1. Social Attachment Social attachment involves development of a “social bond” between individuals. A social bond can form between a mother and her offspring. –Ex. Sheep (ewe and lamb) –moms nurse only their own young (lambs) and reject the lambs of other females A social bond can form between an adult female or male and their mate. –Ex. voles –prairie vole--monogamous species in which one male pairs with one female, a relationship that often extends the lifetime of the individuals; males and females prefer to spend time with each other, they engage in biparental care and show aggression against intruders –montane vole--polygamous species in which males and females pair repeatedly with different members of their species, with females showing most of the parental care Oxytocin has been implicated in the social bond that forms between the ewe and her lamb, as well as social bonding in female prairie voles. Vasopressin has been implicated in social bonding in male prairie voles.

2. Social Attachment-Sheep Nonpregnant ewes: show aversion to the odors of lambs--avoid or withdraw from lambs show aggression toward lambs--“butting” lambs Immediately after parturition, the pregnant ewe shows two responses: maternal behavior –approaching and following the lamb –low-pitched bleating (vocalizations) –sniffing and licking the lamb –permitting suckling (nursing) –behaviors inhibited: withdrawing from lamb & butting the lamb olfactory recognition of lamb –formation of a social bond with lamb leading to selective nursing of own lamb but not that of others (formation of an olfactory memory)

3. Social Attachment-Sheep Hormonal and somatosensory inputs are critical for the display of maternal behavior. –near the end of pregnancy, levels of estrogen and prolactin rise, while the levels of progesterone drop –prolonged exposure to progesterone and estrogen during pregnancy is important for priming the brain to respond to the triggering effects of the drop in progesterone and the rise in estrogen at the time of parturition (prolactin is not thought to be critical for maternal behavior in the ewe) –vaginocervical stimulation (VCS) experienced during the process of birth is important in stimulating the display of maternal behavior –block “neural transmission” associated with VCS by administering an anesthetic to the spinal cord (dura) 1 1/2 hours prior to parturition, maternal behavior will be blocked in 90% of primiparous ewes (birth of first lamb) and in 25% of multiparous ewes –if you stimulate the vagina and cervix of nonpregnant ewes primed with gonadal steroids, maternal behavior will be stimulated; this effect is not seen in nonpregnant females that have not been hormonally primed

5. Social Attachment-Sheep Oxytocin--a critical hormone in the activation of maternal behavior. Oxytocin levels increase during parturition. –oxytocin levels increase significantly within the bloodstream during parturition--uterine contractions, and during nursing--milk-letdown –oxytocin levels also increase significantly within the brain as measured by increased levels within the cerebrospinal fluid (CSF)--fluid that bathes the brain –increased oxytocin levels within the cerebrospinal fluid reflects synthesis and release within the brain as little oxytocin from the bloodstream is thought to pass through the blood-brain-barrier in the adult Oxytocin plays a critical role in “activating” maternal behavior. –in hormonally-primed ewes, administration of oxytocin within the cerebrospinal fluid (CSF) will stimulate the display of maternal behavior--approaching and following the lamb, low-pitched bleating, permitting suckling, sniffing and licking the lamb, and reduced aversive and aggressive responses –note--administration of prolactin does not stimulate maternal behavior in sheep

6. Social Attachment-Sheep Oxytocin--a critical hormone in the activation of maternal behavior. Gonadal steroids and VCS play a critical role in oxytocin regulation. –in hormonally-primed ewes, VCS leads to increased release of oxytocin within the brain as evidenced by increased levels of oxytocin within the cerebrospinal fluid; this effect is not seen in nonpregnant, nonhormonally primed females –as noted previously: if “neural transmission” associated with VCS is blocked by administering an anesthetic to the spinal cord (dura) 1 1/2 hours prior to parturition, maternal behavior will be blocked in 90% of primiparous ewes (birth of first lamb) and in 25% of multiparous ewes –blocking “neural transmission” associated with VCS blocks the rise in oxytocin levels within the CSF; administration of oxytocin to ewes with a spinal block will restore maternal behavior

7. Social Attachment-Sheep Neuroanatomy: Hormonal priming serves to increase oxytocin levels and oxytocin receptors. VCS stimulates release of oxytocin from the PVN. Oxytocin neurons within the PVN project to numerous brain regions with select functions: –reduction in aggressive and aversive responses: oxytocin release within MPOA, BNST, medial amygdala and olfactory bulbs –formation of olfactory memory: oxytocin release within the olfactory bulbs –inhibition of female sex behavior: oxytocin release within the hypothalamus (medibasal hypothalamus--MBH) –immobilization: oxytocin release within the substantia nigra (important for nursing) –facilitation of positive responses (e.g., approach and following, vocalizations): oxytocin release within lateral septum, cingulate cortex and ventral tegmental area (VTA)

8. Social Attachment-Sheep Oxytocin--a critical hormone in the development of a social bond. –within 1-2 hours following parturition, ewe will form a social bond with her lamb –this “social bond” consists of a lasting olfactory memory that allows the ewe to identify her lamb and to allow for selective nursing of her own lamb but not that of others –formation of this “social bond” is critical--if this bond does not form, the ewe will not allow her lamb to suckle –hormonal priming and VCS are important as they increase the levels of oxytocin within the brain “activating” maternal behavior and stimulating the development of a “social bond”. It is possible to cause a female ewe to bond to a strange lamb: –if a pregnant ewe has given birth to her lamb, and 2-3 days later you manually stimulate her vagina and cervix, she will accept and bond with a strange lamb even after she has already bonded with her own lamb –manual stimulation has led to increases in oxytocin levels within the brain that stimulated the development of an olfactory memory

9. Social Attachment-Sheep How does oxytocin play a role in the development of an olfactory memory? –oxytocin stimulates the development of an olfactory memory by increasing the release of norepinephrine (NE) from terminals present within the olfactory bulbs –NE acts within the olfactory bulbs to increase the ewe’s responsiveness to lamb odors (the mechanism is complex, and additional molecules involved) –the plastic changes that occur at the level of the olfactory bulbs are transferred to secondary and tertiary olfactory regions within the brain Evidence for this relationship: –oxytocin levels increase within the olfactory bulb at parturition –oxtocin facilitates the release of NE within the olfactory bulb at parturition –blocking the action of NE by administering an antagonist within the olfactory bulb inhibits the formation of an olfactory memory –lesioning the olfactory bulbs blocks the formation of a selective “social bond” between ewe and lamb

10. Olfactory Bulbs Sensory Receptors Secondary Olfactory Structures lamb odors PVN oxytocin Locus Coeruleus NE + + Tertiary Olfactory Structures Formation of an Olfactory Memory Secondary structures: amygdala & piriform cortex Tertiary structures: orbitofrontal cortex, entorhinal cortex, hippocampus, septum

11. Social Attachment-Sheep Maternal experience in multiparous ewes enhances maternal responsiveness. –it increases the rate at which ewes bond with their lambs: multiparous ewes selectively bond with their lambs within 2 hours, while primiparous ewes require 4 to 6 hours to bond with their lambs –it increases the amount of oxytocin that is released within the olfactory bulbs: oxytocin release within the olfactory bulbs at parturition is much greater in multiparous ewes than in primiparous ewes –it increases the ability of oxytocin to increase release of NE even without hormonal priming associated with pregnancy: administration of oxytocin into the olfactory bulbs of multiparous ewes (not currently pregnant) stimulates NE release within the olfactory bulbs, but this effect is not observed in nulliparous ewes (ewes that were never pregnant) –it underlies numerous differences that exist between primiparous and multiparous ewes: Ex. blocking “neural transmission” associated with VCS blocks maternal behavior in 90% of primiparous ewes but only in 25% of multiparous ewes; multiparous ewes are less dependent upon VCS to stimulate oxytocin release and to activate maternal behavior

12. Social Attachment-Voles Prairie Vole--Monogamous Species: background history: –mouse-sized rodent that lives in burrows across the American Midwest –prairie voles are found in multigenerational family groups with a single breeding pair –the single breeding pair exhibits the classic features of monogamy: 1) a breeding pair shares the same nest and territory where they are in frequent contact--high degree of affiliative behavior (males and females will spend more than 50% sitting side by side), 2) males and females participate in biparental care, 3) intruders of either sex are rejected, and 4) following the death of one of the pair, a new mate is accepted only 20 % of the time –prairie voles are an example of a species that shows “induced ovulation and behavioral estrus”--female must be exposed to a pheromone from an unrelated male which stimulates her reproductive axis stimulating estrogen secretion, sexual receptivity, mating and then ovulation –following mating, a selective and enduring pair bond is formed between male and female prairie voles

13. a female is reproductively inactive until exposed to a male a male pheromone stimulates GnRH release (neuroendocrine reflex) –GnRH release stimulates FSH and LH release, follicular development and secretion of estrogen increasing levels of estrogen stimulate behavioral estrus vaginocervical stimulation (via intromissions from male) stimulates further GnRH release –GnRH release will lead to LH surge and ovulation after ovulation, progesterone will maintain pregnancy if necessary GnRH Neuron HYPO ANT PIT OVARY LH GnRH + GnRH: gonadotrophin releasing hormone FSH: follicle stimulating hormone LH: luteinizing hormone follicle “ovulation” vaginocervical stimulation spinal cord GnRH Neuroendocrine Reflex--twice LH FSH estrogen stimulate sex behavior Induced Estrus &Ovulation pheromone

14. Social Attachment-Voles Montane Vole--Polygamous Species: background history: –they are found in isolated burrows (in high meadows in the Rockies) –they show little interest in social contact; in the laboratory, they spend little time in side- by-side contact –males and females mate with multiple partners (hence the term “polygamous”) –the males show little if any parental care –the females frequently abandon their young between 8 and 14 days postpartum –no pair bond is formed between male and female montane voles

15. Social Attachment-Voles The formation of a pair bond between a male and female prairie vole results in two effects: –preference to spend time with one’s mate over a stranger –display of high levels of aggression against an intruder Partner Preference Test: –following 24 h exposure to a male, the female prairie vole will spend more time in her partner’s cage (compared to the time spent in the neutral or stranger cage), while the female montane vole will spend more time in the neutral cage Resident-Intruder Test: –following 24 h exposure to a female, the male prairie vole shows a significant increase in the frequency of aggressive responses toward an intruder (40-fold induction); this effect was sustained for months after long-term housing with females –in contrast, mating had no effect on intruder aggression in the male montane vole

16. Social Attachment-Voles What makes these species so different? Do these species differ with respect to the central pathways for oxytocin or vasopressin? Does oxytocin or vasopressin play a selective role in pair bonding? Reason for focusing on oxytocin and vasopressin: –oxytocin and vasopressin are produced by neurons in the hypothalamus –these peptides are closely related structurally, differing only in two amino acids –these two hormones are released into the bloodstream (posterior pituitary) and within the brain –oxytocin--milk ejection, uterine contractions, maternal behavior, sex behavior, stress, grooming, and development of social bonds (sheep) –vasopressin--water balance, aggressive behavior, scent marking, stress, grooming

17. Social Attachment-Voles Does oxytocin or vasopressin play a role in pair bonding? Answer? Yes Female Prairie Vole –females that are paired with a male but they do not engage in mating show low levels of partner preference –administration of oxytocin, but not vasopressin, within the cerebrospinal fluid (CSF) of a paired but unmated female significantly increased her preference to spend time with her partner –females that are paired with a male and that also engage in mating show high levels of partner preference –administration of a receptor antagonist for oxytocin, but not for vasopressin, decreases partner preference –oxytocin released with mating is both necessary and sufficient for the formation of a pair bond in the female prairie voles

18. Social Attachment-Voles Does oxytocin or vasopressin play a role in pair bonding? Answer? Yes Male Prairie Vole –when males are exposed to females, but are not permitted to mate, they show neither partner preference (nor the selective aggression) –administration of vasopressin, but not oxytocin, within the cerebrospinal fluid (CSF) of a paired but unmated male significantly increased her preference to spend time with her partner (this included an increase in selective aggression) –males that are paired with a female and that also engage in mating show high levels of partner preference (and selective aggression) –administration of a receptor antagonist for vasopressin, but not for oxytocin, decreases partner preference –vasopressin released during mating is both necessary and sufficient for formation of a partner preference in male prairie voles

19. Social Attachment-Humans The role of hormones in the process of social attachment in humans is less clear. There is clear evidence that hormone levels change in men and women during sex, and in women during child birth (parturition). –in men, levels of oxytocin and vasopressin increase within the cerebrospinal fluid during ejaculation –in women, levels of oxytocin increase within the cerebrospinal fluid (CSF) during parturition; of interest, oxytocin levels within the CSF increase during normal labor (include VCS), but not following delivery by Caesarean section (does not include VCS) Vasopressin and oxytocin receptors do exist within the brains of men and women (postmortem studies). Do changes in hormone levels in humans reflect the development of “social bonds” between men and women, or between a woman and her newborn infant? –we don’t currently know –current studies do not point to a strong relationship in humans

20. Social Attachment-Humans Does social stress alter oxytocin levels or responses to oxytocin? What is the general relationship between stress and oxytocin? What hormonal changes occur in abused women? Are abused women chronically stressed? oxytocin affiliative processes (social attachment) Could alterations in oxytocin levels be a possible mechanism to explain why “abused women” stay in abusive relationships?

21. Social Attachment-Humans Study: Winslow & Insel (1991) Background: –dominant (DOM) and subordinate (SUB) male squirrel monkeys show profound differences in testosterone levels and these differences correlate with different patterns of social, aggressive and nonsocial behaviors –What effect would the administration of oxytocin have on the behavior of DOM and SUB males? Design: –housed 2 male squirrel monkeys together--one male will become DOM while the other males becomes SUB –pairs of males werethen allowed to interact with a female repeatedly; they analyzed the effects of oxytocin administration on (within CSF) on various behaviors among the group (males plus female): 1) aggression, 2) sex behavior, 3) association behavior--affiliative behavior including approach, touch, huddle with partner, and 4) other responses such as grooming

22. Social Attachment-Humans Study: Winslow & Insel (1991) Results: –Reconfirmed finding that differences exist in testosterone levels between DOM and SUB males--DOM males have more testosterone than SUB males –DOM males: administration of oxytocin increased sexual and aggressive behavior –SUB males: administration of oxytocin increased associative behaviors (social affiliation) Conclusion: –the effects of oxytocin on the behavior of male squirrel monkeys depends on their social status; administration of oxytocin in SUB males increased their affiliative responses Possible Interpretations: –different levels of testosterone in DOM and SUB males may explain different responses to oxytocin--testosterone has been shown to increase oxytocin binding within the brain; lower levels of testosterone may reduce the number of oxytocin receptors and lead to differences in the response to oxytocin

23. Social Attachment-Humans Study: Winslow & Insel (1991) Possible Interpretations: –even though levels of testosterone differed between DOM and SUB males, it could be that “subordinate status” is the most critical variable and that prior experiences with “losing” influences how the SUB animas responds to administration of oxytocin Is abuse in women also associated with altered responses to oxytocin?--I don’t know! Some Interesting Comparisons: –increases in oxytocin within the brain stimulates maternal behavior and social bonding in some species (sheep) –stress can also stimulate oxytocin levels within the brain (oxytocin has been implicated in both increasing and decreasing responses to stress) –stress can inhibit production of gonadal steroids –gonadal steroids can affect various levels of hormones and neurotransmitters within the brain--including oxytocin

24. Social Attachment-Humans It is likely that the formation of “social bonds” and the display of parental behavior in humans is not coupled in any simple way to changes in levels of hormones. –Ex. Women (and men) can adopt babies and display perfectly normal maternal responses without ever experiencing pregnancy or parturition--so pregnancy associated changes in gonadal steroids and the process of giving birth (vaginocervical stimulation) are not critical for stimulating maternal behavior nor for developing social bonds. –This does not preclude the possibility that exposure to an infant can secondarily alter hormones levels within the brain that lead to changes in parental responses... An uncoupling of the “activational” effects of hormones on human behavior has also been reported for sex behavior and aggression. Current thesis: Hormones can alter human behavior, however, their effects are more subtle than those observed in lower mammals and as a consequence, they are harder to find and harder to study. Second, the effects of hormones are limited by other processes--e.g., conscious choice.