FTP

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 lHopital 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 uid (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 identication 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. 2006 Wiley Periodicals, Inc. Dev Psychobiol 49: 5470, 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 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 inuence on our research. Therefore, it is a great pleasure and honor to write this review to acknowledge his esteemed contribution to the eld of maternal behavior. Sheep and goats offer a unique opportunity to study the mechanisms by which a mother establishes an exclusive
Developmental Psychobiology. DOI 10.1002/dev
Maternal Bonding in Sheep and Goats
55
FIGURE 1 Establishment of selective behavior after parturition in sheep and goats. Note the inuence of the age of the young on its acceptance. Selective nursing is dened as acceptance of the own lamb and rejection of alien lambs (Adapted from Bordi et al., 1994; Keller et al., 2003; Poindron et al., 1980; Romeyer et al., 1993a).
relationship with her young and thus to investigate how a selective emotional bond is formed in a mammal. Indeed, while the display of maternal responsiveness1 generally depends on physiological facilitation in laboratory species (e.g., rats, voles, rabbits; Bridges & Byrnes, 2000; Gonzalez-Mariscal & Poindron, 2002; Numan, Fleming, & Levy, 2006; Rosenblatt & Siegel, 1981; Rosenblatt et al., 1979), maternal care is rarely selective and mothers care for any young that is present in the nest. In contrast, in most domestic ungulateswith the exception of the swinemothers rapidly develop exclusive care of the neonate they have been familiarized with from parturition. Thus, parturient ewes and goats show an initial transitory period of maternal responsiveness controlled by physiological events related with parturition. At this time, mothers display a very strong but transient attraction for amniotic uid (AF) and accept any neonate that is presented to them (Levy, Poindron, & Le Neindre, 1983; Poindron, Le Neindre, Raksanyi, Trillat, & Orgeur, 1980; Smith, Van-Toller, & Boyes, 1966). But contrary to most mothers of altricial young, 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, while maternal selectivity refers to exclusive care for the young the mother has bonded to.
attached exclusively to their neonate(s) and reject, often with aggressive behavior, any alien young that attempts to suckle (Hersher et al., 1963a; Poindron & Le Neindre, 1980; Smith et al., 1966; Fig. 1). In addition to selective nursing, this exclusive care of the mother for her neonate is exhibited in several other ways. The withdrawal of the own young induces a high state of agitation in the dam, with increased locomotor activity and emission of numerous high-pitched bleats (sheep: Poindron, Caba, Gomora Arrati, Krehbiel, & Beyer, 1994; goat: Addae, Awotwi, Oppong-Anane, & Oddoye, 2000). Also, mothers display a preference for their own young in a two-choice test within 46 hr after parturition, even though nursing is prevented (Keller et al., 2003; Poindron, Gilling, Hernandez, Seran, & Terrazas, 2003a). Another feature of maternal care is that in both species, the maternal bond is not easily broken once it has been established and adoptions of alien young are quite difcult to perform. Spontaneous acceptance of lambs or kids have rarely been reported outside the period surrounding parturition (Hass, 1990), and adoption may necessitate 1 week or more of connement, forced nursing, and olfactory masking (Hersher, Richmond, & Moore, 1963b). Hence, maternal selectivity in domestic sheep and goats has been regarded as a possible example of
56
Poindron, Keller, and Levy
imprinting in adulthood (Gubernick, 1981), given that it appears to share some of the characteristics found in lial imprinting in birds (e.g., presence of a sensitive period and a rapid establishment of an individual preference to an attachment gure). However, whether the activation of maternal responsiveness and the establishment of maternal selectivity are a sole and unique process or two different events is unclear. Indeed, 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, while other focused on the study of individual recognition of the lamb, especially regarding the role of olfactory cues in this process. Consequently, the interrelations between the activation of maternal responsiveness and the establishment of maternal selectivity have been for some time the object of little attention. However, the progress of the last decade concerning the identication of the sensory cues and the brain mechanisms involved in the control of maternal behavior in sheep, allow us to propose now a more comprehensive picture of maternal selectivity, and how it relates to maternal responsiveness. In the present article, we review the relations between these two aspects of maternal behavior in sheep and goats, focusing on three main questions: 1. does the sensitive period concern only maternal responsiveness or also bonding? 2. 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. what are the connections between the physiological and neurobiological factors and the nervous networks controlling maternal responsiveness on one hand, and those involved in maternal selectivity on the other.
and goats, this means that the contact with the neonate at a particular period (presumably parturition), will result in lasting effects on the maternal behavior of the mother. 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, (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, and (3) deprivation of the neonate after some contact during the sensitive period, should be of little consequence on its acceptance when reunited with its dam. However, the results of exposure to, or privation of, the neonate during the sensitive period in sheep and goats may be interpreted in two ways: either in terms of maternal responsiveness (i.e., does the treatment allow the mother to remain responsive to any neonate?), or in terms of bonding (i.e., does the treatment allow the mother to bond to her neonate?). But before we examine this point, let us see rst what is the evidence that allows a distinction between these two aspects of maternal behavior. The rst evidence that there are, indeed, two different aspects of maternal care in sheep and goats comes from the fact that at the very time of parturition, mothers accept any young, especially neonates (Poindron & Le Neindre, 1980; Poindron et al., 1980; Smith et al., 1966), indicating that there is some state of responsiveness to cues common to any neonate. The distinction between maternal responsiveness and selectivity is further supported by the fact that ewes or goats, rendered anosmic before parturition by olfactory bulb ablation, or other methods of anosmia, are able to care for any young, without developing an individual bond with their own (Levy, Locatelli, Piketty, Tillet, & Poindron, 1995b; Morgan, Boundy, Arnold, & Lindsay, 1975; Poindron, 1976a; Romeyer, Poindron, & Orgeur, 1994a). The Sensitive Period and Maternal Responsiveness. High levels of maternal responsiveness, assessed in most studies by the display of maternal care with a short latency (<30 min), are seldom found outside the peripartum period. When females are left undisturbed to give birth, both ewes and does display maternal behavior within minutes following expulsion of the fetus, and even a few hours before parturition if other young are present (Arnold & Morgan, 1975). However, if the neonate is removed at birth, before the mother has had any contact with it, maternal responsiveness fades within a few hours in both species. In most cases, mothers are unable to display immediate maternal care when reunited with their young after 412 hr of separation (Hersher et al., 1963a; Klopfer et al., 1964; Lickliter, 1982; Poindron & Le Neindre, 1980). It is difcult to propose precise boundaries for the sensitive period, 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., 1963b; Klopfer, Adams, & Klopfer, 1964; Klopfer & Gamble, 1966; Klopfer & Klopfer, 1968; Smith et al., 1966). Nonetheless, it became rapidly obvious that these terms, derived from embryology and early studies of imprinting in young birds, were not fully appropriate for the study of maternal bonding. In the present review, we use the term of sensitive period, in the general sense proposed by Bateson (1979) that an individuals characteristics can be more strongly inuenced by a given event at one stage of development than at other stages. Referring to maternal behavior of sheep
57
have been tested vary between studies. Nonetheless, some results suggest that the sensitive period may be shorter in goats than in sheep (Ramrez, Quiles, Hevia, Sotillo, & Ramrez, 1996). Also, parity may inuence this duration (Lickliter, 1982). In any case, 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. 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. Although this cannot be totally ruled out (see below for further discussion of this point), there are several facts indicating that the fading of maternal behavior in mothers deprived of young at parturition is related to maternal responsiveness. If selectivity was necessary for the postpartum maintenance of maternal behavior, ewes, or goats that are anosmic at parturition would not be able to remain maternal, contrary to what is observed (Hernandez, Seran, Vazquez, Delgadillo, & Poindron, 2001; Klopfer & Gamble, 1966). 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, 1980; Fig. 2). Furthermore, after 12 hr of separation from birth, the percentage of mothers that accept a lamb tends to be higher for alien neonates than for the 12-hr-old own lamb, showing that ewes at this time are still more responsive to
neonates than to the individual characteristics of a given lamb (Poindron et al., 1980; Fig 2). Also, the effects of deprivation of the neonate on maternal responsiveness should differ, depending on the time at which the separation occurs, to be sure that they result from the existence of a sensitive period. 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, but to the time at which this separation is applied. For example in sheep, 24 hr of separation from the lamb have no major detrimental effect on maternal behavior in ewes which had 2448 hr of contact before the separation (Fig. 2; Keller, Meurisse, & Levy, 2005; Levy et al., 1991; Poindron & Le Neindre, 1980). Even a few minutes of contact at birth are sufcient for does to maintain maternal responsiveness for 23 hr without their neonate (Gubernick, 1981; Klopfer et al., 1964). Thus, 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.
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. 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, when separation is performed either at birth or after an initial contact of 24 hr. Note that maternal responsiveness fades in a similar fashion in intact and anosmic mothers. Note also the better acceptance of a newborn alien after 12 hr of separation (Adapted from Levy et al., 1991; Poindron & Le Neindre, 1980; Poindron et al., 1980).
58
this point specically. Nonetheless, 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, 1980). After 812 hr of total separation, the proportion of ewes becoming selective after 15 min of contact with their own young (Poindron, 1981), was intermediate between that found for ewes tested either at birth (21%) or after 30 min of contact (61%; Fig. 1), suggesting that the rapidity of establishment of selectivity may not differ fundamentally at birth or 812 hr later. These results would rather support the hypothesis that the rapidity of bonding may not be strongly inuenced by the moment of the sensitive period at which olfactory experience is obtained. However, contradictory results have been obtained in another study investigating the consequences of delaying contact with the neonate (Alexander et al., 1986). 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. While delaying contact did not impair the display of maternal care towards their own lamb, 64% of ewes deprived of their lamb during the rst hour had failed to develop maternal selectivity at 12 hr, versus 9% for ewes in contact with their lamb from birth. These results would rather indicate that the rst hour postpartum is critical for the establishment of selectivity, but it cannot be excluded that they are partly due to exogenous administration of estrogens, which were used in this study (Alexander et al., 1986). Whether reacceptance of the ewes 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, since maternal olfaction plays a major role in selective nursing (see next section). If the establishment of selectivity during the sensitive period is important for the later display of maternal acceptance, anosmia performed during this separation period should impair acceptance of the mothers own young. Only one study has investigated this in the postparturient goat (Klopfer & Gamble, 1966) in a small number of animals, resulting in the rejection of the kid by four does out of seven. Further information can be obtained from studies of anosmia or olfactory cues deprivation several weeks postpartum (Alexander, Stevens, & Bradley, 1983; Poindron & Le Neindre, 1980). Regardless of the method of olfactory deprivation, about half of mothers show some impairment of maternal acceptance of their own young. Thus, once established, the recognition of the lamb by its dam would become an important factor controlling maternal responsiveness. While the onset of the sensitive period certainly reects the onset of maternal responsiveness towards any lamb (therefore independent of maternal attachment), the maintenance of maternal behavior
beyond its initial limits of about 24 hr may well depend on the establishment of selectivity. This is further supported by the fact that when a mother-young separation of 36 hr is performed at 4 hr postpartum, dissociation between maternal responsiveness and selectivity is easily obtained (most mothers are not selective, while they are still maternal), whereas after 7 days of contact, such a dissociation is not found: following a 36 hr separation mothers are either maternal and selective, or not maternal at all (Keller et al., 2005).
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, to a neurosensory control by sensory cues from the young (Poindron & Le Neindre, 1980; Rosenblatt et al., 1979). Hence, 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.
Cues Involved in the Maintenance of Maternal Responsiveness

Evidence from Partial Separation Studies. The effects of deprivation of specic sensory cues during the sensitive period underline that maternal olfaction plays a major role in the maintenance of maternal responsiveness. Thus in the sheep, mothers that cannot smell their lamb during the rst 8 hr postpartum do not maintain maternal responsiveness better than mothers totally isolated from their neonate, regardless of whether they can see them or not (Poindron & Le Neindre, 1980). In contrast, suppression of visual cues does not impede the ability of ewes to remain maternal (Fig. 3; Poindron, Levy, & Krehbiel, 1988). Also, preventing physical contact and thus suppressing the sensory cues provided by licking and suckling, does not impair the maintenance of maternal responsiveness in the ewe, even following 12 hr of treatment (Poindron & Le Neindre, 1980). In the goat however, 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 signicant proportion of mothers (Fig. 4; Bordi et al., 1994; Romeyer et al., 1993a), while no effect is observed in sheep after 12 hr in the same conditions, as long as AF is not removed from the lambs coat (Alexander et al., 1986).
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. Selectivity concerns only mothers that had retained maternal responsiveness (i.e., that accepted their own lamb). Note the importance of olfaction for the maintenance of maternal responsiveness. Note also the facilitation of maternal selectivity in mothers that can see their lamb (Sight Hearing group vs. Olfaction Hearing group; adapted from Poindron & Le Neindre, 1980 and Poindron et al., 1988).
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. For denition of selectivity see Figures 2 and 3. Duration of treatment: in sheep, 12 hr; in goats, 4 hr. Preventing licking and suckling seems to induce more disturbances of maternal responsiveness and selectivity in goats than in sheep (Adapted from Poindron & Le Neindre, 1980 for sheep and from Romeyer et al., 1993a and Bordi et al., 1994 for goats).
60
It is not known whether this detrimental effect results from the privation of the somatosensory cues provided by nursing, or from an impairment of olfactory perception due to licking privation (Romeyer et al., 1993a), or both. If an effect of licking privation was conrmed, it could then suggest some role of the vomeronasal system in the regulation of maternal responsiveness in the goat, as already reported in the rat (Numan et al., 2006). One major source of olfactory stimulation that facilitates the display of maternal behavior at parturition is the AF which bathes the neonate. Ewes undergo a dramatic change of behavior towards AF at the very moment of parturition. AF is strongly repulsive for ewes at any stage of their reproductive cycle, except during a few hours around parturition when they become strongly attracted to it, and this phenomenon is olfactory dependent (Levy et al., 1983). The initial attraction for AF does not depend on the identity of the giver, but is somewhat specic to the own species (Arnould, Piketty, & Levy, 1991). Interestingly, in mothers deprived of their lamb immediately after parturition, the fading of maternal responsiveness parallels that found for AF attraction, suggesting that the two phenomena are closely associated. In fact, maternal acceptance after parturition is facilitated by AF. For example, primiparous parturient ewes are unable to develop an appropriate maternal behavior if AF has been removed from their lambs coat, and in multiparous mothers licking behavior is strongly impaired (Levy & Poindron, 1987). Conversely, smothering 12-hrold alien lambs (whose coat is dry) with AF facilitates their acceptance by parturient mothers (Levy & Poindron, 1984). Also, parturient ewes accept more readily an alien newborn, whose coat is fully wet with AF, than a 12-hr-old alien which coat is already dry. 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., 1980). Another way to investigate the role of maternal olfaction during the sensitive period is to study the effects of prepartum anosmia. Contrary to the privation of olfactory cues in intact mothers, 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. Ewes and goats rendered anosmic before parturition by lesion of the main olfactory epithelium, do care for their neonates and nurse young adequately (Hernandez et al., 2001, 2002; Levy et al., 1995b; Romeyer et al., 1994a). This is also the case following ablation of the olfactory bulbs, even though bulbectomy may slightly facilitate maternal aggression toward the young in sheep (Baldwin & Shillito, 1974; Bouissou, 1968; Poindron, 1976b). In agreement with the effects of AF privation in intact ewes (Levy &
Poindron, 1987), prepartum anosmia also impairs the display of maternal behavior in primiparous ewes (Levy et al., 1995b). However, the effects are less pronounced and do not impede the mothers to display maternal behavior, contrary to what is found after removing AF from the lambs coat in intact dams. So far, no evidence has been found for a specic inuence of the accessory olfactory system on maternal responsiveness following lesion of the vomeronasal organ (Levy et al., 1995b). As a whole, 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. In contrast, such a process does not take place when the olfactory system is intact. Therefore, the effects of anosmia on maternal responsiveness probably do not reect the actual role of this sensory channel in intact mothers. It is more adequate to rely on results of olfactory cues manipulation in intact mothers for studying the role of maternal olfaction. Nonetheless, this does not apply when studying olfactory recognition of the neonate.
Sensory Cues Involved in the Establishment of Maternal Selectivity

The Effects of Prepartum Anosmia. Ewes and does learn to discriminate their own neonate from an alien one very rapidly after parturition. The reported period of contact necessary to do so varies between studies, depending on the experimental procedures used, but 30 min of contact appears sufcient to allow the display of maternal selectivity in more than half of mothers in sheep and goats (Keller et al., 2003; Klopfer et al., 1964; Poindron & Le Neindre, 1980; Smith et al., 1966), and absence of selectivity later than 4 hr postpartum is rare (Keller et al., 2003; Romeyer & Poindron, 1992; Romeyer, Poindron, Porter, Levy, & Orgeur, 1994b). Evidence for the importance of olfaction in the recognition of the young comes from experiments of olfactory bulbs ablation (Baldwin & Shillito, 1974; Bouissou, 1968), section of the main olfactory nerves (Morgan et al., 1975), and peripherally induced anosmia, all these methods preventing the establishment of selective nursing (goat: Hernandez et al., 2002; Klopfer & Gamble, 1966; Romeyer et al., 1994a; sheep: Levy et al., 1995b; Poindron & Le Neindre, 1980; Hernandez et al., 2001). 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, contrary to what occurs for maternal responsiveness. Another issue is determining whether olfactory recognition of the young depends on the main or on the
61
accessory olfactory system. It is unlikely that the effects of peripheral anosmia could be due to the lesion extending to the vomeronasal organ (Cohen-Tannoudji, Lavenet, Locatelli, Tillet, & Signoret, 1989; Levy et al., 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). However, 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, 2000). 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., 2003b). Nonetheless, given the role often played by the accessory system in several social recognition processes in mammals (Johnston, 1998; Keverne, Martel, & Nevison, 1996), the vomeronasal system cannot unequivocally be excluded from participating in the establishment of maternal selectivity. 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), this would nonetheless be consistent with the effects of licking or AF deprivation on the rapidity of establishment of selectivity (see next paragraph). The Nature of the Olfactory Cues Involved in Individual Recognition. The exact nature of the cues responsible for the individual olfactory signature of lambs and kids is yet to be identied. It is well established that these cues are not effective at distances greater than 25 cm (Alexander, 1978; Alexander & Shillito, 1977; Poindron et al., 2003a), suggesting that they are either little volatile and/or present at very low concentrations. Various experiments have demonstrated that they are olfactory signatures unique to each young, even in the case of dizygotic twins (Porter et al., 1991; Romeyer et al., 1993a). Monozygotic twins, however, share much closer signatures, indicating some genotypic basis of olfactory identity (Romeyer et al., 1993b). Transmission of odors from the dam to the neonate, known as maternal labeling (Alexander, Stevens, & Bradley, 1989; Gubernick, 1981), is not critical for the initial establishment of maternal selectivity (Alexander et al., 1986; Poindron et al., 1988; Romeyer et al., 1993a). Nonetheless, it can contribute to the development of odor differences between neonates, for example, in young with initially very similar signatures (e.g., monozygotic twins; Romeyer et al., 1993b). Thus, within a short time after its birth, 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 inuences (Levy, Kendrick, Keverne, Porter, & Romeyer, 1996; Porter, Levy, Nowak, Orgeur, & Schaal, 1994). AF could also participate in the initial olfactory signature of the neonate. 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, 1984). Furthermore, presence of AF on the lambs coat tends to facilitate bonding in mothers deprived of licking (Alexander et al., 1986). 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., 1980 and 24% in that of Keller et al., 2003). Mothers may have already gained some information about the olfactory identity of their lamb at its birth, due to prepartum ingestion of AF. Therefore, AF plays a dual role in the establishment of maternal behavior, facilitating both the immediate acceptance of the newborn, and the establishment of its recognition.
Possible Synergy with Other Sensory Channels. While numerous studies demonstrate that maternal olfaction is an absolute requisite for the establishment of maternal selectivity, little attention has been paid to the possibility that other sensory modalities may contribute to this process as well. The effects of partial sensory deprivation during the sensitive period on maternal selectivity provide evidence supporting this possibility, at least in sheep. It is true that mothers close to their lamb do establish selective behavior, even if physical contact is prevented (Fig. 4). However, if olfactory perception is somewhat limited, 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., 1988), then visual cues have a facilitating inuence on the establishment of maternal selectivity (Fig. 3). This is in agreement also with the fact that marked differences in visual aspect of the lamb may inuence its acceptance at the udder (Alexander & Shillito, 1978), even in anosmic mothers (Poindron, 1976a). In goats, only the effects of physical contact deprivation have been studied, and the results suggest that physical contact may be more important than in sheep. Absence of physical contact with the neonate seems to delay bonding, possibly because of some reinforcing inuence of suckling and/or of vomeronasal input gained from licking (Bordi et al., 1994; Romeyer et al., 1993a). In both species further studies would be necessary to investigate the possibility that other sensory channels (e.g., sight or hearing) could facilitate the formation of the bond. This is especially relevant since recent studies indicate that early recognition of the neonate by visual
62
and/or acoustic cues is also present very rapidly after parturition. Indeed, despite the major importance of maternal olfaction, mother sheep and goats are also able to discriminate their young on the basis of other sensory cues. Thus, in a two-choice test excluding the use of olfactory cues, intact ewes and goats do show a preference for their young at 6 and 4 hr, respectively (Keller et al., 2003; Poindron et al., 2003a). Preference for the neonate on the rst day postpartum has also been found in mothers rendered anosmic before parturition (Ferreira et al., 2000; Poindron et al., 2003a). 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 46 hr postpartum. Also, the respective roles of vision and hearing at this early stage have not been claried, 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, respectively (goats: Terrazas, Seran, Her` nandez, Nowak, & Poindron, 2003; sheep: F. Sebe, personal communication).
in the goat about the factors responsible for the induction of the sensitive period. On the one hand, attempts to induce maternal behavior with sexual steroid treatments have been unsuccessful (Rosenblatt & Siegel, 1981). On the other hand, expulsion of the fetus is likely to be involved, since peridural anesthesia at parturition impairs the display of maternal behavior, even though the effects are much less marked than in the sheep (Poindron et al., 1998). Neural Structures and Neurochemical Processes Involved in Maternal Responsiveness. 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. In one study, brain activations resulting from normal motheryoung interactions were compared with those found in females receiving a treatment to induce maternal receptivity but prevented from displaying maternal care (Da Costa, Broad, & Kendrick, 1997). In another study, these brain activations were measured in mothers rendered anosmic before parturition, which allows the display of maternal responsiveness but prevents the establishment of bonding (Keller, Meurisse, & Levy, 2004a). Both studies revealed that the induction of maternal responsiveness involves extensive neural circuitry in the brain including various limbic and hypothalamic areas. Indeed, the pattern of gene expression observed between ewes displaying maternal behavior (i.e., maternally responsive and selective) and ewes receiving VCS or rendered anosmic before parturition (i.e., maternally responsive, but not selective), were remarkably similar in the medial preoptic area (MPOA), the bed nucleus of the stria terminalis (BNST), and the paraventricular nucleus of the hypothalamus (PVN). Thus, 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, 2003 and Numan et al., 2006). The functional involvement of these structures was explored using various pharmacological approaches. The effects of MPOA and BNST inactivation were investigated in primiparous ewes, by infusing an anesthetic before parturition and during the rst 2 hr postpartum (Levy, Ferreira, Keller, Meurisse, & Perrin, 2005). MPOA inactivation impairs maternal responsiveness whereas inactivation of BNST or infusion of articial cerebrospinal uid do not. However, when interest for the lamb is challenged by taking the young away and by allowing the mother to join it, behavioral impairments are observed both after BNSTor MPOA inactivation, indicating that the BNST is also involved soon after parturition. 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, 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.
Maternal Responsiveness
Hormonal and Proprioceptive Factors Controlling Maternal Responsiveness. Activation of maternal behavior in the ewe depends mainly on two factors, which act in synergy: the prepartum production of estrogen by the placenta and the vaginocervical stimulation (VCS) caused by the expulsion of the fetus. Taken separately, these two factors are hardly effective and only their association induces a rapid display of maternal care (Kendrick & Keverne, 1991; Keverne, Levy, Poindron, & Lindsay, 1983; Poindron et al., 1988). Therefore, the existence of a sensitive period of maternal receptivity is the result of the action of these two factors. Its duration also depends on the time during which these two factors are present. Thus, the length of the sensitive period can be increased by exogenous estradiol treatment (Poindron & Le Neindre, 1980). In addition, attraction for AF, which fades rapidly after parturition, can be reinstated by VCS up to 8 hr postpartum (Poindron et al., 1988). So far, little is known
63
impair some aspects of maternal behavior in parturient ewes (Da Costa, De La Riva, Guevara-Guzman, & Kendrick, 1999). The main action of VCS in the brain is to induce a release of oxytocin (OT) that stimulates maternal respon siveness (Kendrick et al., 1997a; Levy et al., 1996; Numan et al., 2006). Release of OT at birth and/or in response to VCS occurs primarily in the PVN, which is the main source of OT release in the brain. Indeed, in vivo microdialysis revealed that OT is released in the PVN at lambing as well as during articial VCS. Furthermore, retrodialysis infusion of OT stimulates maternal behavior in nonpregnant animals primed with a steroid treatment (Da Costa, Guevara-Guzman, Ohkura, Goode, & Kendrick, 1996). However, OT release also occurs in the BNST, MPOA, and the olfactory bulb during parturition and/or following VCS (Da Costa et al., 1996; Kendrick, Keverne, Hinton, & Goode, 1992a). Hence, OT may also stimulate maternal receptivity by facilitating release of various neurotransmitters within these structures and other neural substrates specically involved in its control (Kendrick et al., 1997a). For example, infusions of OT by retrodialysis at doses that inuence components of maternal behavior can increase noradrenalin (NA) release in the olfactory bulb, MPOA, and PVN, or GABA release in the MPOA and olfactory bulb (Da Costa et al., 1996; Kendrick, Levy, & Keverne, 1992b; Levy, Kendrick, Goode, Guevara-Guzman, & Keverne, 1995a). Various studies indicate that estradiol facilitates the priming of the oxytocinergic system, which in turn facilitates maternal responsiveness at parturition. Indeed, 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, Kendrick, Sirinathsinghji, & Keverne,
1993; Broad et al., 1999a; Meurisse et al., 2005a). This could in turn result in an easier display of maternal behavior at parturition. As a whole, 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, while the MOB is tuned to respond optimally to the cues from the neonate to ensure the immediate display of maternal care (Fig. 5).
Maternal Recognition and Selectivity

Peripheral Factors Involved in the Establishment of Maternal Selectivity. In sheep as well as in goats, expulsion of the fetus facilitates the formation of the maternal bond. Also, VCS performed after the establishment of maternal selectivity allows mothers to form a new bond with an alien newborn (sheep: Kendrick, Levy, & Keverne, 1991; goat: Romeyer et al., 1994b). In other words, VCS has specic effects that promote learning of the olfactory identity of the neonate. Whether estrogen may inuence maternal selectivity remains an open question. Some results in sheep suggest that they may modulate the establishment of bonding (Alexander et al., 1986, 1989) or allow bonding in the absence of VCS (Le Neindre et al., 1979). However, in studies of the sensitive period in which ewes were induced to lamb using high doses of estradiol, we found no evidence for an effect of estradiol on selectivity (Poindron & Le Neindre, 1980). More studies are needed to assess whether estrogen may play some role in olfactory recognition of the lamb, as demonstrated in other types of social memory (Choleris et al., 2003; SanchezAndrade, James, & Kendrick, 2005). In any case, and contrary to what is found for VCS, 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. MOB, main olfactory bulb; MOPA, medial preoptic area; PVN, paraventricular nucleus of the hypothalamus; BNST, bed nucleus of the stria terminalis.
64
induce the acceptance of another lamb (Alexander et al., 1989). Neural Structures and Neurochemical Processes Involved in the Establishment of Maternal Selectivity. As described in Section Sensory Cues at Play During the Sensitive Period for the Establishment of Maternal Responsiveness and Selectivity, early recognition of the newborn lamb or kid, and establishment of selectivity depend on the sense of olfaction. In the sheep, 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. Electrophysiological recordings from olfactory bulb mitral cells showed that these cells respond preferentially to lambs odors after birth. In addition, a proportion of the cells respond preferentially to the odor of the ewes own lamb, supporting the idea that a coding for odor familiarity takes place at the rst relay of the olfactory information (Kendrick et al., 1992b). These electrophysiological changes are reected in concurrent changes in the release of peptides (GABA and Glutamate), and of NA and acetylcholine (ACh) in the MOB (Kendrick et al., 1997b, 1992b; Kendrick, Keverne, Chapman, & Baldwin, 1988a,b; Levy, Guevara-Guzman, Hinton, Kendrick, & Keverne, 1993; Levy et al., 1995a). Using pharmacological tools, these neurochemical releases were shown to be involved in the olfactory learning leading to individual lamb recognition (Ferreira, Meurisse, Gervais, Ravel, & Levy, 2001; Kendrick et al., 1997a; Levy, Gervais, Kindermann, Orgeur, vy, Richard, Meurisse, & Ravel, 1997; & Piketty, 1990; Le Pissonnier, Thiery, Fabre-Nys, Poindron, & Keverne, 1985). OT release that occurs in the MOB at parturition further enhances NA and ACh activation (Levy et al., 1993, 1995a). Therefore, OT is also likely to play some role in the bonding process (Kendrick, 2000), 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. There are indications that the interactions between OT, NA, and ACh that take place in the MOB in the rst hours postpartum are not related only to olfactory recognition memory. The increase of neurotransmitter release is modulated by maternal experience (Levy et al., 1993, 1995a). 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, 1994), recent results indicate that in fact primiparous ewes are as fast as experienced mothers to develop maternal selectivity (Keller et al., 2003). Therefore, these neurobiological differences concern probably other aspects of maternal behavior. They may be related with the more frequent display of maternal disturbances found in primiparous mothers (Dwyer & Lawrence, 2000;
Poindron, Raksanyi, Orgeur, & Le Neindre, 1984), the lack of response to VCS in nonpregnant nulliparous ewes (Kendrick & Keverne, 1991) or the inability of inexperienced mothers to compensate for the privation of AF olfactory cues or VCS (Levy & Poindron, 1987; Poindron & Levy, 1990). A possible contribution of the accessory olfactory system in the olfactory recognition of the young remains an open question, since perception of volatile compounds by the VNO has been demonstrated, at least in rodents (Johnston, 1998; Leinders-Zufall et al., 2000; Trinh & Storm, 2003). In a recent experiment, 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, but also in the anatomically distinct AOB (Keller, 2003). 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., 1989; Levy et al., 1995b). In this context, several nonexclusive explanations can account for this effect. It is possible that the reduction of licking behavior in anosmic ewes (Levy et al., 1995b) results in a lower stimulation of the VNO sensory neurons by AF and lamb odors. 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). Indeed, in the sheep both MOB and AOB send projections to the cortical nucleus of the amygdala (Jansen, Iwamoto, & Jackson, 1998; Meurisse, Perrin, Keller, & Levy, 2005b). Thus it is likely that lesion of the MOB also results in a lower activation of the accessory olfactory network. Centrifugal projections from the cortical nucleus to the AOB could be responsible for this effect (Pitkanen, 2000). Additional olfactory structures, other than the MOB, also play an important role in the establishment and display of maternal selectivity, as illustrated in Figure 6. Immediate early gene expression related to the learning of the lamb odor increases in secondary (piriform cortex, medial, and cortical nuclei of the amygdala) and tertiary (orbitofrontal and frontal medial cortex, entorhinal cortex) olfactory processing regions. 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., 1997; Keller et al., 2004a). The functional involvement of these structures has been addressed by studying the effects of their reversible blockade. While inactivation of the piriform cortex has no effect on the establishment of maternal selectivity (Broad,
65
partum) leads to an enhanced activation of frontal and orbitofrontal cortices (Keller et al., 2004a,b, 2005; Sanchez-Andrade et al., 2005). Thus, consolidation processes induce time-dependent reorganization in the network engaged in lamb recognition. The functional signicance of this enhanced activation remains to be explored.
CONCLUSIONS AND PERSPECTIVES

This review underlines that in domestic sheep and goats, maternal responsiveness and maternal selectivity are two intermingled processes that lead to maternal attachment. These two components are synchronized since maternal receptivity is present at parturition and bonding starts as soon as contact with the neonate occurs. They also share immediate triggering factors, estrogen priming, and VCS induced by expulsion of the fetus. However, the neural mechanisms that control maternal responsiveness and selectivity differ in various aspects. While the olfactory system is involved in the display of maternal responsiveness as well as in the establishment of selectivity, it is not clear if the neurochemical processes are the same in the two processes. In particular, identication of the neurochemical events occurring in the MOB to induce attraction towards AF, would be necessary to clarify this point. Furthermore, the more central structures involved in maternal responsiveness and in selectivity are clearly different. Targets of estrogen and VCS for the activation of maternal responsiveness appear to be mainly hypothalamic structures sensitive to estrogen and OT (MPOA, BNST, and PVN). In contrast, the structures responsible for olfactory recognition memory are rather limbic and cortical (medial and cortical amygdala, frontal cortices). Regarding the nature of the sensitive period, two possibilities have been generally considered so far. 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.e., the establishment of an enduring bond has to occur during this sensitive period), or the sensitive period is only related to maternal responsiveness. However, the evidence from the literature reviewed here indicates that while the physiological factors responsible for responsiveness and selectivity are the same, their neural targets are different, as are probably also some of the neurobiological processes activated. Thus, an alternative explanation for the apparent intermingling between the sensitive period on the one hand and responsiveness and selectivity on the other, may be the existence of two sensitive periods, one within the other. Estrogen and VCS induce a temporary state of maternal responsiveness that lasts for several hours, and interacting with the neonate allows its consolidation. At the same
FIGURE 6 Neuronal network involved in the establishment of maternal selectivity in the ewe. CoA, cortical amygdala; EC, entorhinal cortex; FMC, frontal medial cortex; MeA, medial amygdala; MOB, main olfactory bulb; OFC, orbitofrontal cortex; PC, piriform cortex. Shaded structures: evidence of involvement includes Fos activation and lesion or inactivation studies. Nonshaded structures: evidence of involvement includes Fos activation only.
Hinton, Keverne, Da Costa, & Kendrick, 1999b), infusing tetracaine in the medial frontal cortex inhibits the aggressive rejection behavior directed to alien lambs (Broad, Hinton, Keverne, & Kendrick, 2002). A more preeminent role for the medial and the cortical nuclei of the amygdala, which receive olfactory input from the olfactory bulbs, has been recently demonstrated (Keller, Perrin, Meurisse, Ferreira, & Levy, 2004b). Infusion of lidocaine in both nuclei prevented mothers from learning the identity of their own lamb and to establish maternal selectivity. 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. Moreover, the fact that maternal care was not inhibited conrmed that the neural network involved in olfactory recognition of the lamb differs from the one involved in the control of maternal responsiveness. It has been shown that across consolidation processes, retrieval of memories involves time-dependent participation of a set of cerebral regions (Bontempi, Jaffard, & Destrade, 1996; Frankland & Bontempi, 2005; Maviel, Durkin, Menzaghi, & Bontempi, 2004). While during lamb memory formation, extensive immediately early genes activation was found throughout the olfactory processing network, it appears that only few brain structures are engaged in retrieval of lamb memory once consolidated. During the early stages of memory consolidation, piriform and entorhinal cortices show signicant expression of activation markers, while retrieval of more consolidated memory (7 days post-
66
time, VCS would also tune the olfactory system and related structures for the rapid olfactory learning of the neonates identity, which takes place in less than 2 hr. This tuning is also temporary, since attachment to another young is impossible once the mother has learned the identity of her offspring, unless reactivation by another birth process occurs, as in the case of twin-bearing mothers. Finally, the bond keeps consolidating after its initial formation, since transitory mother-young separation after parturition has less consequence on both maternal responsiveness and maternal selectivity at 1 week postpartum than at 24 hr. Furthermore, it seems that it is only at about 7 days that the two components are totally indissociable and that maternal nursing can hardly be displayed independently from the recognition of the offspring. Several questions still need studying to fully understand how maternal responsiveness and selectivity interact in the control of maternal care display, especially once the initial inuence of parturition has faded. The nature of the learning and the neurobiological processes allowing the consolidation of maternal responsiveness has not been studied. It would be worthy to investigate whether the mechanisms involved in the consolidation of maternal responsiveness per se are similar to those identied for maternal memory in species that do not develop selective care (e.g., the rat; Levy & Fleming, 2006). Also, the apparent tuning of the maternal olfactory function for nonindividual cues from AF on the one hand, together with specic receptivity for individual cues on the other, could suggest the existence of some predisposition process, somewhat similar to that reported in lial imprinting (Bolhuis, 1991, 1999; Horn & McCabe, 1984). Compound stimuli may facilitate consolidation of both maternal responsiveness and olfactory memory. Identifying the nature of the chemosensory cues involved in AF attraction and in olfactory recognition of the neonate are necessary to clarify this point. Finally, while the neurobiological aspects of olfactory memory formation and recall have been the object of various studies (Brennan & Keverne, 1997; Keller et al., 2004a,b, 2005; Kendrick, 2000; Levy & Fleming, 2006; SanchezAndrade et al., 2005), it is not clear whether they depend on the learning of the olfactory cues by mere exposure or if they result from an associative learning involving some other unconditioned stimulus. Investigating a possible synergy between olfaction and other sensory modalities in the formation and consolidation of olfactory memory would allow to identify sensory cues possibly involved in this associative process. Indeed, mothers are highly responsive to visual and acoustic cues from neonates. Moreover, the existence of an early visual and/or auditory recognition of the neonate raises the possibility that the sensitive period is not limited to the olfactory system.
While it is clear that the factors stimulating maternal responsiveness at parturition also result in the newborn becoming highly attractive and rewarding, the exact neurobiological mechanisms controlling this rewarding value of the neonate have not been identied. Opiates, which are commonly involved in social rewarding systems (Keverne, 1992; Panksepp, Nelson, & Bekkedal, 1997) seem to play only a secondary role in the case of maternal behavior in sheep (Caba et al., 1995; Kendrick & Keverne, 1989; Keverne & Kendrick, 1991). The dopamine projections to the nucleus accumbens, a wellknown system involved in reinforcement and social bonding (Curtis & Wang, 2005; Young, Lim, Gingrich, & Insel, 2001), could also participate in the rewarding value of the young. Furthermore, OT release could facilitate dopamine release in this nucleus. Similarly, the mechanisms by which the affective value of the mother for any neonate become limited to the offspring she has learned to recognize are yet to be identied. Pharmacological investigations of the factors controlling maternal responses in separation-reunion paradigms after bonding is established, will bring valuable information in this regard.
REFERENCES
Addae, P. C., Awotwi, E. K., Oppong-Anane, K., & Oddoye, E. O. K. (2000). Behavioural interactions between West African dwarf nanny goats and their single-born kids during the rst 48 hours post-partum. Applied Animal Behaviour Science, 67, 7788. Alexander, G. (1978). Odour, and the recognition of lambs by Merino ewes. Applied Animal Ethology, 4, 153158. Alexander, G., Poindron, P., Le Neindre, P., Stevens, D., Levy, F., & Bradley, L. (1986). Importance of the rst hour postpartum for exclusive maternal bonding in sheep. Applied Animal Behaviour Science, 16, 295300. Alexander, G., & Shillito, E. E. (1977). The importance of odour, appearance and voice in maternal recognition of the young in Merino sheep (Ovis aries). Applied Animal Ethology, 3, 127135. Alexander, G., & Shillito, E. E. (1978). Maternal responses in merino ewes to articially coloured lambs. Applied Animal Ethology, 4, 141152. Alexander, G., Stevens, D., & Bradley, L. R. (1983). Washing lambs and connement as aids to fostering. Applied Animal Ethology, 10, 251261. Alexander, G., Stevens, D., & Bradley, L. R. (1989). Maternal acceptance of alien lambs in ewes treated and untreated with oestrogen at birth. Australian Journal of Experimental Agriculture, 29, 173178. Arnold, G. W., & Morgan, P. D. (1975). Behaviour of the ewe and lamb at lambing and its relationship to lamb mortality. Applied Animal Ethology, 2, 2546.
Developmental Psychobiology. DOI 10.1002/dev Arnould, C., Piketty, V., & Levy, F. (1991). Behaviour of ewes at parturition toward amniotic uids from sheep, cows and goats. Applied Animal Behaviour Science, 32, 191196. Baldwin, B. A., & Shillito, E. E. (1974). The effects of ablation of the olfactory bulbs on parturition and maternal behaviour in Soay sheep. Animal Behaviour, 22, 220223. Bateson, P. P. G. (1979). How do sensitive periods arise and what are they for? Animal Behaviour, 27, 470486. Bolhuis, J. J. (1991). Mechanisms of avian imprinting: A review. Biological Reviews, 66, 303345. Bolhuis, J. J. (1999). Early learning and the development of lial preferences in the chick. Behavioural Brain Research, 98, 245252. Bontempi, B., Jaffard, R., & Destrade, C. (1996). Differential temporal evolution of post-training changes in regional brain glucose metabolism induced by repeated spatial discrimination training in mice: Visualization of the memory consolidation process? European Journal of Neuroscience, 8, 23482360. Booth, K. K., & Katz, L. S. (2000). Role of the vomeronasal organ in neonatal offspring recognition in sheep. Biology of Reproduction, 63, 953958. Bordi, A., De Rosa, G., Napolitano, F., Litterio, M., Marino, V., & Rubino, R. (1994). Postpartum development of the mother-young relationship in goats. Applied Animal Behaviour Science, 42, 145152. Bouissou, M. F. (1968). Effet de lablation des bulbes olfactifs ` sur la reconnaissance du jeune par sa mere chez les Ovins. Revue de Comportement Animal, 2, 7783. Brennan, P. A., & Keverne, E. B. (1997). Neural mechanisms of mammalian olfactory learning. Progress in Neurobiology, 51, 457481. Bridges, R. S., & Byrnes, E. M. (2000). Neuroendocrine regulation of maternal behavior. In P. M. Conn & M. E. Freeman (Eds.), Neuroendocrinology in physiology and medicine (pp. 301315). Totowa, USA: Humana Press. Broad, K. D., Hinton, M. R., Keverne, E. B., Da Costa, A. P. C., & Kendrick, K. M. (1999b). The role of the piriform cortex in olfactory memory formation. Society for Neuroscience Abstract, 25, 662.665. Broad, K. D., Hinton, M. R., Keverne, E. B., & Kendrick, K. M. (2002). Involvement of the medial prefrontal cortex in mediating behavioural responses to odour cues rather than olfactory recognition memory. Neuroscience, 114, 715729. Broad, K. D., Kendrick, K. M., Sirinathsinghji, D. J., & Keverne, E. B. (1993). Changes in oxytocin immunoreactivity and mRNA expression in the sheep brain during pregnancy, parturition and lactation and in response to oestrogen and progesterone. Journal of Neuroendocrinology, 5, 435444. Broad, K. D., Levy, F., Evans, G., Kimura, T., Keverne, E. B., & Kendrick, K. M. (1999a). Previous maternal experience potentiates the effect of parturition on oxytocin receptor mRNA expression in the paraventricular nucleus. European Journal of Neuroscience, 11, 37253737. Caba, M., Poindron, P., Krehbiel, D., Levy, F., Romeyer, A., & Venier, G. (1995). Naltrexone delays the onset of maternal
67
behavior in primiparous parturient ewes. Pharmacology, Biochemistry and Behavior, 52, 743748. Choleris, E., Gustafsson, J. A., Korach, K. S., Muglia, L. J., Pfaff, D. W., & Ogawa, S. (2003). Ann estrogen-dependent four-gene micronet regulating social recognition: A study with oxytocin and estrogen receptor-alpha and -beta knockout mice. Proceedings of the National Academy of Sciences of the United States of America, 100, 61926197. Cohen-Tannoudji, J., Lavenet, C., Locatelli, A., Tillet, Y., & Signoret, J. P. (1989). Non-involvement of the accessory olfactory system in the LH response of anoestrous ewes to male odour. Journal of Reproduction and Fertility, 86, 135 144. Curtis, J. T., & Wang, Z. (2005). Ventral tegmental area involvement in pair bonding in male prairie voles. Physiology and Behavior, 86, 338346. Da Costa, A. P., Broad, K. D., & Kendrick, K. M. (1997). Olfactory memory and maternal behaviour-induced changes in c-fos and zif/268 mRNA expression in the sheep brain. Brain Research Molecular Brain Research, 46, 6376. Da Costa, A. P., De La Riva, C., Guevara-Guzman, R., & Kendrick, K. M. (1999). C-fos and c-jun in the paraventricular nucleus play a role in regulating peptide gene expression, oxytocin and glutamate release, and maternal behaviour. European Journal of Neuroscience, 11, 2199 2210. Da Costa, A. P., Guevara-Guzman, R. G., Ohkura, S., Goode, J. A., & Kendrick, K. M. (1996). The role of oxytocin release in the paraventricular nucleus in the control of maternal behaviour in the sheep. Journal of Neuroendocrinology, 8, 163177. Dwyer, C. M., & Lawrence, A. B. (2000). Maternal behaviour in domestic sheep (Ovis aries): Consistency and change with maternal experience. Behaviour, 137, 13911413. Ferreira, G., Meurisse, M., Gervais, R., Ravel, N., & Levy, F. (2001). Extensive immunolesions of basal forebrain cholinergic system impair offspring recognition in sheep. Neuroscience, 106, 103115. Ferreira, G., Terrazas, A., Poindron, P., Nowak, R., Orgeur, P., & Levy, F. (2000). Learning of olfactory cues is not necessary for early lamb recognition by the mother. Physiology and Behavior, 69, 405412. Frankland, P. W., & Bontempi, B. (2005). The organization of recent and remote memories. Nature Review Neuroscience, 6, 119130. Gonzalez-Mariscal, G., & Poindron, P. (2002). Parental care in mammals: Immediate internal and sensory factors of control. In D. W. Pfaff, A. P. Arnold, A. M. Etgen, S. E. Fahrfbach, & R. T. Rubin (Eds.), Hormones, brain and behavior (Vol. 1, pp. 215298). New York: Academic Press. Gubernick, D. J. (1981). Parent and infant attachment in mammals. In D. J. Gubernick & P. H. Klopfer (Eds.), Parental care in mammals (pp. 243305). New-York: Plenum Press. Hass, C. C. (1990). Alternative maternal-care patterns in two herds of bighorn sheep. Journal of Mammalogy, 71, 2435. Hernandez, H., Seran, N., Vazquez, H., Delgadillo, J. A., & Poindron, P. (2001). Maternal selectivity suppression through peripheral anosmia affects neither overall nursing frequency
68
Developmental Psychobiology. DOI 10.1002/dev control of maternal behaviour and olfactory recognition of offspring. Brain Research Bulletin, 44, 383395. Kendrick, K. M., Guevara-Guzman, R., Zorrilla, J., Hinton, M. R., Broad, K. D., Mimmack, M., & Ohkura, S. (1997b). Formation of olfactory memories mediated by nitric oxide. Nature, 388, 670674. Kendrick, K. M., & Keverne, E. B. (1991). Importance of progesterone and estrogen priming for the induction of maternal behavior by vaginocervical stimulation in sheep: Effects of maternal experience. Physiology and Behavior, 49, 745750. Kendrick, K. M., Keverne, E. B., Chapman, C., & Baldwin, B. A. (1988a). Intracranial dialysis measurement of oxytocin, monoamine and uric acid release from the olfactory bulb and substantia nigra of sheep during parturition, suckling, separation from lambs and eating. Brain Research, 439, 1 10. Kendrick, K. M., Keverne, E. B., Chapman, C., & Baldwin, B. A. (1988b). Microdialysis measurement of oxytocin, aspartate, gama-aminobutyric acid and glutamate release from the olfactory bulb of the sheep during vaginocervical stimulation. Brain Research, 442, 171174. Kendrick, K. M., Keverne, E. B., Hinton, M. R., & Goode, J. A. (1992a). Oxytocin, amino acid and monoamine release in the region of the medial preoptic area and bed nucleus of the stria terminalis of the sheep during parturition and suckling. Brain Research, 569, 199209. Kendrick, K. M., Levy, F., & Keverne, E. B. (1991). Importance of vaginocervical stimulation for the formation of maternal bonding in primiparous and multiparous parturient ewes. Physiology and Behavior, 50, 595600. Kendrick, K. M., Levy, F., & Keverne, E. B. (1992b). Changes in the sensory processing of olfactory signals induced by birth in sheep. Science, 256, 833836. Keverne, E. B. (1992). Primate social relationships: Their determinants and consequences. Advances in the Study of Behavior, 21, 137. Keverne, E. B., & Kendrick, K. M. (1991). Morphine and corticotrophin-releasing factor potentiate maternal acceptance in multiparous ewes after vaginocervical stimulation. Brain Research, 540, 5562. Keverne, E. B., Levy, F., Poindron, P., & Lindsay, D. R. (1983). Vaginal stimulation: An important determinant of maternal bonding in sheep. Science, 219, 8183. Keverne, E. B., Martel, F. L., & Nevison, C. M. (1996). Primate brain evolution: Genetic and functional considerations. Proceedings of the Royal Society of London. Series B: Biological Sciences, 263, 689696. Klopfer, P. H., Adams, D. K., & Klopfer, M. S. (1964). Maternal imprinting in goats. Proceedings of the National Academy of Sciences of the United States of America, 52, 911 914. Klopfer, P. H., & Gamble, J. (1966). Maternal imprinting in goats: The role of chemical senses. Zeitschrift Fur Tierpsychologie, 23, 588592. Klopfer, P. H., & Klopfer, M. S. (1968). Maternal imprinting in goats: Fostering of alien young. Zeitschrift Fur Tierpsychologie, 25, 862866.
and duration, nor lactation performance in ewes. Behavioural Processes, 53, 203209. Hernandez, H., Serafn, N., Terrazas, A., Marnet, P. G., Kann, G., Delgadillo, J. A., & Poindron, P. (2002). Maternal olfaction differentially modulates oxytocin and prolactin release during suckling in goats. Hormones and Behavior, 42, 232244. Hersher, L., Richmond, J. B., & Moore, A. U. (1963a). Maternal behavior in sheep and goats. In H. L. Rheingold (Ed.), Maternal behavior in mammals (pp. 203232). New-York: John Wiley and Sons Inc. Hersher, L., Richmond, J. B., & Moore, A. U. (1963b). Modiability of the critical period for the development of maternal behavior in sheep and goats. Behaviour, 20, 311319. Horn, G., & McCabe, B. J. (1984). Predispositions and preferences. Effects on imprinting of lesions to the chick brain. Animal Behaviour, 32, 288292. Jansen, H. T., Iwamoto, G. A., & Jackson, G. L. (1998). Central connections of the ovine olfactory bulb formation identied using wheat germ agglutinin-conjugated horseradish peroxidase. Brain Research Bulletin, 45, 2739. Johnston, R. E. (1998). Pheromones, the vomeronasal system, and communication: From hormonal responses to individual recognition. Annals of New York Academy of Sciences, 855, 333348. Keller, M. (2003). Processus dacquisition et de consolidations impliques dans la memorisation des caracteristiques multisensorielles du jeune par la brebis: Approches comportementale et neurobiologique. Unpublished Doctorat dUniversite, Paris XIII, Paris. Keller, M., Meurisse, M., Poindron, P., Nowak, R., Ferreira, G., Shayit, M., & Levy, F. (2003). Maternal experience inuences the establishment of visual/auditory, but not olfactory recognition of the newborn lamb by ewes at parturition. Developmental Psychobiology, 43, 167176. Keller, M., Meurisse, M., & Levy, F. (2004a). Mapping the neural substrates involved in maternal responsiveness and lamb olfactory memory in parturient ewes using Fos Iimaging. Behavioral Neuroscience, 118, 12741284. Keller, M., Meurisse, M., & Levy, F. (2005). Mapping of brain networks involved in consolidation of lamb recognition memory. Neuroscience, 133, 359369. Keller, M., Perrin, G., Meurisse, M., Ferreira, G., & Levy, F. (2004b). Cortical and medial amygdala are both involved in the formation of olfactory offspring memory in sheep. European Journal of Neuroscience, 20, 34333441. Kendrick, K. M. (1994). Neurobiological correlates of visual and olfactory recognition in sheep. Behavioural Processes, 33, 89112. Kendrick, K. M. (2000). Oxytocin, motherhood and bonding. Experimental Physiology, 85S, 111124. Kendrick, K. M., & Keverne, E. B. (1989). Effects of intracerebroventricular infusions of naltrexone and phentolamine on central and peripheral oxytocin release and on maternal behaviour induced by vaginocervical stimulation in the ewe. Brain Research, 505, 329332. Kendrick, K. M., Da Costa, A. P., Broad, K. D., Ohkura, S., Guevara, R., Levy, F., & Keverne, E. B. (1997a). Neural
Developmental Psychobiology. DOI 10.1002/dev Le Neindre, P., Poindron, P., & Delouis, C. (1979). Hormonal induction of maternal behavior in non-pregnant ewes. Physiology and Behavior, 22, 731734. Leinders-Zufall, T., Lane, A. P., Puche, A. C., Ma, W., Novotny, M. V., Shipley, M. T., & Zufall, F. (2000). Ultrasensitive pheromone detection by mammalian vomeronasal neurons. Nature, 405, 792796. Levy, F., Ferreira, G., Keller, M., Meurisse, M., & Perrin, G. (2005). Neural substrates involved in the control of maternal responsiveness and maternal selectivity differ in sheep. Developmental Psychobiology, 47, 436. Levy, F., & Fleming, A. S. (2006). The neurobiology of maternal behavior in Mammals. In P. J. Marshall & N. A. Fox (Eds.), The development of social engagement. Neurobiological perspectives (pp. 197246). New York: Oxford University Press. Levy, F., Gervais, R., Kindermann, U., Orgeur, P., & Piketty, V. (1990). Importance of beta-noradrenergic receptors in the olfactory bulb of sheep for recognition of lambs. Behavioral Neuroscience, 104, 464469. Levy, F., Gervais, R., Kindermann, U., Litterio, M., Poindron, P., & Porter, R. (1991). Effects of early post-partum separation on maintenance of maternal responsiveness and selectivity in parturient ewes. Applied Animal Behaviour Science, 31, 101110. Levy, F., Guevara-Guzman, R., Hinton, M. R., Kendrick, K. M., & Keverne, E. B. (1993). Effects of parturition and maternal experience on noradrenaline and acetylcholine release in the olfactory bulb of sheep. Behavioral Neuroscience, 107, 662 668. Levy, F., Kendrick, K. M., Goode, J. A., Guevara-Guzman, R., & Keverne, E. B. (1995a). Oxytocin and vasopressin release in the olfactory bulb of parturient ewes: Changes with maternal experience and effects on acetylcholine, gammaaminobutyric acid, glutamate and noradrenaline release. Brain Research, 669, 197206. Levy, F., Kendrick, K., Keverne, E. B., Porter, R. H., & Romeyer, A. (1996). Physiological, sensory and experiential factors of parental care in sheep. Advances in the Study of Behavior, 25, 385473. Levy, F., Locatelli, A., Piketty, V., Tillet, Y., & Poindron, P. (1995b). Involvement of the main but not the accessory olfactory system in maternal behavior of primiparous and multiparous ewes. Physiology and Behavior, 57, 97104. Levy, F., & Poindron, P. (1984). Inuence du liquide amniotique sur la manifestation du comportement maternel chez la brebis parturiente. Biology of Behaviour, 9, 271278. Levy, F., & Poindron, P. (1987). The importance of amniotic uids for the establishment of maternal behaviour in experienced and inexperienced ewes. Animal Behaviour, 35, 11881192. Levy, F., Poindron, P., & Le Neindre, P. (1983). Attraction and repulsion by amniotic uids and their olfactory control in the ewe around parturition. Physiology and Behavior, 31, 687 692. Levy, F., Richard, P., Meurisse, M., & Ravel, N. (1997). Scopolamine impairs the ability of parturient ewes to learn to recognise their lambs. Psychopharmacology, 129, 8590.
69
Lickliter, R. E. (1982). Effects of a post-partum separation on maternal responsiveness in primiparous and multiparous domestic goats. Applied Animal Ethology, 8, 537542. Maviel, T., Durkin, T. P., Menzaghi, F., & Bontempi, B. (2004). Sites of neocortical reorganization critical for remote spatial memory. Science, 305, 9699. Meurisse, M., Gonzalez, A., Delsol, G., Caba, M., Levy, F., & Poindron, P. (2005a). Estradiol receptora expression in hypothalamic and limbic regions of ewes is inuenced by physiological state and maternal experience. Hormones and Behavior, 48, 3443. Meurisse, M., Perrin, G., Keller, M., & Levy, F. (2005b). Neuroanatomical connections of the cortical and medial amygdala in sheep. Paper presented at the 7th biannual meeting of the french neuroscience society, Lille. Morgan, P. D., Boundy, C. A. P., Arnold, G. W., & Lindsay, D. R. (1975). The roles played by the senses of the ewe in the location and recognition of lambs. Applied Animal Ethology, 1, 139150. Numan, M., Fleming, A. S., & Levy, F. (2006). Maternal behavior. In J. D. Neill (Ed.), The physiology of reproduction, 3rd edition (Vol. 2, pp. 19211993). New York: Elsevier. Numan, M., & Insel, T. R. (2003). The neurobiology of parental behavior. New York: Springer-Verlag. Panksepp, J., Nelson, E., & Bekkedal, M. (1997). Brain systems for the mediation of social separation distress and social reward. Annals of the New York Academy of Sciences, 807, 78100. Pissonnier, D., Thiery, J. C., Fabre-Nys, C., Poindron, P., & Keverne, E. B. (1985). The importance of olfactory bulb noradrenalin for maternal recognition in sheep. Physiology and Behavior, 35, 361363. Pitkanen, A. (2000). Connectivity of the rat amygdaloid complex. In J. Aggleton (Ed.), The amygdala: A functional analysis (pp. 31117). Oxford: Oxford University Press. Poindron, P. (1976a). Effets de la suppression de lodorat, sans lesion des bulbes olfactifs, sur la selectivite du comportement maternel de la Brebis. Comptes Rendus Hebdomadaires Des Seances de lAcademie des Sciences de Paris. Serie D: Sciences Naturelles, 282, 489491. Poindron, P. (1976b). Mother-young relationships in intact or anosmic ewes at the time of suckling. Biology of Behaviour, 2, 161177. ` Poindron, P. (1981). Contribution a letude des mecanismes de regulation du comportement maternel chez la brebis (Ovis aries ` L.). Unpublished Doctorat dEtat es Sciences Naturelles, Universite de Provence (Aix-Marseille 1), Marseille, France. Poindron, P., Caba, M., Gomora Arrati, P., Krehbiel, D., & Beyer, C. (1994). Responses of maternal and non-maternal ewes to social and mother-young separation. Behavioural Processes, 31, 97110. Poindron, P., Gilling, G., Hernandez, H., Seran, N., & Terrazas, A. (2003a). Early recognition of newborn goat kids by their mother: INon-olfactory discrimination. Developmental Psychobiology, 43, 8289. Poindron, P., Hernandez, H., Navarro, M. L., Gonzalez, F., Delgadillo, J. A., & Garcia, S. (1998). Relaciones madre-cria
70
Developmental Psychobiology. DOI 10.1002/dev Romeyer, A., & Poindron, P. (1992). Early maternal discrimination of alien kids by post-parturient goats. Behavioural Processes, 26, 103112. Romeyer, A., Poindron, P., & Orgeur, P. (1994a). Olfaction mediates the establishment of selective bonding in goats. Physiology and Behavior, 56, 693700. Romeyer, A., Poindron, P., Porter, R. H., Levy, F., & Orgeur, P. (1994b). Establishment of maternal bonding and its mediation by vaginocervical stimulation in goats. Physiology and Behavior, 55, 395400. Romeyer, A., Porter, R. H., Levy, F., Nowak, R., Orgeur, P., & Poindron, P. (1993a). Maternal labelling is not necessary for the establishment of discrimination between kids by recently parturient goats. Animal Behaviour, 46, 705712. Romeyer, A., Porter, R. H., Poindron, P., Orgeur, P., Chesne, P., & Poulain, N. (1993b). Recognition of dizygotic and monozygotic twin lambs by ewes. Behaviour, 127, 119139. Rosenblatt, J. S., & Siegel, H. I. (1981). Factors governing the onset and maintenance of maternal behavior among nonprimate Mammals. In D. J. Gubernick & P. H. Klopfer (Eds.), Parental care in mammals (pp. 1376). New-York: Plenum Press. Rosenblatt, J. S., Siegel, H. I., & Mayer, A. D. (1979). Progress in the study of maternal behavior in the rat: Hormonal, nonhormonal, sensory, and developmental aspects. Advances in the Study of Behavior, 10, 225311. Sanchez-Andrade, G., James, B. M., & Kendrick, K. M. (2005). Neural encoding of olfactory recognition memory. Journal of Reproduction and Development, 51, 547558. Smith, F. V., Van-Toller, C., & Boyes, T. (1966). The critical period in the attachment of lambs and ewes. Animal Behaviour, 14, 120125. Terrazas, A., Seran, N., Hernandez, H., Nowak, R., & Poindron, P. (2003). Early recognition of newborn goat kids by their mother: II. Auditory recognition and evidence of an individual acoustic signature in the neonate. Developmental Psychobiology, 43, 311320. Trinh, K., & Storm, D. R. (2003). Vomeronasal organ detects odorants in absence of signaling through main olfactory epithelium. Nature Neuroscience, 6, 519525. Young, L. J., Lim, M. M., Gingrich, B., & Insel, T. R. (2001). Cellular mechanisms of social attachment. Hormones and Behavior, 40, 133138.
en cabras. Proceedings of the XIII Reunion Nacional Sobre Caprinocultura, San Luis Potosi, Mexico, 2123 Octobre 1998, pp. 4866. Poindron, P., & Le Neindre, P. (1980). Endocrine and sensory regulation of maternal behavior in the ewe. Advances in the Study of Behavior, 11, 75119. Poindron, P., Le Neindre, P., Raksanyi, I., Trillat, G., & Orgeur, P. (1980). Importance of the characteristics of the young in the manifestation and establishment of maternal behaviour in sheep. Reproduction Nutrition Development, 20, 817 826. Poindron, P., & Levy, F. (1990). Physiological, sensory and experiential determinants of maternal behaviour in sheep. In N. A. Krasnegor & R. B. Bridges (Eds.), Mammalian parenting: Biochemical, neurobiological and behavioral determinants (pp. 133156). New-York: Oxford University Press. Poindron, P., Levy, F., & Krehbiel, D. (1988). Genital, olfactory, and endocrine interactions in the development of maternal behaviour in the parturient ewe. Psychoneuroendocrinology, 13, 99125. Poindron, P., Raksanyi, I., Orgeur, P., & Le Neindre, P. (1984). ` Comparaison du comportement maternel en bergerie a la parturition chez des brebis primipares ou multipares de race Romanov, Prealpes de Sud et Ile-de-France. Genetique Selection Evolution, 16, 503522. Poindron, P., Seran, N., Terrazas, A., Hernandez, H., Meurisse, M., Houot, B., et al. (2003b). Comparison of the effects of two methods of main olfactory system impairment on olfactory discrimination and selective nursing of lamb by ewes. Acta Neurobiologiae Experimentalis, 63 (Supplement), 48. Porter, R. H., Levy, F., Nowak, R., Orgeur, P., & Schaal, B. (1994). Lambs individual odor signatures: Mosaic hypothesis. Advances in the Biosciences, 93, 233238. Porter, R. H., Levy, F., Poindron, P., Litterio, M., Schaal, B., & Beyer, C. (1991). Individual olfactory signatures as major determinants of early maternal discrimination in sheep. Developmental Psychobiology, 24, 151158. Ramrez, A., Quiles, A., Hevia, M. L., Sotillo, F., & Ramrez, M. C. (1996). Effects of immediate and early postpartum separation on maintenance of maternal responsiveness in parturient multiparous goats. Applied Animal Behaviour Science, 48, 215224.

FTP

Încărcat de

Informații document

Descriere originală:

Titlu original

Drepturi de autor

Formate disponibile

Partajați acest document

Partajați sau inserați document

Opțiuni de partajare

Vi se pare util acest document?

Este necorespunzător acest conținut?

Drepturi de autor:

Formate disponibile

FTP

Încărcat de

Drepturi de autor:

Formate disponibile

Pascal Poindron Frederic Levy

Developmental Psychobiology. DOI 10.1002/dev

Maternal Bonding in Sheep and Goats

Poindron, Keller, and Levy

Developmental Psychobiology. DOI 10.1002/dev

THE SENSITIVE PERIOD Sensitive Period Versus Critical Period

Developmental Psychobiology. DOI 10.1002/dev

Maternal Bonding in Sheep and Goats

The Sensitive Period and Maternal Selectivity

Poindron, Keller, and Levy

Developmental Psychobiology. DOI 10.1002/dev

Cues Involved in the Maintenance of Maternal Responsiveness

Developmental Psychobiology. DOI 10.1002/dev

Maternal Bonding in Sheep and Goats

Poindron, Keller, and Levy

Developmental Psychobiology. DOI 10.1002/dev

Sensory Cues Involved in the Establishment of Maternal Selectivity

Developmental Psychobiology. DOI 10.1002/dev

Maternal Bonding in Sheep and Goats

Poindron, Keller, and Levy

Developmental Psychobiology. DOI 10.1002/dev

PHYSIOLOGICAL AND NEUROBIOLOGICAL CONTROL OF MATERNAL RESPONSIVENESS AND SELECTIVITY

Developmental Psychobiology. DOI 10.1002/dev

Maternal Bonding in Sheep and Goats

Maternal Recognition and Selectivity

Poindron, Keller, and Levy

Developmental Psychobiology. DOI 10.1002/dev

Developmental Psychobiology. DOI 10.1002/dev

Maternal Bonding in Sheep and Goats

CONCLUSIONS AND PERSPECTIVES

Poindron, Keller, and Levy

Developmental Psychobiology. DOI 10.1002/dev

Maternal Bonding in Sheep and Goats

Poindron, Keller, and Levy

Maternal Bonding in Sheep and Goats

Poindron, Keller, and Levy

S-ar putea să vă placă și