1. Perinatal Behavior Amanda Robinson

2. Lesson Plan Day 1 Prenatal Maternal Behavior Normal behavior in production animals Stress effects Fetal Behavior Human fetal behaviors Pain perception Onset of consciousness Neonatal Behavior Onset of consciousness continued Assessing newborn welfare Basic behavior states Day 2 Postnatal Maternal Behavior Normal behavior in production animals Endocrine control of behavior

3. Prenatal Maternal Behavior

4. Preparturient Behavior in Cattle Maternal behavior actually begins prior to calving Cows demonstrate some tendencies to select a birth site Wehrend et al. (2006) reported that approximately one third of cows performed ‘nestbuilding-like behavior’ in the hours before calving Cattle appear to invest little effort in preparing a nesting site likely because the precocial young spend little time at the birth site following parturition (Poindron, 2005)

5. Preparturient Behavior in Cattle Some studies (and some producers) report that most cows isolate themselves at calving; other studies (and other producers) claim the tendency to isolate is not that strong depends on age of the female and the environmental conditions Cows appear to adjust their behavior to the conditions present at calving Cattle, bison and reindeer all seek isolation at calving when they are in an area that has adequate cover (forest, etc.) Without cover they are more likely to calve in the immediate vicinity of the herd- herd protection (Lidfors et. al., 1994) Adaptability of the behavior is beneficial for reducing predation Hide offspring if possible or use the defenses of the herd when unable to hide Also possible that physical separation from the herd helps the cow to bond with her calf without interference from other cows First-calf-heifers are more likely to isolate themselves from the herd than mature cows (Lidfors et al., 1994) Heifers tend to have lower dominance ranks within the herd so they are easily disturbed by older cows and therefore more prone to move away from dominant cows at calving

6. Preparturient Behavior in Ewes Ewes do not show nest-building behaviors However, wild and feral breeds of sheep usually withdraw from the social group a few days before parturition They move to remote and(or) sheltered parts of the home range Some domestic ewes still show reduced levels of this behavior, however they may spend only a few hours away from the flock around parturition

7. Maternal Stress Impacts Chronic stressors cause persistent elevated levels of maternal cortisol which may cross through the placenta Placental CRH plays a vital role in fetal development and parturition, naturally increases over course of gestation Chronically elevated levels may slow fetal growth (resulting in lower birth weight infants) or stimulate preterm birth

8. Maternal Stress and Preterm Births

9. Maternal Stress and Fetal Growth

10. Endocrine Control of Maternal Behavior Onset of maternal behavior ewes depends on exposure to estradiol in late pregnancy and on the vaginocervical stimulation (VCS) that occurs as the lamb is delivered Neither stimulus is effective alone. Treatment of nonparturient ewes with estradiol and progesterone are required for maternal behavior to be induced by artificial VCS Short-latency maternal care in sheep is elicited by central release of oxytocin from the paraventricular nucleus Release of oxytocin is triggered by peripheral sensory response to stretching of the vagina and cervix during birth Both oxytocin release and maternal behavior can be abolished by peridural anesthesia Priming roles of estradiol and progesterone for the onset of maternal behavior is because they increase mRNA expression of oxytocin and its receptor in key brain regions associated with the onset of maternal care and in the periphery

11. Endocrine Control of Maternal Behavior In the sheep (unlike the rat) the expression of maternal behavior is also potentiated by opioids and corticotrophin releasing factor (CRF) Intracerebroventricular morphine treatment increases the peripheral and central release of oxytocin with vaginocervical stimulation and also increases maternal acceptance behaviors Increased expression of maternal behavior induced by intracerebroventricular injections of CRF CRF mRNA expression is elevated in the paraventricular nucleus and BNST of postpartum ewes compared to pregnant or lactating animals Conversely, opioid antagonists prevent increases in oxytocin that normally accompanies vaginocervical stimulation and delay or inhibit appearance of maternal behaviors Precursor genes for opioids (pro-opiomelanocortin and pre-proenkephalin) normally increase in the hypothalamus at parturition and can be influenced by estrogen and progesterone treatment Variation in opioid synthesis and release at parturition may also contribute to individual variation in expression of maternal behaviors in the sheep http://onlinelibrary.wiley.com/doi/10.1111/j.1365-2826.2008.01657.x/full

12. Fetal Behavior

13. Functions of Embryonic and Fetal Behavior Necessary for normal anatomical and physiological development Serves adaptive functions as a behavior Serves as practice for future behavior Is an epiphenomenon of no particular importance

14. How and Where is Embryonic Behavior First Exhibited? Is it myogenic? or… Is it neurogenic/ reflexes? What part(s) of the body move first?

15. Rat Fetal Movement Study Fetal muscular activity is not myogenic and hence must arise from nervous stimulation derived and organized at the spinal level Behavioral repertoire of rat fetuses on Day 17 occurs about the same time that intersegmental spinal reflexes appear and also when other specific receptors are identified during the fetal period including; nerotensin, beta-adrenergic, oxytocin, vasopressin,and muscarinic cholinergic binding sites become active. Behavioral diversity exhibits a monotonic increase from Day 16 through term even though overall activity peaks on Day 18 due to more complex movements and subcategories of the seven basic movement become recognizable as the fetus matures to term.

16. Categories of Fetal Behavior

19. Fetal Yawning

20. More Yawns

21. Somatosensation 7 wkfirst responses to upper lip 8-9 wkperibuccal free nerve endings found 8-9 wk 11 wkface, palmar, plantar 15 wktrunk 13-14 wkwhole body responds Proprioception 20-25 wkvestibular Chemosensation Olfaction 4 wktrigeminal (somatosensation) 11 wkciliated receptors 20-30 wkfunctional olfaction Gustation 12 wktaste buds Audition 4 wkcochlea begins to differentiate 8 wkorgan of Corti begins to develop 18-20 wkorgan of Corti begins to function 20 wkcochlea appears mature 20-25 wkfirst cardiac responses to sound 23-29 wkfirst responses obtained 24-28 wkfirst responses to vibro-acoustic stimuli 27-28 wkfirst responses to pure tones 33 wkinner ear mature Vision 30-32 doptic vesicles form 13 wkrods, cones, begin to form, not complete until after 20 wkeyes open Maturation of Sensory Functions in Humans

22. Birth as a Behavioral “Non-event” Neuro-behavioral systems are functional prior to birth develop in anticipation of need For example, suckling swallowing “respiration” hiccups yawning So, other than constraints imposed by the intra-uterine environment (e.g. fetuses cannot cry without air), there is little behavioral difference between a late-term fetus and a newborn

23. What Distinguishes Newborn From Fetal Behaviors is That They Become Necessary for Survival For example, “breathing” is not functional as respiration in the fetus, but is essential to the newborn How is initiation of breathing assured: 1. Temperature change is a noxious stimulus 2. Anoxia produced by clamping umbilical cord 3. Fluid is expelled from lungs during delivery, the remainder quickly absorbed. Spanking a newborn is not necessary to initiate breathing, and birthing in warm water makes little sense from either a physiological or evolutionary perspective. 4. Changes in other sensory inputs

24. Similarly, suckling and swallowing are essential to the newborn, but have been previously expressed by the fetus So from a neuro-behavioral perspective, birth really is a “non-event,” unlike, for example, amphibian metamorphosis.

25. Neonatal and Fetal Pain Perception Can the fetus feel pain in utero similar to adults? Critical cortico-thalamic connections appear to be present by 24-28 weeks of gestation Suggests that the fetus can potentially feel pain by the third trimester Nociceptive stimuli elicit physiological stress-like responses in the human fetus in utero Physiologic processing of nociceptive stimulus and perceiving a nociceptive stimulus as painful are not the same

26. Fetal & Neonatal Pain Perception There is both a physiological and emotional or cognitive aspect of pain perception Processing can be independent of perception (i.e. surgeries under general anesthesia) Nociceptive stimuli can elicit subcortically mediated physiological stress responses despite unconsciousness To emotionally experience pain, we must be cognitively aware of the stimulus = we must be conscious

27. Fetal & Neonatal Pain Perception Is the fetus ever conscious or aware? Consciousness occurs when all the incoming information from the external and internal environment are available to all parts of the cortex at the same time Sleep is an arousable state of unconsciousness It is possible to be awake and not conscious It is possible to be awake and conscious It is NOT possible to be asleep and conscious No strong evidence that the fetus is ever awake

28. Fetal & Neonatal Pain Perception The fetus is actively kept asleep (unconscious) by a variety of endogenous inhibitory factors: Adenosine (a potent neuroinhibitory and sleep inducing agent) Allopregnanolone and pregnanolone (two neurosteroidal anaesthetics), Prostaglandin D2 (a potent sleep-inducing hormone) A placental neural inhibitor, warmth, buoyancy and cushioned tactile stimulation. Nociceptive pathways are intact from around mid- gestation, however, the critical aspect of cortical awareness in the process of pain perception is missing No direct evidence to suggest subcortical effects of nociceptor input in the fetus can alter neural development and have adverse affects

29. Fetal & Neonatal Pain Perception  Post parturition  Substantial withdrawal of the neuroinhibitors  Adenosine  Involvement of neuroactivators:  Including 17β-estradiol (a potent neuroactive steroid with widespread excitatory effects in the brain), noradrenaline (released from excitatory locus coeruleus nerves that extend throughout the brain),  A barrage of novel sensory information associated with the newborn's first exposure to air, gravity, hard surfaces, unlimited space and, usually, to cold ambient conditions.  Animals must be sentient and conscious for suffering to occur  Consciousness occurs for the first time after birth  Breathing oxygenates the newborn enough to remove the dominant adenosine inhibition of brain function  Newborns that do not breathe will die without suffering  Newborns that do breathe, but not sufficiently to remove adenosine will die without suffering  Most animals become conscious within minutes of birth and have the potential to suffer

30. …parturition is an involuntary process and an involuntary process cannot be helped. The point is not to disturb it.” (Odent, 1987, p. 105)

31. Neonatal Behavior

32. Neonate Behavior Dependent on Level of Consciousness Responsiveness to painful stimuli in anesthetised newborn and young animals of varying neurological maturity (wallaby joeys, rat pups and lambs) Patterns of neurological development, as indicated by electroencephalographic (EEG) activity, are similar in different species EEG activity is absent (isoelectric) initially. Then intermittent spikes followed by longer more sustained epochs separated by isoelectric periods This is followed by a continuous undifferentiated EEG which differentiates into alternating rapid-eye-movement (REM) and non-REM sleep-like patterns Finally, the EEG shows characteristics indicating conscious awareness Timing of these developmental changes depends on neurological maturity of the young at birth

33. Precocial born in a relatively mature state Altricial born in a relatively immature state

34. Neonate Behavior Dependent on Level of Consciousness In wallaby joeys (extremely immature) EEG remains isoelectric until about 100-120 days of in-pouch age and becomes continuous by about 150-160 days, with behavioral signs of conscious awareness apparent by about 160-180 days In rat pups (immature) EEG is isoelectric, intermittent or continuous but undifferentiated at birth with REM/non-REM differentiation occurring between postnatal days 12-18, and conscious awareness appearing no earlier than this In lambs (mature) REM/non-REM differentiation occurs before birth (at 0.8 pregnancy) with conscious awareness appearing only minutes after birth Pain-specific EEG responses of these three species depends on neurological maturity and, in lambs, on proximity to birth Novel implications for pain management of newborn animals Onset of conscious perception does not seem to follow an "on- off" phenomenon Develops gradually, even in species that are neurologically mature at birth

35. 35©2011 The McGraw-Hill Companies, Inc. All rights reserved. Postnatal Scoring Vigor Score Apgar Scale:

36. Modified APGAR for Calves

38. Newborn Piglet Modified APGAR Assessed within one min after birth based on the following variables: Heart rate (beats per min) [less than 120 (bradycardia), between 121 and 160 (normal), and more than 161 (tachycardia)] Latency to breathing (in min) (interval between birth and first breath more than 1 min, between 16 s and 1 min, and less than 15 s) Color of the skin on the snout (pale, pink or cyanotic); latency to standing, measured as the interval between birth and the first time the neonate stands on all four legs (classified as more than 5 min, between 1 and 5 min, and less than 1 min) Skin staining with meconium (severe, mild, or absent) (Zaleski and Hacker 1993; Mota-Rojas et al. 2005) Each one of these variables is assigned a score between 0 (least favorable) and two (most favorable), as well as an overall result ranging from one to 10 that was obtained for each neonate piglet Score below six indicates a failing grade on the vitality scale test

39. Neurologic/Sensory States of Consciousness Deep sleep: no body movements, palms open Light sleep: some body movements Drowsy: startle, eyes open, “no one home” Quiet alert: few movements, intent, focused Active alert: body movements, facial movements, fussy periods Crying: active body movements, eyes open or closed

40. Crying Tears Jerking motions Color in face changes Tight muscles Rapid breathing Generally don’t respond

41. Bleating in Lambs When removed from the ewe and tested in isolation, lambs emit more distress bleats than when paired with a social partner—either their twin (P < 0.01) or an unfamiliar lamb (P < 0.05). Rates of distress bleating by paired unfamiliar lambs were greater than for familiar twins tested together (P < 0.02). The presence of an agemate lamb therefore appears to alleviate, at least to some extent, the stress associated with maternal separation Lower rates of bleating by twin pairs in contrast with paired unfamiliar lambs suggest that twins recognize one another Prior to testing, twins interacted closely and thereby had the opportunity to become mutually acquainted Porter, R.H., 1995. Influence of a conspecific agemate on distress bleating by lambs Applied Animal Behaviour Science Volume 45:239–244

42. Active Alert Lots of body movements Facial movements Fussy periods Eyes open and alert

43. Little body movement Eyes open and wide Steady, regular breathing Highly responsive Wants to learn and play - interactive For young babies, requires active effort to control Quiet Alert

44. Variable movement Irregular breathing Opens and closes eyes Eyes glazed Takes time to react Easily startled Drowsy

45. Moves a little every now and then Irregular breathing Facial twitches Rapid Eye Movements (REM) Easy to wake Light Sleep

46. No body movement Rhythmic breathing Bursts of suckling Startles but does not wake Does not respond Hard to wake Deep Sleep

47. Questions?

48. Behavior is linked to neurologic and sensory cues

49. Human Neurologic/Sensory Periods of Reactivity First Begins at birth Continues for 1 – 2 hours  Alert, good suckle reflex, irregular heart rate and respirations Second Begins around 4 hours  May spit up mucus  Pass meconium  Coordinated, active suckling Equilibrates by 8 hours of age Newborns typically sleep ~17/day in short bursts

50. Neurologic/Sensory Sight Newborns can see Best at about 18 inches Enjoy high contrast (black & white) Will gaze or fix on objects Uncoordinated eye movements May mimic slow, repeating facial movements

51. Sensory and Perceptual Development Vision and Visual Perception –Born with blurry vision –Focusing ability develops by 3 to 4 months –Ability to discriminate between colors improves by 6 months –Infants engage in selective visual attention, and are especially drawn to pictures of their mothers and other human faces –Depth perception develops by about 6 months

52. Neurologic/Sensory Hearing Begins in utero (24 weeks) Enjoys speech cadence Entrainment “baby talk” singsong Teaching Talk to the baby! Watch baby for “I need a break” cues

53. Sensory and Perceptual Development Hearing and Auditory Perception –Acuity of hearing improves so that by 6 months they have well-developed auditory perception –Infants can localize the sources of sounds within the first days of life –Infants are especially attentive to human speech, preferring their mother’s voice

54. Sensory and Perceptual Development Touch, taste and smell are fully operational at birth They discriminate among sweet, salty, sour, and bitter tastes They can distinguish the smell of their mother by 4 months Touch is well developed, even in newborns Newborns also feel pain

55. Neurologic/Sensory Taste Amniotic fluid has taste and baby has been tasting in utero Prefers sweet tastes Suckling is essential Reduces pain and stress Satisfying Nourishment May improve brain neurological development May decrease risk of SIDS

56. Neurologic/Sensory Smell Sense present at birth Newborns can identify their own mother’s breast pads by smell alone Newborns may use smell to help establish nursing Not washing their hands right away

57. Neurologic/Sensory Touch Infants are highly sensitive to touch Startle easily Treat with respect Bonding Touch progression Swaddling Seems to calm some babies

58. Neonatal Stage Learning and Habituation –Learning is readily observable from birth –Infants habituate to their surroundings –Habituation is also used as a research technique Neonatal Assessment –Hospitals perform evaluations to assess neurological and behavioral functioning

59. Sensory and Perceptual Development Infants gradually integrate sensory perceptions—sensory integration They can match a film to its matching soundtrack by 4 months Sensory integration becomes better refined as development proceeds For instance, they can recognize something risky and avoid the danger

60. Types of Infant Cues Young infants try to tell caregivers when they want to interact (engagement cues) Young infants try to tell caregivers when they need to “take a break” or something to be different (disengagement cues) Interactions will have both types of cues, caregivers need to look for pattern Kelly et al. Promoting First Relationships, NCAST Pub 2003

61. Engagement Cues “I want to be near you” Obvious Looking intently at face Rooting Feeding sounds Smiling Smooth body movements Subtle Eyes open Face relaxed Feeding posture Raising head Following voice and face Kelly et al. Promoting First Relationships, NCAST Pub 2003

62. Disengagement Cues “I need a break” Obvious Turns away Pushes, arches away Crying Choking, coughing Extending fingers, stiff hand Falling asleep Subtle Looks away Faster breathing Yawning Hand to ear Grimace Glazed look Kelly et al. Promoting First Relationships, NCAST Pub 2003

63. Clustered Cues: Hunger Clenched fingers and fists over chest and tummy Flexed arms and legs Mouthing Rooting Fast breathing Sucking noises/motions Kelly et al. Promoting First Relationships, NCAST Pub 2003

64. Clustered Cues: Full Arms and legs extended Fingers extended and relaxed Pushing away Falling asleep Slow or decreased sucking Back arching Kelly et al. Promoting First Relationships, NCAST Pub 2003

65. Infant Sleep States Active sleep (REM) is considered to be important for brain development Babies dream and more blood flows to the brain bringing nutrients to active brain cells Images stimulate brain function Peirano et al. J Pediatr 2003; 143: 70-9. Quiet sleep is deep sleep  No dreaming  Little or no movement  Important for the brain to rest  Infants “cycle” through active sleep, quiet sleep, and waking.

66. Infant Sleep Cycles Infant sleep cycles are 60 minutes long (adult cycles are 90 minutes long) Infants sleep 13-14 hours per day from 2-12 months – but not all at once! Initially, newborns will wake with each cycle (every 1-2 hours) Peirano et al. J Pediatr 2003; 143: 70-9 Wake

67. Newborn Sleep/Wake Cycle AS QS Wake Newborns start sleep in Active Sleep (AS) (dreaming for 20-30 mins) and move to Quiet Sleep (QS) Infants in active sleep may wake up easily when put down, because active sleep is a light sleep

68. Circadian Rhythms An internal time-keeping system, the “biological clock” Suprachiasmatic nucleus (SCN) is the site of the master pacemaker controlling circadian rhythms Develops early in gestation Is present in the fetus and newborn Functional rhythms do occur during fetal life The clock of the SCN oscillates with a near 24-hour period Solar day/night is regulated by light

69. Circadian Rhythms 12 hour light cycling conditions influences the repetitive oscillations in hormone levels that are very regular and cycle once every 24 hours Cortisol levels follow the biological clock Cortisol levels ↑ to peak levels at night during rest Cortisol levels continually ↓ during the day

70. Circadian Rhythms Individual components of the circadian system develops postnatally Early postnatal period The developing circadian system is synchronized by maternal cues Disturbing diurnal rhythms do have an effect on developing neonates Constant light trials show that disturbances in biological rhythms and sleep states and inhibition of weight gain and visual development occur Constant light in SOME hospital infant nurseries (24 hour attention) – hospitals have shifted from this paradigm

71. Postnatal Maternal Behavior

72. Maternal vs. Paternal vs. Biparental Environmental demands have played a role in determining parental styles Maternal Behavior – mothers Paternal Behavior – fathers Biparental – both parents Alloparenting - parenting given by individuals that are not the biological mother or father

73. Benefits of Parental Behavior in Animals Ultimate reasons: passing on genes Proximal reasons: protection nutrition temperature regulation shelter learning (instincts)

74. Benefits of Parental Behavior in Humans Evidence suggests that early life environment (parental care) is important for development 30% of mothers who were abused, abuse their own babies 5% who were not abused, abuse their own babies (Knutson, 1995) Sensitive mother - securely-attached infant (Goldberg) Securely-attached infant--- relationally-secure adult (Waters et al., 2000)

75. Maternal Behavior Any behavior that contributes directly to the survival of offspring that have left the body of the female (Nelson, 2005) Sensitization/ concaveation: process whereby continuous exposure to young pups can induce maternal responsiveness in non-lactating female rodents (Rosenblatt, 1967)

76. PATERNAL BEHAVIOUR Reversed roles: highly advanced paternal care examples: pipefish seahorse stickleback fish

77. BI-PARENTAL CARE Both parents contribute to raising the offspring Examples: Penguins Ring doves California mice Voles Marmoset monkeys Humans

78. Differences Between Species in the Amount of Care Provided

79. Different Types of Maternal Care in Eutherian Mammals Precocial Born at an advanced stage of development Little or no help is required for survival ex. lambs, other ungluates Hider-type vs. follower-type Altricial Born at an early stage of development. Helpless  require substantial parental care to survive ex. Dogs, rats, rabbits Third type - can also be semi-precocial/semi-altricial; ex. humans and other primates

80. Maternal Behavior in Humans Many cultural differences – no clear set of maternal behaviors Affectionate behaviors: patting, cuddling and kissing etc. Instrumental behaviors: changing diapers, changing the clothing and burping the infant etc.

81. Sensory Changes in New Mothers Compared to non-mothers, new mothers find odors associated with infants more pleasing (or less aversive): general body odor, urine and feces New mothers are good at identifying the odor, cries and tactile features of their infant

82. Description of Rat Maternal Behavior Nest building Pup retrieval Pup licking Nursing postures Normally these behaviors are evident soon after parturition Rats that have never given birth (nulliparious or virgins) do not show these behaviors

83. Hormones and Behavior Hormones modulate behavior Hormones can be necessary for a behavior A particular level of hormone in an animal does not ensure a behavior will occur. A particular level of hormone does not have the same effect in every animal.

84. The Onset of Maternal Behavior HIGH LOW Virgin / onset of pregnancy Day 16 parturition

85. Pregnancy and Parturitional Endocrine Profile

86. Parabiotic Preparation Preparation where blood is exchanged between a rat that was maternal and a rat that was not maternal Soon after exchange, virgin rat will exhibit maternal behavior Conclusion: blood- borne factor is important in the induction of maternal behavior in rats

87. 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

88. Mothers with an increased ratio of estradiol to progesterone show more positive attachment to their infants than mothers whose pregnancy endocrine profile shows a negative shift (or no change) Maternal Behavior in Humans – Hormones: Estradiol and Progesterone

89. Latency to Become Maternal After Hormonal Treatment - + - Bridges,1984

90. Social Attachment - Sheep 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 administration of prolactin does not stimulate maternal behavior in sheep

91. Social Attachment – Oxytocin and Vasopressin Development of a “social bond” between individuals A social bond can form between a mother and her offspring Sheep (ewe and lamb) - ewes 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. prairie vole--monogamous species - one male pairs with one female often for life they engage in biparental care and show aggression against intruders montane vole--polygamous species - males and females pair repeatedly with different members of their species, with females providing 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

92. Social Attachment - Sheep Gonadal steroids and vaginocervical stimulation (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 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

93. 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 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 oxytocin 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

94. 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

95. 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

96. Oxytocin Numan & Insel (2003)

97. Social Attachment - Humans Role of hormones 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? Not currently clear, but recent studies do not point to a strong relationship in humans

98. Social Attachment - Humans Probable that“social bonds” and the display of parental behavior in humans is not coupled in any simple way to changes in levels of hormones 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... Current hypothesis: Hormones can alter human behavior, however, effects are more subtle than those observed in lower mammals and affected by other processes--e.g., conscious choice

99. Other Hormones – Glucocorticoids (Corticosterone) Moderate increases in corticosterone facilitates maternal pup licking in rats

100. Like other motivated behavior, maternal behavior is dependent on the hypothalamus Specifically, medial preoptic area (MPOA) of the hypothalamus is the most important nucleus for maternal behavior Lesions of MPOA will abolish maternal behavior Neural Circuitry of Maternal Behavior

101. Cortical lesions do not significantly impact maternal behavior Amygdala inhibits the activity/behavior produced by the MPOA Multiple sources of evidence: electrolytic lesions destroy all the tissue (cell bodies and axons)

102. QUESTIONS??

103. Vasopressin Gene sequences on alleles may predict behavior AVPR1a – Gene that codes for vasopressin receptor Longer alleles (repeat of sequence) more monogamous behavior – voles Similar sequence may predict success of opposite success relationships in humans (Walum et al., 2008)

104. Oxytocin and Vasopressin Neurons - Production Oxytocin and vasopressin can be released directly circulation and directly into the brain Peripheral versus central release OT and AVP receptors are localized in the limbic system

105. Oxytocin Receptor Oxytocin receptor: membrane-bound G-protein coupled receptor that along with the 3 vasopressin receptors form the OT-AVP receptor family Oxytocin receptors: in uterus, kidney, and brain Facilitation of maternal behavior requires increase in central rather than peripheral oxytocin Oxytocin’s effects require estrogen priming

106. Oxytocin and Social Behaviors Oxytocin can be released during social interactions pair bonding and sex mother – infant bonding Birth – uterine contractions Suckling - lactation Although oxytocin is measured in the blood, it can be directly released in the brain

107. Maternal care in horses

108. First mare-foal interaction Gestation: 315-365 days (average=340) Parturition = act of giving birth After parturition: Mare licks fetal membranes = Process to become familiar rather than cleaning Olfactory cues !!! Primary socialization established within 2 hrs. Separation  extreme anxiety + disorientation by the foal

109. First mare-foal interaction (cont.) Foal develops motor/auditory/tactile skills fast Foal initially follows any large object Gradually learns ‘correct object’ First nursing attempt after standing: Standing: within 60, up to 120 minutes after birth  Fillies vs. Colts Nursing: 30 – 120 minutes after birth ‘air sucking’ Nursing position = reverse parallel Bunting

110. Indicators of maternal care 1. Proximity Distance between mare and foal On pasture < 5 m on day 1 Due to foal behavior, even when lying down Very little physical contact Recumbency response: “when her foal lies down, the mare stops engaging in any other activity and stays near her young, by instinct on alert for predators, even though there may be no such dangers anywhere near” Trends with age

111. Indicators of maternal care (cont.) 2. Nursing Definitions (research-based): 1979: The time a foal first nuzzled the mare’s udder for 3 seconds until the final time the foal removed its head from the medial side of the mare’s hind limb 1980-81: Start of a nursing bout was recorded when the foal actually sucked for the first time 1983: A period of nursing activity delimited by intervals of non-nursing activity lasting for  27 secs

112. Indicators of maternal care (cont.) Definitions (cont.): 1992: Including pre-nurse nuzzling, sucking, intra- bout pauses and intra-bout nuzzling 1994: Including pre-suck nuzzle, pre-suck pause, suck, intra-suck nuzzle and intra-suck pause

113. Indicators of maternal care (cont.) Functions of nursing: Nourishment Initial passive transfer of immunity (Colostrum) Comfort Behavior

114. Indicators of maternal care (cont.) Nursing Behavior Initiation of nursing : By mare By foal  Crossing the bow

115. Indicators of maternal care (cont.) Nursing Behavior Nursing bout frequency and duration Frequency (per hour) Belgian draft horses 9 Draft + mule foals 14 Welsh ponies 4 Duration: 78 – 84 seconds

116. Indicators of maternal care (cont.) Nursing bout termination Constant individual differences between foals Mares < Foal Termination by foal: Remove head from udder Walk away Termination by mare (Welsh ponies): Walk away Kick at abdomen Lift hind limb to obstruct nursing Direct aggression against foal

117. Indicators of maternal care (cont.) 3. Aggression Rare during first month; nursing related Different forms: Laying back of ears Bite threat Bite Kick threat Kick Squeal Bunt Tail swish

118. Indicators of maternal care (cont.) Response from foal No discernable response Short pause in nursing Aggressing back at the mare

119. Indicators of maternal care (cont.) 4. Other interactions Mutual grooming = Reciprocal coat care in which the partners nuzzle and chew on one another’s coat Fillies (  ) groom about twice as much as colts (  ) do

120. Indicators of maternal care (cont.) 4. Other interactions Play 3 major types of play: general motor, interactive, and object manipulation In stall: foal explores environment by mouthing parts of stall, mare’s tail/ear/halter On pasture: Galloping away from the mare in what appears to be thrill-seaking behavior