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American Journal of Primatology 73:516–529 (2011) REVIEW ARTICLE Emotions, Stress, and Maternal Motivation in Primates DARIO MAESTRIPIERIÃ Department of Comparative Human Development, The University of Chicago, Chicago, Illinois Recent research conducted with nonhuman primates confirms that adaptive emotional processes, such as maternal attraction arousability and maternal anxiety arousability, enhance and sustain female motivation to interact with infants, invest in them, and protect them during the postpartum period. Changes in these emotional processes, and concomitant changes in maternal motivation, facilitate the reduction and eventual termination of maternal investment associated with infant weaning. Although laboratory studies of rodents and socially deprived rhesus monkeys have suggested that nulliparous females are neophobic and find infant stimuli aversive, recent primate research indicates that neophobia or aversion to infant stimuli do not occur in females with normal developmental experience. Furthermore, although some rodent and human studies have shown that lactation is accompanied by physiological hyporesponsiveness to stress, other studies of rodents, nonhuman primates, and humans indicate that mothers are highly vulnerable to stress and that stress-induced dysregulation of emotions can interfere with maternal motivation and parenting behavior. It is possible that some aspects of the emotional and experiential regulation of maternal motivation and parental behavior are different in different mammalian species. However, variation in the environments in which subjects are tested and in their developmental experience may also be responsible for the some discrepancies between the results of different studies. Am. J. Primatol. 73:516–529, 2011. r 2010 Wiley-Liss, Inc. Key words: emotions; arousal; maternal motivation; rhesus monkeys; mammals INTRODUCTION in raising their litters without any prior maternal experience. In fact, in some of these species, Female parental care is the rule among the over nulliparous females avoid any contact with other 300 species of nonhuman primates, the exceptions females’ pups or kill them and cannibalize them, at being a few socially monogamous species in which least in the laboratory [e.g. Fleming & Orpen, 1986]. fathers carry their infants. Social monogamy and In rodents, maternal responsiveness and behavior paternal care are mainly concentrated among New are probably under relatively strong genetic control World monkeys and associated with particular repro- and are regulated by a combination of hormonal ductive or ecological characteristics (e.g. the produc- changes induced by pregnancy and lactation along tion of twins in marmosets and tamarins) [Snowdon with sensory stimulation from the offspring [e.g. & Suomi, 1982]. Among the Old World monkeys and Fleming & Orpen, 1986]. Unlike rodents, Old World the apes, females typically give birth to one infant at a monkeys, apes, and humans have relatively long life time, feed their offspring with milk for 1 year or more, spans, and in these species, many aspects of maternal and in some cases continue investing in them for the behavior depend, in part, on experience acquired rest of their lives with little or no contribution from during development. For example, nonhuman pri- males. During the period of infant dependence, mate mothers need experience to learn how to carry maternal care manifests itself mainly as breastfeed- their infants properly, to allow infants to maintain ing, carrying, and protecting the infant. Among great nipple contact long enough to obtain their necessary apes, mothers also play with their infants and share solid food with them. Primate maternal behavior is generally comparable, in terms of its basic character- istics, to that of many other mammalian species, ÃCorrespondence to: Dario Maestripieri, Department of Compara- although primate infants are generally carried more tive Human Development, The University of Chicago, 5730 S. Woodlawn Avenue, Chicago, IL 60637. E-mail: [email protected] by their mothers than other mammalian young. Received 2 July 2010; revised 8 August 2010; revision accepted In mammalian species with a short life span 12 August 2010 (e.g. many rodents), first-time mothers exhibit a full DOI 10.1002/ajp.20882 repertoire of maternal behavior from the moment Published online 24 September 2010 in Wiley Online Library their offspring are born and are generally successful (wileyonlinelibrary.com). r 2010 Wiley-Liss, Inc. Emotions, Stress, and Maternal Motivation / 517 nourishment, to protect infants from unwanted maternal motivation and facilitate the expression of attention from other conspecifics, and to encourage adaptive behavior. Stress-induced dysregulation of infant independence and weaning [e.g. Pryce, 1996]. emotions and their physiological substrates, how- In rhesus monkeys, newborn infants spend a ever, can alter maternal motivation and cause great deal of time nursing or sleeping on their maladaptive parenting behavior. mother’s chest. During this time, they are cradled Pryce [1992] proposed a systems model of the and groomed by mothers. Mothers carry their infants regulation of maternal motivation in mammals, in while they travel for several months. During time which emotional processes play a central role (Fig. 1). devoted to resting or social activities, however, The model was based mainly on research conducted infants spend increasing amounts of time out of with laboratory rats, sheep, and socially deprived contact with their mothers, in order to explore the rhesus monkeys. In this model, there are some inputs, environment or to play with other infants. Mothers some outputs, and some intermediary processes. The may restrict and control their infants’ activities by main inputs to the system are infant stimuli. The physically restraining them and by making contact outputs are maternal motivation and maternal beha- with them frequently. During the first few weeks of vior. Crucial intermediary processes are previous infant life, mothers are almost entirely responsible maternal experience, female hormonal state, and an for maintaining contact and proximity with their emotional system called maternal arousability. The infants. For example, infants tend to break contact maternal arousability system comprises four different and walk away from their mothers, while mothers subsystems: maternal attraction arousability, mater- follow them and reestablish contact. During the nal anxiety arousability, maternal aversion arousabil- second or third month of infant life, however, ity, and novelty-fear arousability. Attraction and responsibility for maintaining contact and proximity anxiety arousability have positive influences on ma- shifts to infants. Therefore, mothers frequently ternal motivation, whereas aversion arousability and break contact and walk away from their infants, novelty-fear arousability inhibit maternal motivation. while infants follow their mothers and make contact According to Pryce’s model, immature mamma- with them. Mothers encourage their infants’ inde- lian females are exposed to infant stimuli before they pendence by breaking contact with them frequently are reproductively mature; they store these stimuli in and physically rejecting their infants’ attempts to memory and gain practical experience with them. make contact and gain access to the nipples. The Memory and experience of infant stimuli gained early frequency of maternal rejection increases steadily in a female’s life will facilitate the recognition of these with infant age, peaking when infants are approxi- stimuli later in life and enhance motivation to interact mately 6 months old, when the mating season begins with them via the influence of positive arousability and mothers return into estrus. intermediary processes. Infant stimuli can be passive Although these basic features of maternal (e.g. visual or olfactory characteristics) or active (e.g. behavior are observed in all rhesus monkey females, facial expressions, vocalizations, or motor behavior). individual mothers differ greatly from one another in When females reach puberty and conceive, hormonal the frequency with which they cradle or groom their changes during pregnancy and around the time of infants, make or break contact with them, or restrain parturition enhance maternal motivation and facil- or reject them. Individual differences in maternal itate the expression of maternal behavior. Maternal behavior are consistent over time and across differ- arousability is the most direct intermediary variable ent infants. These differences are accounted for by regulating maternal motivation and is itself regulated sociodemographic characteristics of the mothers (e.g. by three input factors: infant stimuli, previous their age, previous maternal experience, or dom- experience, and neuroendocrine state. inance rank), those of their infants (e.g. age or sex), The maternal attraction arousability subsystem and those of the surrounding environment (e.g. processes passive, visual and olfactory stimuli and is availability of food, risk of predation, risk of aggres- enhanced by sensory recognition of the infant and by sion or infant kidnapping by other group members). neuroendocrine changes occurring during pregnancy Among the mothers’ characteristics that affect their and parturition. These stimuli include the shape of motivation to take care of their infants and the infant faces, the configurations of their bodies, or quality of their maternal care, their personality
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