1. since the conditions in which animals THE SENSITIVE PERIOD Sensitive Period Versus Critical Period The terms ‘‘critical period’’ and ‘‘imprinting’’ have been used in various early studies of maternal bonding in sheep and goats (Hersher et al. 1964. presence of a sensitive period and a rapid establishment of an individual preference to an attachment figure). indicating that there is some state of responsiveness to cues common to any neonate. 1966). Tillet. given that it appears to share some of the characteristics found in filial imprinting in birds (e. Nonetheless. This implies several things: (1) privation of contact during the sensitive period leads to poorer performances towards the young than in the absence of privation.. Consequently. & Poindron. Boundy. However. 1980. DOI 10. research on maternal behavior of sheep and goats has developed in two main directions: some work investigated the physiological factors controlling the activation of maternal responsiveness. Smith et al. 1963a. especially regarding the role of olfactory cues in this process. rendered anosmic before parturition by olfactory bulb ablation. When females are left undisturbed to give birth.g.. mothers accept any young. and those involved in maternal selectivity on the other. and goats.. It is difficult to propose precise boundaries for the sensitive period. 1995b. and (3) deprivation of the neonate after some contact during the sensitive period. But before we examine this point. Morgan. in the general sense proposed by Bateson (1979) that ‘‘an individual’s characteristics can be more strongly influenced by a given event at one stage of development than at other stages. High levels of maternal responsiveness. In most cases. Locatelli. what are the connections between the physiological and neurobiological factors and the nervous networks controlling maternal responsiveness on one hand. Poindron & Le Neindre. Klopfer. whether the activation of maternal responsiveness and the establishment of maternal selectivity are a sole and unique process or two different events is unclear. The distinction between maternal responsiveness and selectivity is further supported by the fact that ewes or goats. does the treatment allow the mother to bond to her neonate?).’’ Referring to maternal behavior of sheep . Arnold. Romeyer. Poindron et al. However. we use the term of sensitive period. derived from embryology and early studies of imprinting in young birds. or in terms of bonding (i. Poindron. this means that the contact with the neonate at a particular period (presumably parturition). and even a few hours before parturition if other young are present (Arnold & Morgan. does the sensitive period concern only maternal responsiveness or also bonding? 2.. will result in lasting effects on the maternal behavior of the mother. allow us to propose now a more comprehensive picture of maternal selectivity. & Klopfer.e. Klopfer & Klopfer.. or other methods of anosmia.e. especially neonates (Poindron & Le Neindre. are the cues eliciting the initial display of maternal behavior towards any neonate the same as those involved in the establishment of maternal recognition of the own young? 3. Smith et al. and Levy Developmental Psychobiology. before the mother has had any contact with it.. & Orgeur. Keller. The Sensitive Period and Maternal Responsiveness. the interrelations between the activation of maternal responsiveness and the establishment of maternal selectivity have been for some time the object of little attention. Adams. while other focused on the study of individual recognition of the lamb. are able to care for any young. 1966. the neonate during the sensitive period in sheep and goats may be interpreted in two ways: either in terms of maternal responsiveness (i.. 1982. In the present article. we review the relations between these two aspects of maternal behavior in sheep and goats. both ewes and does display maternal behavior within minutes following expulsion of the fetus. mothers are unable to display immediate maternal care when reunited with their young after 4–12 hr of separation (Hersher et al. the results of exposure to.56 ´ Poindron. However. 1968.. the progress of the last decade concerning the identification of the sensory cues and the brain mechanisms involved in the control of maternal behavior in sheep. 1964. 1980). 1966). were not fully appropriate for the study of maternal bonding. Lickliter. 1976a. two different aspects of maternal care in sheep and goats comes from the fact that at the very time of parturition. The first evidence that there are. it became rapidly obvious that these terms. 1994a). indeed. or privation of. 1981).

Thus. 2001. The fading of maternal responsiveness occurring when mothers are deprived of their neonate at birth is not due merely to the duration of the mother-young separation. Also. 1980. Poindron & Le Neindre. some results suggest that the sensitive period may be shorter in ´ goats than in sheep (Ramırez. or goats that are anosmic at parturition would not be able to remain maternal. 24 hr of separation from the lamb have no major detrimental effect on maternal behavior in ewes which had 24–48 hr of contact before the separation (Fig.. Note that maternal responsiveness fades in a similar fashion in intact and anosmic mothers. If selectivity was necessary for the postpartum maintenance of maternal behavior. DOI 10. Fig. ewes. there are several facts indicating that the fading of maternal behavior in mothers deprived of young at parturition is related to maternal responsiveness. Fig 2). when separation is performed either at birth or after an initial contact of 24 hr. the effects of deprivation of the neonate on maternal responsiveness should differ. For example in sheep. Levy et al. Poindron & Le Neindre. 2).. It could be argued that the inability of mothers to display maternal care after deprivation of the neonate at birth is due to the fact that they have not had the opportunity to bond to their young. contrary ´ to what is observed (Hernandez. Meurisse. Serafin. 1980). the percentage of mothers that accept a lamb tends to be higher for alien neonates than for the 12-hr-old own lamb. Sotillo. Poindron et al. Although this cannot be totally ruled out (see below for further discussion of this point). showing that ewes at this time are still more responsive to neonates than to the individual characteristics of a given lamb (Poindron et al. Quiles. Note also the better acceptance of a newborn alien after 12 hr of separation (Adapted from ´ Levy et al. & Poindron.. but to the time at which this separation is applied. it seems from the literature available that the initial period of maternal responsiveness during which mothers will spontaneously care for a young is shorter than 12 hr in most mothers (Fig.1002/dev Maternal Bonding in Sheep and Goats 57 have been tested vary between studies. the sensitive period can be regarded as a phase during which maternal responsiveness is sustained by the experience that the mother gains while interacting with her neonate. 1991. 1982).. Delgadillo. As a matter of fact the decline of maternal responsiveness is similar in intact and in anosmic ewes separated from their lamb (Poindron & Le Neindre. & ´ Ramırez. In any case. 1991. 2005. No experiments have ever investigated FIGURE 2 Effect of various times of separation from the neonate on the maintenance of maternal responsiveness in multiparous ewes. to be sure that they result from the existence of a sensitive period.Developmental Psychobiology. Klopfer & Gamble.. 1996). 1980. Nonetheless. 2. after 12 hr of separation from birth. Furthermore. parity may influence this duration (Lickliter. ´ ´ & Levy. 1966). Also. Klopfer et al. depending on the time at which the separation occurs. Keller. 1980). Hevia. Vazquez. Even a few minutes of contact at birth are sufficient for does to maintain maternal responsiveness for 2–3 hr without their neonate (Gubernick. 1964). 1981. The Sensitive Period and Maternal Selectivity One way to assess whether the establishment of maternal selectivity depends on the sensitive period is to study the rapidity with which selectivity develops at various times during this period. . 1980. 2).

once established. while no effect is observed in sheep after 12 hr in the same conditions. Only one study has investigated this in the postparturient goat (Klopfer & Gamble. even following 12 hr of treatment (Poindron & Le Neindre. resulting in the rejection of the kid by four does out of seven. These results would rather indicate that the first hour postpartum is critical for the establishment of selectivity. 1979). 1986). If the establishment of selectivity during the sensitive period is important for the later display of maternal acceptance. suggesting that the rapidity of establishment of selectivity may not differ fundamentally at birth or 8–12 hr later. 1980).58 ´ Poindron. Cues Involved in the Maintenance of Maternal Responsiveness Evidence from Partial Separation Studies. 3. does not impair the maintenance of maternal responsiveness in the ewe. However. The effects of deprivation of specific sensory cues during the sensitive period underline that maternal olfaction plays a major role in the maintenance of maternal responsiveness.. but it cannot be excluded that they are partly due to exogenous administration of estrogens. . Poindron. Stevens. Mothers were exposed to their lamb placed in a double wire cage either at birth or 1 hour later and tested at 12 hr postpartum. 1986). While the onset of the sensitive period certainly reflects the onset of maternal responsiveness towards any lamb (therefore independent of maternal attachment). 1966) in a small number of animals. and Levy Developmental Psychobiology. such a dissociation is not found: following a 36 hr separation mothers are either maternal and selective. preventing physical contact and thus suppressing the sensory cues provided by licking and suckling. the maintenance of maternal behavior beyond its initial limits of about 24 hr may well depend on the establishment of selectivity. anosmia performed during this separation period should impair acceptance of the mother’s own young. 1980. contradictory results have been obtained in another study investigating the consequences of delaying contact with the neonate (Alexander et al. the proportion of ewes becoming selective after 15 min of contact with their own young (Poindron. whereas after 7 days of contact. 1980). SENSORY CUES AT PLAY DURING THE SENSITIVE PERIOD FOR THE ESTABLISHMENT OF MATERNAL RESPONSIVENESS AND SELECTIVITY The sensitive period is generally considered a transition from a control of maternal responsiveness by physiological factors internal to the mother. In the goat however. 1980). Nonetheless. was intermediate between that found for ewes tested either at birth (21%) or after 30 min of contact (61%. 4. & Krehbiel. 1). Further information can be obtained from studies of anosmia or olfactory cues deprivation several weeks postpartum (Alexander. In contrast. DOI 10. 1994. & Bradley.. While delaying contact did not impair the display of maternal care towards their own lamb. Bordi et al. Levy. 64% of ewes deprived of their lamb during the first hour had failed to develop maternal selectivity at 12 hr. 1993a).. Keller.. to a neurosensory control by sensory cues from the young (Poindron & Le Neindre. as long as AF is not removed from the lamb’s coat (Alexander et al. Thus. Regardless of the method of olfactory deprivation. Romeyer et al. This is further supported by the fact that when a mother-young separation of 36 hr is performed at 4 hr postpartum. After 8–12 hr of total separation.. suppression of visual cues does not impede the ability of ewes to ´ remain maternal (Fig. regardless of whether they can see them or not (Poindron & Le Neindre. These results would rather support the hypothesis that the rapidity of bonding may not be strongly influenced by the moment of the sensitive period at which olfactory experience is obtained. Fig. Poindron & Le Neindre. versus 9% for ewes in contact with their lamb from birth. or not maternal at all (Keller et al. 1988). presenting or suppressing cues of the neonate during the sensitive period will provide valuable information about their importance for the maintenance of maternal responsiveness and selectivity beyond the sensitive period. 1981). 1980). some indications can be obtained from studies in which mothers totally separated from their lamb at birth were tested for the acceptance of an alien lamb several hours later (Poindron & Le Neindre. 1986). 1983. since maternal olfaction plays a major role in selective nursing (see next section). dissociation between maternal responsiveness and selectivity is easily obtained (most mothers are not selective.. which were used in this study (Alexander et al. Whether reacceptance of the ewe’s own young after a separation performed several hours after parturition is due to the establishment of maternal selectivity can also be investigated by studying the effects of postpartum anosmia. the recognition of the lamb by its dam would become an important factor controlling maternal responsiveness. Also. about half of mothers show some impairment of maternal acceptance of their own young. mothers that cannot smell their lamb during the first 8 hr postpartum do not maintain maternal responsiveness better than mothers totally isolated from their neonate. Thus in the sheep. Rosenblatt et al. 2005). Hence.1002/dev this point specifically.. physical contact probably plays a more important role for the maintenance of maternal responsiveness: preventing licking and suckling for 4 hr prevents the maintenance of maternal responsiveness in a significant proportion of mothers (Fig. while they are still maternal).

1988). in goats. 1980 for sheep and from Romeyer et al. Duration of treatment: in sheep. FIGURE 4 Effect of preventing licking and nursing of the neonate during the sensitive period on the maintenance of maternal responsiveness and the establishment of selective nursing in sheep and goats.Developmental Psychobiology. 1980 and Poindron et al. 1993a and Bordi et al.1002/dev Maternal Bonding in Sheep and Goats 59 FIGURE 3 Effects of exposure to various sensory cues from the lamb during the sensitive period on the maintenance of maternal responsiveness and the establishment of selective nursing. For definition of selectivity see Figures 2 and 3. .. adapted from Poindron & Le Neindre. Selectivity concerns only mothers that had retained maternal responsiveness (i. Preventing licking and suckling seems to induce more disturbances of maternal responsiveness and selectivity in goats than in sheep (Adapted from Poindron & Le Neindre. Note the importance of olfaction for the maintenance of maternal responsiveness... Olfaction þ Hearing group. DOI 10. that accepted their own lamb).. 4 hr. 12 hr.e. Note also the facilitation of maternal selectivity in mothers that can see their lamb (Sight þ Hearing group vs. 1994 for goats).

Romeyer et al. Romeyer & Poindron. 1991). 1995b). Poindron.. For example. Smith et al. Conversely. In contrast. 1976b).. 1980. in mothers deprived of their lamb immediately after parturition.. 1974. Bouissou. the fading of maternal responsiveness parallels that found for AF attraction.. depending on the experimental procedures used. & Levy. 1980.1002/dev It is not known whether this detrimental effect results from the privation of the somatosensory cues provided by nursing. and absence of selectivity later than 4 hr postpartum is rare (Keller et al. & Orgeur. section of the main olfactory nerves (Morgan et al. contrary to what occurs for maternal responsiveness. If an effect of licking privation was confirmed. As a whole.. the effects are less pronounced and do not impede the mothers to display maternal behavior. Therefore. sheep: Levy et al. except during a few hours around parturition when they become strongly attracted to it. than a 12-hr-old alien which coat is already dry. In agreement ´ with the effects of AF privation in intact ewes (Levy & Poindron. 1992. parturient ewes accept more readily an alien newborn. 1995b. ´ Levy et al. no evidence has been found for a specific influence of the accessory olfactory system on maternal responsiveness following ´ lesion of the vomeronasal organ (Levy et al. do care for their neonates and ´ nurse young adequately (Hernandez et al. comparing the slight effects of prepartum anosmia with those obtained by preventing the perception of olfactory stimuli in the intact mother indicates that prepartum anosmia can be compensated for by other sensory cues. Ewes undergo a dramatic change of behavior towards AF at the very moment of parturition. but is somewhat ´ specific to the own species (Arnould. 1964. 2001. Evidence for the importance of olfaction in the recognition of the young comes from experiments of olfactory bulbs ablation (Baldwin & Shillito. and this phenomenon is olfactory dependent ´ (Levy et al. ´ Romeyer et al. Interestingly. it could then suggest some role of the vomeronasal system in the regulation of maternal responsiveness in the goat. Klopfer et al. 2001). 2006). contrary to what is found after removing AF from the lamb’s coat in intact dams.. This convergence of results indicates that (1) maternal selectivity depends primarily on olfactory recognition of the young and (2) that this monosensory control is not subject to compensatory processes when the olfactory system is lesioned. 2002. Also. Ewes and does learn to discriminate their own neonate from an alien one very rapidly after parturition. or from an impairment of olfactory perception due to licking privation (Romeyer et al. Contrary to the privation of olfactory cues in intact mothers. Hernandez et al. Poindron & Le Neindre. 1994b). as already reported in the rat (Numan et al. maternal acceptance after parturition is facilitated by AF. such a process does not take place when the olfactory system is intact. 1974. ´ Romeyer. prepartum anosmia also impairs the ´ display of maternal behavior in primiparous ewes (Levy et al.. 1987). and peripherally induced anosmia. So far. This is also the case following ablation of the olfactory bulbs. 1968). primiparous parturient ewes are unable to develop an appropriate maternal behavior if AF has been removed from their lamb’s coat. Nonetheless. 1984). prepartum lesion of the main olfactory mucosa or ablation of the olfactory bulbs has little consequences on the display of maternal behavior at parturition or its maintenance. Sensory Cues Involved in the Establishment of Maternal Selectivity The Effects of Prepartum Anosmia. Bouissou.. Another way to investigate the role of maternal olfaction during the sensitive period is to study the effects of prepartum anosmia. Levy. Porter. 1983). and Levy Developmental Psychobiology. Poindron ´ & Le Neindre. suggesting that the two phenomena are closely associated. 1987). 1966. 2002. The initial attraction for AF does not depend on the identity of the giver.60 ´ Poindron. the effects of anosmia on maternal responsiveness probably do not reflect the actual role of this sensory channel in intact mothers. 1995b). even though bulbectomy may slightly facilitate maternal aggression toward the young in sheep (Baldwin & Shillito.. In fact. 2003. but 30 min of contact appears sufficient to allow the display of maternal selectivity in more than half of mothers in sheep and goats (Keller et al.. 1966). or both. and in multiparous mothers licking behavior is strongly impaired ´ (Levy & Poindron. 1975). 1968.. The reported period of contact necessary to do so varies between studies... whose coat is fully wet with AF. Keller. 1994a). smothering 12-hrold alien lambs (whose coat is dry) with AF facilitates ´ their acceptance by parturient mothers (Levy & Poindron.. DOI 10. 1994a. 1980).. AF also facilitates acceptance in mothers that have been immediately separated from their neonate at birth for 12 hr: they tend to accept more readily an alien newborn than their own 12-hr-old dry lamb (Poindron et al.. It is more adequate to rely on results of olfactory cues manipulation in intact mothers for studying the role of maternal olfaction. One major source of olfactory stimulation that facilitates the display of maternal behavior at parturition is the AF which bathes the neonate. Ewes and goats rendered anosmic before parturition by lesion of the main olfactory epithelium. Piketty. 1995b.. Another issue is determining whether olfactory recognition of the young depends on the main or on the . this does not apply when studying olfactory recognition of the neonate. AF is strongly repulsive for ewes at any stage of their reproductive cycle. However. Poindron.. all these methods preventing the establishment of selective nursing ´ (goat: Hernandez et al. 1993a). Klopfer & Gamble. 2003.

1994). In goats. Furthermore.. Tillet. Orgeur. even if physical contact is prevented (Fig. Thus. share much closer signatures. 1994. even in anosmic mothers (Poindron. at least in sheep. 1995b) and this is further supported by the studies of the neurobiological processes involved in olfactory memory formation (see Section Physiological and Neurobiological Control of Maternal Responsiveness and Selectivity). Absence of physical contact with the neonate seems to delay bonding.. Stevens. in young with initially very similar signatures (e. Romeyer et al. Poindron et al. 2003a). Levy et al. Romeyer et al. This is especially relevant since recent studies indicate that early recognition of the neonate by visual .1002/dev Maternal Bonding in Sheep and Goats 61 accessory olfactory system. Romeyer et al. However.. Mothers may have already gained some information about the olfactory identity of their lamb at its birth. & Schaal. 1989. 1977. this would nonetheless be consistent with the effects of licking or AF deprivation on the rapidity of establishment of selectivity (see next paragraph). Alexander & Shillito. 1978).. Gubernick. & Signoret. Various experiments have demonstrated that they are olfactory signatures unique to each young. presence of AF on the lamb’s coat tends to facilitate bonding in mothers deprived of licking (Alexander et al. Possible Synergy with Other Sensory Channels. It is unlikely that the effects of peripheral anosmia could be due to the lesion extending to the vomeronasal organ (Cohen-Tannoudji. 1996.. The discrepancy between these results and the rest of the literature are probably due mainly to an ineffective lesion of the main olfactory mucosa associated with inadequate testing of anosmia (Poindron et al. 1976a). 2000). The Nature of the Olfactory Cues Involved in Individual Recognition. due to prepartum ingestion of AF. 1984). only the effects of physical contact deprivation have been studied. & Nevison. 1993b). 4). While there is little neurobiological evidence to indicate a participation of the vomeronasal system in olfactory recognition of the neonate (see Section Physiological and Neurobiological Control of Maternal Responsiveness and Selectivity). & ´ Romeyer.. then visual cues have a facilitating influence on the establishment of maternal selectivity (Fig. Therefore. for example when the lamb is kept in a smell-proof box and its odor provided to the mother by a ventilation system every 30 min (Poindron et al. 3).. ´ Locatelli. Levy. AF could also participate in the initial olfactory signature of the neonate. possibly because of some reinforcing influence of suckling and/or of vomeronasal input gained from licking (Bordi et al. given the role often played by the accessory system in several social recognition processes in mammals (Johnston. It is true that mothers close to their lamb do establish selective behavior.. DOI 10. 1993a). facilitating both the immediate acceptance of the newborn. Nowak.. Monozygotic twins. within a short time after its birth. Lavenet. Keverne.. 1993b). it can contribute to the development of odor differences between neonates. known as maternal labeling (Alexander. The exact nature of the cues responsible for the individual olfactory signature of lambs and kids is yet to be identified. 1996). 1993a). AF plays a dual role in the establishment of maternal behavior. the vomeronasal system cannot unequivocally be excluded from participating in the establishment of maternal selectivity. monozygotic twins. there is one report in sheep suggesting that the establishment of olfactory recognition of the newborn depends on the accessory rather than on the MOB (Booth & Katz..g. 1981). Nonetheless.. 1986. It is well established that these cues are not effective at distances greater than 25 cm (Alexander. for example. Kendrick. 1991. and the results suggest that physical contact may be more important than in sheep. the individual olfactory signature of a young is likely to be made of a mosaic of compounds resulting from complex interactions between genotypic and environ- ´ mental influences (Levy. 1998. little attention has been paid to the possibility that other sensory modalities may contribute to this process as well. Poindron et al. 1980 and 24% in that of Keller et al. sight or hearing) could facilitate the formation of the bond. however. Martel. Porter. The facilitating effect of AF on the acceptance of dry alien lambs is more marked if AF ´ from the own mother/lamb is used (Levy & Poindron. & Bradley. 2003). 1986). Porter. 2003b). and the establishment of its recognition. Transmission of odors from the dam to the neonate.. Romeyer et al. suggesting that they are either little volatile and/or present at very low concentrations. The effects of partial sensory deprivation during the sensitive period on maternal selectivity provide evidence supporting this possibility. if olfactory perception is somewhat limited. even in the case of dizygotic twins (Porter et al.g. 1978. 1989. This is in agreement also with the fact that marked differences in visual aspect of the lamb may influence its acceptance at the udder (Alexander & Shillito. The presence of individual olfactory cues in AF could also partly explain why some ewes already discriminate their neonate from an alien one at parturition (10% in the study of Poindron et al. indicating some genotypic basis of olfactory identity (Romeyer et al.. 1993a). 1988. However. Nonetheless. In both species further studies would be necessary to investigate the possibility that other sensory channels (e... 1988)..Developmental Psychobiology.. While numerous studies demonstrate that maternal olfaction is an absolute requisite for the establishment of maternal selectivity. is not critical for the initial establishment of maternal selectivity (Alexander et al. Keverne.

62 ´ Poindron. In one study. & Perrin. & Kendrick. Poindron. Poindron et al. 2006). maternally responsive and selective) and ewes receiving VCS or rendered anosmic before parturition (i. & Lindsay. can be reinstated by VCS up to 8 hr postpartum (Poindron et al. & Poindron. 1991. MPOA inactivation impairs maternal responsiveness whereas inactivation of BNST or infusion of artificial cerebrospinal fluid do not. Indeed. 2003.. 1988). Taken separately. in the goat about the factors responsible for the induction of the sensitive period. 1981). 1988). by infusing an anesthetic before parturition and during the first 2 hr postpartum ´ (Levy.. Keller. expulsion of the fetus is likely to be involved. In addition. which fades rapidly after parturition. although it has been established that ewes and goats are already able to recognize the voice of their neonate at 24 and 48 hr postpartum. despite the major importance of maternal olfaction. Poindron et al. 2005). when interest for the lamb is challenged by taking the young away and by allowing the mother to join it. Sebe. these structures certainly represent the core of the circuitry for maternal receptivity in sheep as they also do in rodents (see reviews by Numan & Insel. & Levy. Keverne. and the paraventricular nucleus of the hypothalamus (PVN). even though the effects are much less marked than in the sheep (Poindron et al.. 1997). 2000. intact ewes and goats do show a preference for their young at 6 and 4 hr. The functional involvement of the PVN has been demonstrated through c-fos and c-jun antisense infusions that PHYSIOLOGICAL AND NEUROBIOLOGICAL CONTROL OF MATERNAL RESPONSIVENESS AND SELECTIVITY In the last decade.. Ferreira. On the one hand. maternally responsive.. attempts to induce maternal behavior with sexual steroid treatments have been unsuccessful (Rosenblatt & Siegel. Also. mother sheep and goats are also able to discriminate their young on the basis of other sensory cues. The effects of MPOA and BNST inactivation were investigated in primiparous ewes. Levy.. Thus. Preference for the neonate on the first day postpartum has also been found in mothers rendered anosmic before parturition (Ferreira et al.. On the other hand.e. 1980). 1998). and Levy Developmental Psychobiology. 2003 and Numan et al. indicating that the BNST is also involved soon after parturition. Indeed. since peridural anesthesia at parturition impairs the display of maternal behavior..e. behavioral impairments are observed both after BNSTor MPOA inactivation. However. 2003. Nowak. the respective roles of vision and hearing at this early stage have not been clarified. Keller. the length of the sensitive period can be increased by exogenous estradiol treatment (Poindron & Le Neindre.1002/dev and/or acoustic cues is also present very rapidly after parturition. 2003a). which act in synergy: the prepartum production of estrogen by the placenta and the vaginocervical stimulation (VCS) caused by the expulsion of the fetus. 2004a). these two factors are hardly effective and only their association induces a rapid display of maternal care (Kendrick & ´ Keverne. which allows the display of maternal responsiveness but prevents the establishment of bonding ´ (Keller. So far. sheep: F. The use of various immediate early genes as markers of neuronal activation has allowed the investigation of the neuronal networks involved in the activation of maternal responsiveness in the ewe. Thus. Her` nandez. brain activations resulting from normal mother–young interactions were compared with those found in females receiving a treatment to induce maternal receptivity but prevented from displaying maternal care (Da Costa. Serafin. the pattern of gene expression observed between ewes displaying maternal behavior (i. attraction for AF. Thus. studies of the physiological factors and brain mechanisms that regulate the onset of maternal behavior in sheep have led to a better understanding of the relationships between maternal responsiveness and the formation of a selective bond. Poindron et al. Neural Structures and Neurochemical Processes Involved in Maternal Responsiveness. The functional involvement of these structures was explored using various pharmacological approaches. Its duration also depends on the time during which these two factors are present. these brain activations were measured in mothers rendered anosmic before parturition. Therefore. respectively (goats: Terrazas. 2003a).. Activation of maternal behavior in the ewe depends mainly on two factors. DOI 10. Both studies revealed that the induction of maternal responsiveness involves extensive neural circuitry in the brain including various limbic and hypothalamic areas. Meurisse. Maternal Responsiveness Hormonal and Proprioceptive Factors Controlling Maternal Responsiveness. Meurisse. in a two-choice test excluding the use of olfactory cues. It has not yet been investigated whether ewes and goats may show a preference for their own neonate without the help of olfactory cues earlier than 4–6 hr postpartum. Broad. but not selective).. personal communication). In another study. respectively (Keller et al. the existence of a sensitive period of maternal receptivity is the result of the action of these two factors. 1983. the bed nucleus of the stria terminalis (BNST). were remarkably similar in the medial preoptic area (MPOA). little is known .

. Sirinathsinghji.. & Kendrick. Goode. However. expulsion of the fetus facilitates the formation of the maternal bond. In any case. 1980). Some results in sheep suggest that they may modulate the establishment of bonding (Alexander et al. Hence. Meurisse et al. DOI 10. Furthermore. & Keverne. 1996). & Keverne. 1989) or allow bonding in the absence of VCS (Le Neindre et al. paraventricular nucleus of the hypothalamus. 1994b). Indeed.. 2005). & Keverne. 1992b. 1995a). Kendrick.. main olfactory bulb.. 1996. 1997a). 1992a). in studies of the sensitive period in which ewes were induced to lamb using high doses of estradiol.1002/dev Maternal Bonding in Sheep and Goats 63 impair some aspects of maternal behavior in parturient ewes (Da Costa. an increased number of cells containing estradiol receptors in the hypothalamic oxytocinergic system may be responsible for the higher expression of OT receptor mRNA (Broad. which in turn facilitates maternal responsiveness at parturition. 1979). Levy et al. retrodialysis infusion of OT stimulates maternal behavior in nonpregnant animals primed with a steroid treatment (Da Costa. Hinton. This could in turn result in an easier display of maternal behavior at parturition. VCS performed after the establishment of maternal selectivity allows mothers to form a new ´ bond with an alien newborn (sheep: Kendrick. Kendrick.. In other words. medial preoptic area. MPOA. De La Riva. MOPA.. & Kendrick. MPOA. or GABA release in the MPOA and olfactory bulb (Da Costa et al. it appears that initial maternal responsiveness depends on the activation of a neural network in which the MPOA and the PVN play a central role. in vivo microdialysis revealed that OT is released in the PVN at lambing as well as during artificial VCS. Ohkura... bed nucleus of the stria terminalis. & Goode. Broad et al. . 1999).. and PVN. 1993. Various studies indicate that estradiol facilitates the priming of the oxytocinergic system. administration of estrogen after the formation of the bond does not allow to Amniotic Fluids MOB MPOA BNST PVN Vagino-cervical Stimulation Maternal Ca re Olfa ct o ry i n p u t s Oxyto ci ner gic i np uts V a g i n o c e r v i c a l st i m u la t i o n i n p u t s FIGURE 5 Neuronal network involved in the activation of maternal responsiveness in the ewe. 1991. The main action of VCS in the brain is to induce a release of oxytocin (OT) that stimulates maternal respon´ siveness (Kendrick et al. BNST.Developmental Psychobiology. Goode. and the olfactory bulb during parturition and/or following VCS (Da Costa et al. ´ ´ Kendrick.. we found no evidence for an effect of estradiol on selectivity (Poindron & Le Neindre. Numan et al. SanchezAndrade. OT release also occurs in the BNST. 1986. 5). PVN. Whether estrogen may influence maternal selectivity remains an open question. Guevara-Guzman. As a whole. Release of OT at birth and/or in response to VCS occurs primarily in the PVN. & Kendrick. 1999a. In sheep as well as in goats. infusions of OT by retrodialysis at doses that influence components of maternal behavior can increase noradrenalin (NA) release in the olfactory bulb. Keverne. 1997a. 2006). 2005a). as demonstrated in other types of social memory (Choleris et al. while the MOB is tuned to respond optimally to the cues from the neonate to ensure the immediate display of maternal care (Fig. Maternal Recognition and Selectivity Peripheral Factors Involved in the Establishment of Maternal Selectivity. VCS has specific effects that promote learning of the olfactory identity of the neonate. 1996. 2003. Indeed. which is the main source of OT release in the brain.. More studies are needed to assess whether estrogen may play some role in olfactory recognition of the lamb. Levy. and contrary to what is found for VCS. Kendrick. Also. Levy. & Keverne. Levy. MOB. James. For example. 1996. OT may also stimulate maternal receptivity by facilitating release of various neurotransmitters within these structures and other neural substrates specifically involved in its control (Kendrick et al. Guevara-Guzman. However. goat: Romeyer et al. Guevara-Guzman.

Poindron. early recognition of the newborn lamb or kid. 2003). & Levy.. Meurisse. Levy et al. Trinh & Storm. NA. While inactivation of the piriform cortex has no effect on the establishment of maternal selectivity (Broad. 2000). Therefore.. 1993. 1995b). and Levy Developmental Psychobiology.. Using pharmacological tools.. as illustrated in Figure 6. ´ Kendrick et al. A possible contribution of the accessory olfactory system in the olfactory recognition of the young remains an open question. 2000). 1997. Neural Structures and Neurochemical Processes Involved in the Establishment of Maternal Selectivity. There are indications that the interactions between OT. Leinders-Zufall et al. & Le Neindre. these neurochemical releases were shown to be involved in the olfactory learning leading to individual lamb recognition (Ferreira. It is possible that the reduction of licking behavior ´ in anosmic ewes (Levy et al.. but also in the anatomically distinct AOB (Keller. Iwamoto. 1991) or the inability of inexperienced mothers to compensate for the privation of AF ´ olfactory cues or VCS (Levy & Poindron. 2000. Poindron ´ & Levy. 1987. since perception of volatile compounds by the VNO has been demonstrated. & Piketty. Kendrick. Levy et al. 1998.. 1985). these neurobiological differences concern probably other aspects of maternal behavior. 1990). Chapman.. 1984). and ACh that take place in the MOB in the first hours postpartum are not related only to olfactory recognition memory. Indeed. & Jackson. Additional olfactory structures. Kendrick. Keller. 2001. & Keverne. The functional involvement of these structures has been addressed by studying the effects of their reversible blockade. and cortical nuclei of the amygdala) and tertiary (orbitofrontal and frontal medial cortex. in the sheep both MOB and AOB send projections to the cortical nucleus of the amygdala (Jansen. 1990. also play an important role in the establishment and display of maternal selectivity.1002/dev induce the acceptance of another lamb (Alexander et al.. & Baldwin. Keller et al. supporting the idea that a coding for odor familiarity takes place at the first relay of the olfactory information (Kendrick et al. Ravel. evidence for the involvement of the main olfactory bulb (MOB) in the recognition of the young comes from electrophysiological and neurochemical studies performed during the early postpartum period. 1992b. recent results indicate that in fact primiparous ewes are as fast as experienced mothers to develop maternal selectivity (Keller et al. Orgeur. ´ vy. at least in rodents (Johnston. Therefore. other than the MOB. although it is not totally clear whether it is directly by acting on the learning process or indirectly through its modulatory action on NA and ACh release. 1995a). entorhinal cortex) olfactory processing regions. we found that anosmia induced by irrigation of the nasal cavities with zinc sulfate induces a loss of cellular activation of the immediate early gene zif-268 in the granular layer not only of the MOB. Guevara-Guzman. They may be related with the more frequent display of maternal disturbances found in primiparous mothers (Dwyer & Lawrence. As described in Section Sensory Cues at Play During the Sensitive Period for the Establishment of Maternal Responsiveness and Selectivity. While this was initially though to relate to the fact that primiparous mothers (without previous maternal experience) were slower to establish a selective bond (Kendrick. 1997. In a recent experiment. the lack of response to VCS in nonpregnant nulliparous ewes (Kendrick & Keverne. 2003). several nonexclusive explanations can account for this effect. 2005b).. Centrifugal projections from the cortical nucleus to the AOB could be responsible ¨ for this effect (Pitkanen.b. 1994). ´ Levy. 1995b) results in a lower stimulation of the VNO sensory neurons by AF and lamb odors. 2000. Keller.. Raksanyi. Thiery. OT release that occurs in the MOB at parturition ´ further enhances NA and ACh activation (Levy et al. Hinton. This concomitant decrease of zif-268 activity in MOB and AOB could also result from interactions between the main and accessory olfactory systems in structures of convergence for the two olfactory systems (see below for details about other structures involved in maternal selectivity). Keverne. OT is also likely to play some role in the bonding process (Kendrick. medial. 1989). These activations occur when ewes are exposed to lambs after birth but not if they receive VCS alone or if they are rendered anosmic through zinc sulfate treatment (Da Costa et al. 1997b. In the sheep. Gervais. Electrophysiological recordings from olfactory bulb mitral cells showed that these cells respond preferentially to lambs odors after birth. 1995a). Levy. Meurisse. Poindron. Previous works performed in our laboratory have shown that such an irrigation of the nasal cavities with zinc sulfate does not affect the integrity of the neuroreceptors of the VNO in sheep (Cohen´ Tannoudji et al. Meurisse. a proportion of the cells respond preferentially to the odor of the ewe’s own lamb. These electrophysiological changes are reflected in concurrent changes in the release of peptides (GABA and Glutamate). and of NA and acetylcholine (ACh) in the MOB (Kendrick et al. 1997a. The increase of neurotransmitter release is ´ modulated by maternal experience (Levy et al. Thus it is likely that lesion of the MOB also results in a lower activation of the accessory olfactory network. 1993. Fabre-Nys. Gervais. 1992b). ´ Perrin. & Levy. Kindermann. 1988a. Le ´ Pissonnier. DOI 10.. 1995a). 2003).. Orgeur. and establishment of selectivity depend on the sense of olfaction.. . 1989.64 ´ Poindron. In this context. 1998. 2004a). & Keverne.. & Ravel. Immediate early gene expression related to the learning of the lamb odor increases in secondary (piriform cortex. In addition. Richard. ´ 1993.

the structures responsible for olfactory recognition memory are rather limbic and cortical (medial and cortical amygdala. While the olfactory system is involved in the display of maternal responsiveness as well as in the establishment of selectivity. 2004). medial amygdala. Ferreira. and interacting with the neonate allows its consolidation. 2002). 2004b). Furthermore. the neural mechanisms that control maternal responsiveness and selectivity differ in various aspects. Sanchez-Andrade et al. Moreover. 2005). Either the sensitive period has to do with bonding and can be regarded as part of an imprinting process similar to the one existing in young birds (i. Hinton. They also share immediate triggering factors. However. EC. the more central structures involved in maternal responsiveness and in selectivity are clearly different. Hinton.b. retrieval of memories involves time-dependent participation of a set of cerebral regions (Bontempi. A more preeminent role for the medial and the cortical nuclei of the amygdala. may be the existence of two sensitive periods. as are probably also some of the neurobiological processes activated. maternal responsiveness and maternal selectivity are two intermingled processes that lead to maternal attachment. would be necessary to clarify this point. piriform and entorhinal cortices show significant expression of activation markers. Thus. PC. ´ Perrin. The functional significance of this enhanced activation remains to be explored. has been recently demonstrated (Keller. It has been shown that across consolidation processes. CONCLUSIONS AND PERSPECTIVES This review underlines that in domestic sheep and goats.. DOI 10. FMC. Maviel. CoA. Da Costa. These two components are synchronized since maternal receptivity is present at parturition and bonding starts as soon as contact with the neonate occurs. while retrieval of more consolidated memory (7 days post- . cortical amygdala. consolidation processes induce time-dependent reorganization in the network engaged in lamb recognition. Menzaghi. Durkin. the fact that maternal care was not inhibited confirmed that the neural network involved in olfactory recognition of the lamb differs from the one involved in the control of maternal responsiveness. identification of the neurochemical events occurring in the MOB to induce attraction towards AF. In particular.Developmental Psychobiology. it is not clear if the neurochemical processes are the same in the two processes. the establishment of an enduring bond has to occur during this sensitive period). This effect was due to the blockade of the olfactory memory per se and not to effects on the display of rejection behavior itself or disturbance of olfactory perception. & Kendrick. Targets of estrogen and VCS for the activation of maternal responsiveness appear to be mainly hypothalamic structures sensitive to estrogen and OT (MPOA. one within the other. Estrogen and VCS induce a temporary state of maternal responsiveness that lasts for several hours. frontal cortices). Meurisse.1002/dev Maternal Bonding in Sheep and Goats 65 partum) leads to an enhanced activation of frontal and orbitofrontal cortices (Keller et al. & Bontempi. OFC. their neural targets are different. Shaded structures: evidence of involvement includes Fos activation and lesion or inactivation studies. which receive olfactory input from the olfactory bulbs. MOB.. BNST. Regarding the nature of the sensitive period. At the same FIGURE 6 Neuronal network involved in the establishment of maternal selectivity in the ewe. & Destrade. or the sensitive period is only related to maternal responsiveness. Jaffard. While during lamb memory formation. frontal medial cortex. During the early stages of memory consolidation. entorhinal cortex. Keverne. and PVN).. & Levy.e. However. orbitofrontal cortex. In contrast. & Kendrick. piriform cortex. estrogen priming. Keverne. MeA. 1996. Infusion of lidocaine in both nuclei prevented mothers from learning the identity of their own lamb and to establish maternal selectivity. 2004a. main olfactory bulb. 2005. Frankland & Bontempi. two possibilities have been generally considered so far. it appears that only few brain structures are engaged in retrieval of lamb memory once consolidated. the evidence from the literature reviewed here indicates that while the physiological factors responsible for responsiveness and selectivity are the same. an alternative explanation for the apparent intermingling between the sensitive period on the one hand and responsiveness and selectivity on the other. Thus. extensive immediately early genes activation was found throughout the olfactory processing network. and VCS induced by expulsion of the fetus. infusing tetracaine in the medial frontal cortex inhibits the aggressive rejection behavior directed to alien lambs (Broad. Nonshaded structures: evidence of involvement includes Fos activation only. 1999b). 2005.

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