Perinatal Behavior
Amanda Robinson
Lesson Plan
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Day 1
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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
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Day 2
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Postnatal Maternal Behavior
 Normal behavior in
production animals
 Endocrine control of
behavior
Prenatal Maternal
Behavior
Preparturient Behavior in Cattle
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Maternal behavior actually begins prior to calving
Cows demonstrate some tendencies to select a birth site
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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)
Preparturient Behavior in Cattle
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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
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Cattle, bison and reindeer all seek isolation at calving when they
are in an area that has adequate cover (forest, etc.)
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depends on age of the female and the environmental conditions
Cows appear to adjust their behavior to the conditions present at calving
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
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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
Preparturient Behavior in Ewes
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Ewes do not show nest-building behaviors
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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
Maternal Stress Impacts
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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
Maternal Stress and Preterm Births
Maternal Stress and Fetal Growth
Endocrine Control of Maternal
Behavior
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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
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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
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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
Endocrine Control of Maternal
Behavior
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In the sheep (unlike the rat) the expression of maternal behavior is
also potentiated by opioids and corticotrophin releasing factor (CRF)
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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
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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
Fetal Behavior
Functions of Embryonic and
Fetal Behavior
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Necessary for normal anatomical and
physiological development
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Serves adaptive functions as a behavior
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Serves as practice for future behavior
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Is an epiphenomenon of no particular
importance
Categories of Fetal Behavior
The Appearance of Fetal Movements in Early Pregnancy
Movement
Gestation of First Appearance (wks)
Heartbeat
6
Any movement (lateral head movement) 7
Startle
8
Generalized movements
8
Hiccups
8
First cutaneous sensitivity (cheek)
8
Isolated arm movements
9
Head retroflexion
9
Hand-face contact
10
Breathing
10
Jaw opening
10
Stretching
10
Head anteflexion
10
Swallow
10
Cutaneous sensitivity (palms)
11
Yawn
11
Suck
12
Cutaneous sensitivity (soles)
12
From De Vries et al. (1982). The emergence of fetal behaviour. I. Qualitative aspects.
Early Hum Dev; 7: 301-22
Fetal
Yawning
More
Yawns
Maturation of Sensory Functions in Humans
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Somatosensation
7 wk
8-9 wk
11 wk
15 wk
13-14 wk
first responses to upper lip
peribuccal free nerve endings found 8-9 wk
face, palmar, plantar
trunk
whole body responds
20-25 wk
vestibular
4 wk
11 wk
20-30 wk
trigeminal (somatosensation)
ciliated receptors
functional olfaction
12 wk
taste buds
4 wk
8 wk
18-20 wk
20 wk
20-25 wk
23-29 wk
24-28 wk
27-28 wk
33 wk
cochlea begins to differentiate
organ of Corti begins to develop
organ of Corti begins to function
cochlea appears mature
first cardiac responses to sound
first responses obtained
first responses to vibro-acoustic stimuli
first responses to pure tones
inner ear mature
30-32 d
13 wk
20 wk
optic vesicles form
rods, cones, begin to form, not complete until after
eyes open
Proprioception
Chemosensation
Olfaction
Gustation
•
•
Audition
Vision
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
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.
4. Changes in other sensory inputs
• Spanking a newborn is not necessary
to initiate breathing, and birthing in warm
water makes little sense from either a
physiological or evolutionary perspective.
• 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.
Neonatal and Fetal Pain Perception
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Can the fetus feel pain in utero similar to adults?
Critical cortico-thalamic connections appear to be
present by 24-28 weeks of gestation
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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
Fetal & Neonatal Pain Perception
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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
Fetal & Neonatal Pain Perception
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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
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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
Fetal & Neonatal Pain Perception
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The fetus is actively kept asleep (unconscious) by a
variety of endogenous inhibitory factors:
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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 midgestation, 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
Fetal & Neonatal Pain Perception
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Post parturition
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Substantial withdrawal of the neuroinhibitors
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Involvement of neuroactivators:
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Adenosine
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
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Consciousness occurs for the first time after birth
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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

…parturition is an involuntary process and an
involuntary process cannot be helped. The
point is not to disturb it.” (Odent, 1987, p.
105)
Neonatal Behavior
Neonate Behavior Dependent
on Level of Consciousness
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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
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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
Precocial
born in a
relatively mature
state
Altricial
born in a
relatively immature
state
Neonate Behavior Dependent
on Level of Consciousness
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In wallaby joeys (extremely immature)
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In rat pups (immature)
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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
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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)
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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
Novel implications for pain management of newborn animals
Onset of conscious perception does not seem to follow an "onoff" phenomenon
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Develops gradually, even in species that are neurologically mature at birth
Postnatal Scoring Vigor Score
Apgar Scale:
©2011 The McGraw-Hill Companies, Inc. All rights
reserved.
35
Modified APGAR for Calves
Newborn Piglet Modified APGAR
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Assessed within one min after birth based on the following variables:
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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
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Score below six indicates a failing grade on the vitality scale test
Neurologic/Sensory
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States of Consciousness
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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
Crying
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Tears
Jerking motions
Color in face
changes
Tight muscles
Rapid breathing
Generally don’t
respond
Bleating in Lambs
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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
Active Alert
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Lots of body movements
Facial movements
Fussy periods
Eyes open and alert
Quiet Alert
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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
Drowsy
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Variable movement
Irregular breathing
Opens and closes
eyes
Eyes glazed
Takes time to react
Easily startled
Light Sleep
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Moves a little
every now and
then
Irregular breathing
Facial twitches
Rapid Eye
Movements (REM)
Easy to wake
Deep Sleep
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No body movement
Rhythmic breathing
Bursts of suckling
Startles but does
not wake
Does not respond
Hard to wake
Questions?
Behavior is linked to
neurologic and sensory cues
Human Neurologic/Sensory
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Periods of Reactivity
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First
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Begins at birth
Continues for 1 – 2 hours
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Second
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Begins around 4 hours
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Alert, good suckle reflex, irregular heart rate and respirations
May spit up mucus
Pass meconium
Coordinated, active suckling
Equilibrates by 8 hours of age
Newborns typically sleep ~17/day in short bursts
Neurologic/Sensory
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Sight
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Newborns can see
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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
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
Neurologic/Sensory
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Hearing
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Begins in utero (24 weeks)
Enjoys speech cadence
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Entrainment
“baby talk” singsong
Teaching
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Talk to the baby!
Watch baby for “I need a break” cues
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
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
Neurologic/Sensory
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Taste
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Amniotic fluid has taste and baby has been
tasting in utero
Prefers sweet tastes
Suckling is essential
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Reduces pain and stress
Satisfying
Nourishment
May improve brain neurological development
May decrease risk of SIDS
Neurologic/Sensory
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Smell
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Sense present at birth
Newborns can identify their own mother’s breast
pads by smell alone
Newborns may use smell to help establish nursing
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Not washing their hands right away
Neurologic/Sensory
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Touch
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Bonding
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Infants are highly sensitive to touch
Startle easily
Treat with respect
Touch progression
Swaddling
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Seems to calm some babies
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
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
Infant Sleep States

Active sleep (REM)
is considered to be
important for brain
development
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Babies dream and
more blood flows to
the brain bringing
nutrients to active
brain cells
Images stimulate
brain function
• Quiet sleep is
deep sleep
No dreaming
 Little or no movement
 Important for the brain
to rest

Peirano et al. J Pediatr 2003; 143: 70-9.
 Infants “cycle” through active sleep, quiet sleep, and waking.
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
Newborn Sleep/Wake
Cycle
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
Circadian Rhythms
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An internal time-keeping system, the “biological clock”
Suprachiasmatic nucleus (SCN) is the site of the master
pacemaker controlling circadian rhythms
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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
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

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Cortisol levels ↑ to peak levels at night during rest
Cortisol levels continually ↓ during the day
Circadian Rhythms

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Individual components of the circadian system develops
postnatally
Early postnatal period
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The developing circadian system is synchronized by maternal
cues
Disturbing diurnal rhythms do have an effect on
developing neonates
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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
Postnatal Maternal
Behavior
Maternal vs. Paternal vs.
Biparental
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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
Benefits of Parental
Behavior in Animals
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Ultimate reasons: passing on
genes
Proximal reasons:
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protection
nutrition
temperature regulation
shelter
learning (instincts)
Benefits of Parental
Behavior in Humans
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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)
Maternal Behavior

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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)
PATERNAL BEHAVIOUR

Reversed roles:
highly advanced
paternal care
examples:
 pipefish
 seahorse
 stickleback fish
BI-PARENTAL CARE
Both parents contribute
to raising the offspring
Examples:
 Penguins
 Ring doves
 California mice
 Voles
 Marmoset monkeys
 Humans

Differences Between Species
in the Amount of Care
Provided
Different Types of Maternal
Care in Eutherian Mammals
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Altricial
Born at an early stage of
development.
Helpless  require substantial
parental care to survive
ex. Dogs, rats, rabbits
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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
Third type - can also be semi-precocial/semi-altricial; ex. humans
and other primates
Maternal Behavior in Humans
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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.
Sensory Changes in New Mothers

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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
Description of Rat Maternal
Behavior
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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
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.
The Onset of Maternal
Behavior
HIGH
parturition
LOW
Virgin / onset of pregnancy
Day 16
Pregnancy and Parturitional
Endocrine Profile
Parabiotic Preparation
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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: bloodborne factor is
important in the
induction of maternal
behavior in rats
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
Maternal Behavior in Humans –
Hormones: Estradiol and
Progesterone

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)
LATENCY IN DAYS (median)
Latency to Become Maternal
After Hormonal Treatment
10
9
8
7
6
5
4
3
2
1
0
+ Estrogen and
- progesterone
-
Progesterone
Control-vehicle
Hormone Treatment
Bridges,1984
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
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
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
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
Sensory
Receptors
Olfactory
Bulbs
PVN
+
+
oxytocin
lamb
odors
Secondary
Olfactory
Structures
Tertiary
Olfactory
Structures
NE
Locus
Coeruleus
Formation of an
Olfactory Memory
Secondary structures: amygdala & piriform cortex
Tertiary structures: orbitofrontal cortex, entorhinal cortex, hippocampus, septum
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
Oxytocin
Numan & Insel (2003)
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
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
Other Hormones –
Glucocorticoids
(Corticosterone)
Moderate
increases in
corticosterone
facilitates
maternal pup
licking in rats
160
140
Duration (mean sec)

120
100
80
60
40
20
0
0ug
25ug
100ug
CORTICOSTERONE (ug/ml)
300ug
Neural Circuitry of Maternal
Behavior



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



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)
QUESTIONS??