Chp 8: Hormone-Behavior Relations in the Regulation
of Parental Behavior
Overview:
•
Parental behavior evolved to supplement physiological mechanisms of
reproduction--increasing the likelihood that the offspring will survive.
•
Different patterns of parental behavior
•
In females, hormones of pregnancy synchronize several events:
– reproductive tract: stimulate uterine contractions (parturition or childbirth)
– mammary gland: stimulate production and secretion of milk (lactation)
– central nervous system: stimulate parental behavior
•
In males, hormonal changes are not strongly linked to parental responses
•
Consider two main examples in detail:
– hormones, pregnancy and parental behavior in the female rat
– hormones and parental behavior in male and female ring doves
•
Link: oxytocin--maternal behavior--social bonds
Hormonal Regulation of Parental Behavior
Parental behavior varies in different species:
Species exhibiting oviparity (egg laying):
•
Ex: birds, reptiles, fish
•
parental behavior involves:
– laying eggs (and building nests)
– incubating eggs until they hatch
– brooding--care of hatchlings by providing warmth, feeding and protection
Species exhibiting viviparity (birth of live young):
•
Ex: rats, mice, horses, primates (humans)
•
parental behavior involves:
– care of the young at the time of birth--warmth, feeding (nursing), protection
Hormonal Regulation of Parental Behavior
Three main patterns of parental behavior based on developmental status of young:
Nesting Pattern:
•
species with altricial newborn: young that are very immature at birth--cannot
see, hear or move well, nor regulate their body temperature or feed themselves
•
require extended parental care (prolonged care in nests)
•
Avian species: robins, pigeons, doves
– parental care involves building nests, feeding, warmth, protection (aggression toward
intruders)
– 80% of all bird species are altricial
•
Mammalian species: rats, rabbits, cats
– parental care involves building nests, feeding (nursing), licking to stimulate waste
elimination, pup retrieval, and protection
Hormonal Regulation of Parental Behavior
Three main patterns of parental behavior based on developmental status of young:
Leading-Following Pattern:
•
species with precocial newborn: young that are quite mature at birth--young
have vision, hearing, locomotive ability, and the ability to achieve
thermoregulation
•
parental care is limited--young depend on mother for food (may include nursing)
and protection, but soon after birth young can feed themselves
•
in many instances, the mother leads the young who follow her
•
Avian species: chickens and ducks (10% avian species)
•
Mammalian species: ungulates (sheep, cows), guinea pigs, whales
Hormonal Regulation of Parental Behavior
Three main patterns of parental behavior based on developmental status of young:
Clinging-Carrying Pattern:
•
species with semialtricial/semiprecocial newborn: young are considered
“intermediate” in development compared to altricial and precocial species;
typically, young can hear and see, but require assistance in locomotion
•
parental care involves transportation (young will cling to mother or be carried by
her), feeding (nursing), thermoregulation and protection
•
Avian species: gulls and terns (10% avian species)
– nestbuilding is minimal, young are fairly mobile and parents feed young special food
which is often regurgitated
•
Mammalian species: most primate species (including humans)
Hormonal Regulation of Parental Behavior
What role do hormones play in parental behavior?
•
female rat as a model
Broad overview:
•
events that occur with mating, fertilization and the start of pregnancy
•
events that occur during pregnancy (22 gestation period in the rat)
•
events that occur at the end of pregnancy:
– parturition
– lactation
– maternal behavior
– aggressive behavior
– postpartum estrus
Female Rat is a Spontaneous Ovulator:
GnRH Neuron
HYPO
Ovulation:
• as follicles develop in ovary
+
GnRH
GnRH
surge
ANT
PIT
– in female rats, increases in
estrogen lead to a GnRH
surge (positive feedback)
FSH
LH
follicle
LH surge
– increasing levels of estrogen
are released
estrogen
OVARY
– GnRH surge leads to LH
surge
– LH surge leads to ovulation
“ovulation”
GnRH: gonadotropin-releasing hormone
FSH: follicle stimulating hormone
LH: luteinizing hormone
Formation of the Corpus Luteum
Not Spontaneously Functional:
•
corpus luteum will not form unless
female engages in copulation
– Ex: rats
•
•
•
critical stimulus--vaginocervical
stimulation (e.g., intromissions)
insertion of penis into vagina by
male during mating will stimulate a
neuroendocrine reflex in the female
leading to release of PRL which
then acts to form the corpus luteum
corpus luteum will secrete
progesterone
PRL Neuroendocrine Reflex
PRF Neuron
HYPO
+
PRF
ANT
PIT
PRL
spinal cord
follicle
egg
OVARY
vaginocervical
stimulation
“corpus luteum”
forms
PRF: prolactin releasing factor
PRL: prolactin
progesterone
Female Rat as a Model
Events that occur with mating, fertilization and the start of pregnancy:
•
a female rat has gone through a spontaneous estrous cycle
– increased estrogen lead to a GnRH surge, LH surge and ovulation
– increased estrogen followed by a preovulatory rise in progesterone stimulated
proceptive and receptive behaviors--female mated with a male rat (multiple eggs are
released and fertilized by sperm leading to development of several embryos)
•
intromissions associated with mating activated a neuroendocrine reflex leading
to formation of the corpus luteum
– prolactin maintains the corpus luteum
– LH stimulates production of progesterone from corpus luteum (smaller amounts of
estrogen)
– estrogen: important for preparing uterus for implantation
– progesterone: important for implantation of embryo into uterine wall and
maintenance of pregnancy
Female Rat as a Model
Events that occur with mating, fertilization and the start of pregnancy:
•
a placenta will be formed between each developing embryo and will become
embedded into wall of uterus
•
placenta is a high vascularized
organ that allows nutritive
substances and gases in
mother’s blood to diffuse to
MOM
embryo
nutrients
gases
embryo and a mechanism for
metabolic
waste
products
metabolic wastes to leave
developing embryo
•
placenta can also produce
hormones
placenta
Female Rat as a Model
Events that occur during pregnancy:
•
pregnancy lasts approximately 22 days in the rat (gestational period)
•
progesterone: levels rise shortly after mating and are elevated throughout
pregnancy until near parturition (end of pregnancy)
•
estrogen: levels are relatively low during first half of pregnancy, but rise
significantly during the second half of pregnancy
•
midway through pregnancy (days 12-13), regulation of ovarian hormone
secretion switches from Mom’s anterior pituitary to the placenta
– LH (released from Mom’s pituitary) is replaced by chorionic gonadotropin
– PRL (released from Mom’s pituitary) is replaced by placental lactogen
– species differences in terms of when, and if, this switch takes place (summarized in
Table 8.1)
Female Rat as a Model
1
1st Half
12
2nd Half
22
Placenta
OVARY
LH
Mom’s
Anterior
pituitary
PRL
follicle
egg
“corpus luteum”
progesterone
(estrogen)
chorionic
gonadotropin
placental
lactogen
gonadal
steroids
Female Rat as a Model
Events that occur during pregnancy:
•
mammary glands must develop to provide milk for nursing (lactation)
•
full development of the mammary glands requires hormones and stimulation of the
nipples and genital region
•
hormonal control:
– progesterone stimulates proliferation of secretory cells located in the alveoli of mammary
gland
– estrogen stimulates duct development (carry milk from secretory cells to nipple)
– prolactin (placental lactogen) stimulates synthesis of milk by secretory cells
– at parturition, with nursing of young, oxytocin (from Mom’s posterior pituitary) will
stimulate release of milk (milk-letdown)
– at parturition, with nursing of young, prolactin (from Mom’s anterior pituitary) will rise
and stimulate milk synthesis
Female Rat as a Model
Events that occur during pregnancy:
•
somatosensory control:
– during pregnancy, the female rat will lick her ventral body region (nipples and genital
region)
– this sensory input is critical for normal development of mammary glands
– Exp. #1: if you block the ability of a female to lick her ventral region by fitting her with
a collar so that she can’t lick her body, mammary development will be significantly
impaired (50% of normal development on day 21)
– Exp. #2: if you take another group of collared females (that cannot lick themselves), and
stimulate them with a brush along the nipples and genital region, you can stimulate full
mammary development
Female Rat as a Model
Events that occur at the end of pregnancy:
•
levels of progesterone drop
•
levels of estrogen remain elevated
•
levels of prolactin rise
•
These hormonal events (and others) signal the end of pregnancy, initiate labor
(parturition), and initiate maternal behavior and maternal aggression.
•
In addition, the process of giving birth--uterine-cervical-vaginal stimulation-stimulates postpartum estrus:
•
8-11 hours after parturition, females will be sexually receptive and will mate
•
18 hours after parturition, ovulation occurs and the female can become pregnant
(although implantation is delayed while female engages in nursing)
Female Rat as a Model
Maternal Behavior:
•
4 components of maternal behavior in the female rat:
– nestbuilding
– pup licking
– nursing
– pup retrieval
•
maternal behavior increases gradually during 2nd half of pregnancy--all components
of behavior can be seen 24-48 hours prior to parturition
•
maternal behavior lasts for 3-4 weeks
Female Rat as a Model
Maternal Aggression:
•
aggression displayed toward other adults viewed as “ intruders”
– When an intruder comes near the nest, the mother will approach and sniff the intruder and
then launch an attack that is aimed at the intruder’s neck and head region. The female
bites at the neck of the intruder, climbs its back and pins it in place. The intruder usually
will flee, but if escape is not possible, the intruder will become immobile and may turn
over on its back--freezing and submissive behavior usually terminates the female’s
aggression, although repeated attacks can occur.
•
aggressive behavior protects newborn from attacks and cannibalism
•
increases gradually during 2nd half of pregnancy--high levels of aggression seen 24-
48 hours prior to parturition
•
maternal aggression also lasts for 3-4 weeks
Female Rat as a Model
Hormones have two main effects on processes associated with pregnancy:
•
hormonal “priming”--action of one or several hormones that prepare the way for
subsequent hormones to produce their effects
– elevations in estrogen and progesterone during pregnancy set the stage for elevated levels
of estrogen to stimulate several events at parturition
•
hormonal “triggering”--action of estrogen in triggering or stimulating several
events at the time of parturition
– estrogen levels are elevated while progesterone levels drop
– estrogen acts to stimulate: maternal behavior, aggressive behavior, sex behavior, uterine
contractions and lactation
– estrogen’s actions involve several processes: 1) increased expression of the estrogen
receptor, 2) increased expression of receptors for other hormones, 3) increased synthesis
and release of other hormones
Female Rat as a Model
hormonal “priming”
•
elevations in estrogen and progesterone during pregnancy stimulate the expression of
estrogen receptors within MPOA (but not within hypothalamus!)
– estrogen receptors within the MPOA reach “peak” levels by day 13 of pregnancy and
remain elevated through day 22 (parturition)
– replicate finding--pretreatment of nonpregnancy females with estrogen and progesterone
for 16 days can elevate estrogens receptors within MPOA
•
the “priming” effect of estrogen and progesterone on estrogen receptors within
MPOA is thought to be important for the rapid onset of maternal behavior
– MPOA is important for maternal behavior--lesioning MPOA will block maternal
responses
– estrogen implants in MPOA (in addition to elevated levels of progesterone) can stimulate
maternal behavior in nonpregnance female rats
Female Rat as a Model
hormonal “triggering”
•
estrogen levels are elevated while progesterone levels drop
•
drop in progesterone allows estrogen to stimulate several processes:
– maternal behavior
– sex behavior
– uterine contractions
– lactation
•
estrogen’s actions involve several processes:
– increased expression of the estrogen receptor (ER)
– estrogen--ERs-->increased expression of receptors for other hormones: oxytocin
receptors, prostaglandin receptors, prolactin receptors
– estrogen--ERs-->increased synthesis and release of other hormones: oxytocin, prolactin
Female Rat as a Model
hormonal “triggering”
myometrium
of uterus
pregnancy
parturition
progesterone
inhibits
uterine
contractility
drop in
progesterone
stimulates
uterine contractility
delivery
of
fetus
Female Rat as a Model
hormonal “triggering”
myometrium
of uterus
drop in
progesterone
oxytocin stimulates
uterine contractility
(posterior pituitary)
prostaglandins stimulates
uterine contractility
(uterus)
estrogen increases ERs in uterus;
estrogen-ERs leads to:
increase in oxytocin
receptors in uterus
increase in prostaglandin
receptors in uterus
Female Rat as a Model
hormonal “triggering”
lactation
pregnancy
parturition
progesterone
inhibits
release of
prolactin &
oxytocin
into
bloodstream
increased
release of
prolactin &
oxytocin
nursing
hormonal “triggering”
drop in progesterone
HYPOTHALAMUS
estrogen increases in ERs in
neurons in hypothalamus;
estrogen-ERs leads to:
PRF Neuron
Oxytocin Neuron
PRF
stimulates release of
prolactin from anterior
pituitary and oxytocin
from posterior pituitary
prolactin acts to stimulate
milk synthesis while
oxytocin acts to stimulate
milk letdown (release)
PITUITARY
Anterior
Posterior
oxytocin
PRL
MAMMARY
GLAND
Female Rat as a Model
hormonal “triggering”
female sex
behavior
pregnancy
parturition
progesterone
inhibits
display of
female sex
behavior
(inhibitory part
of the biphasic
action of
progesterone--due
to prolonged
exposure)
display of
postpartum
estrus
continuation
of
reproductive
activities
Female Rat as a Model
hormonal “triggering”
female sex
behavior
drop in
progesterone
increase in ERs in VMH
estrogen-ERs leads to:
display of
proceptive
and
receptive
behaviors
if a male
is present
Female Rat as a Model
hormonal “triggering”
maternal
behavior
pregnancy
parturition
maternal behavior
develops gradually
during gestation,
and is present
24-48 hrs
prior to parturition;
high levels of
progesterone inhibit
rapid display of
maternal behavior
just prior to, and
immediately after,
parturition
female shows
maternal behavior
(rapid onset)
survival
of
offspring
hormonal “triggering”
drop in progesterone
estrogen increases ERs in
neurons in MPOA &
hypothalamus;
estrogen-ERs leads to:
+
HYPO
increased release of PRL into
blood and brain, increased
expression of PRL-Rs in
MPOA, and maternal behavior
E
MPOA
PRF Neuron
E
Maternal
Behavior
Oxytocin Neuron
E
PRF
PITUITARY
Anterior
prolactin acts at PRL-Rs
in MPOA to stimulate
maternal behavior
synergism between estrogen &
PRL--1) PRL can stimulate
ERs in MPOA, and
2) estrogen can increase PRL-Rs
and PRL release in MPOA
?
Posterior
oxytocin
PRL
MAMMARY
GLAND
Female Rat as a Model
2 phases to maternal behavior:
•
hormonal phase:
– decrease in progesterone, increase in prolactin with elevated levels of estrogen
– hormonal changes are important for the initiation of maternal behavior
– however, once maternal behavior has been initiated, removal of the ovaries, adrenal gland,
pituitary and placenta will not affect behavior (i.e., removal of gonadal steroids and
peptide/protein hormones present within bloodstream)
•
nonhormonal phase:
– a transition occurs in which maintenance of maternal behavior depends on stimuli
received from young (pups): suckling by pups at nipple, visual stimuli, auditory stimuli
(crying)
– neurocircuits within the brain that process somatosensory, visual, auditory information can
feed into, and stimulate, neurons within MPOA to stimulate maternal behavior
•
transition period last approximately one week following parturition
OLD SLIDE: hormonal “triggering”
drop in progesterone
estrogen increases ERs in
neurons in MPOA &
hypothalamus;
estrogen-ERs leads to:
+
HYPO
increased release of PRL into
blood and brain, increased
expression of PRL-Rs in
MPOA, and maternal behavior
E
MPOA
PRF Neuron
E
Maternal
Behavior
Oxytocin Neuron
E
PRF
PITUITARY
Anterior
prolactin acts at PRL-Rs
in MPOA to stimulate
maternal behavior
synergism between estrogen &
PRL--1) PRL can stimulate
ERs in MPOA, and
2) estrogen can increase PRL-Rs
and PRL release in MPOA
?
Posterior
oxytocin
PRL
MAMMARY
GLAND
NEW SLIDE: hormonal “triggering”
drop in progesterone
estrogen increases ERs in
neurons in MPOA &
hypothalamus;
estrogen-ERs leads to:
MPOA
increased synthesis and release
of PRL into blood and brain, and
stimulation of maternal behavior
HYPO
E
+
?
Maternal
Behavior
E
PRL Neuron
PRF Neuron
E
Oxytocin Neuron
E
PRF
prolactin acts at PRL-Rs
in MPOA to stimulate
maternal behavior
(rapid onset)
synergism between estrogen & PRL
1) PRL may enhance interaction
of estrogen to its receptor,
2) estrogen can increase PRL
synthesis and release
PITUITARY
Anterior
Posterior
oxytocin
PRL
MAMMARY
GLAND
Interaction Between Estrogen and Prolactin
Estrogen and prolactin both act to facilitate maternal behavior at the level of the MPOA.
How does this occur?
•
Prolactin can enhance interaction of estrogen with its receptor
– Ex. Mammary gland
– prolactin changes the form of the estrogen receptor within cytoplasm
– 4S receptor is found in the unstimulated tissue, while 8S receptor is observed following
administration of hormone; 8S form shows increased binding of estrogen
– prolactin changes the form of the estrogen receptor: 4S-->8S (in cytoplasm); thus,
prolactin increases “sensitivity of ERs to estrogen” by changing the form of the receptor
(can be thought of as increasing the number of “functional” ERs)
– estrogen then binds to ER and stimulates its translocation from the cytoplasm to the
nucleus; estrogen bound to ER in the nucleus can then mediate gene transcription
•
It is possible that prolactin is stimulating a similar process in MPOA to enhance
display of maternal behavior--however, we don’t have direct proof!
Interaction Between Estrogen and Prolactin
Prolactin can act at the MPOA to stimulate rapid onset of maternal behavior.
– In steroid primed females, administration of prolactin into the MPOA can stimulate rapid
onset of maternal behavior.
– Prolactin neurons exist within the brain and project into the MPOA (as well as within
other brain regions).
– A subset of prolactin neurons within the brain also accumulate estrogen receptors;
estrogen can positively regulate levels of prolactin within the brain..
– There is also evidence that prolactin can be transported from blood into the brain via
specific transporters.
– If you block the rise in prolactin with an inhibitor bromocriptine, you can delay but not
prevent the onset of maternal behavior.
– Prolactin is believed to act by stimulating rapid onset of maternal behavior--critical
because in real life, if mom (or dad) does not care for the pups they will die.
Interaction Between Estrogen and Prolactin
Estrogen and prolactin both act to facilitate maternal behavior at the level of the MPOA.
How do these mechanisms interact? Don’t fully understand...
•
Prolactin increases can increase sensitivity of neurons to the effects of estrogen.
•
Estrogen is important for the initiation of maternal behavior.
•
However, once maternal behavior is initiated, estrogen levels are relatively low, and
are not believed to be important for maintenance of maternal behavior.
•
Suckling by pups is one stimulus that has been shown to be important for
maintenance of maternal behavior.
•
Suckling increases levels of prolactin within the blood and brain.
•
Prolactin is believed to be important for the rapid onset of maternal behavior (which
is critical).
•
Blocking prolactin levels delays the onset of maternal behavior but it does not
prevent it…possibility that other mechanisms may also exist to facilitate response.
Female Rat as a Model
2 phases to maternal behavior:
•
hormonal phase:
– decrease in progesterone, increase in prolactin with elevated levels of estrogen
– hormonal changes are important for the initiation of maternal behavior
– however, once maternal behavior has been initiated, removal of the ovaries, adrenal gland,
pituitary and placenta will not affect behavior (i.e., removal of gonadal steroids and
peptide/protein hormones present within bloodstream)
•
nonhormonal phase:
– a transition occurs in which maintenance of maternal behavior depends on stimuli
received from young (pups): suckling by pups at nipple, visual stimuli, auditory stimuli
(crying)
– neurocircuits within the brain that process somatosensory, visual, auditory information can
feed into, and stimulate, neurons within MPOA to stimulate maternal behavior
•
transition period last approximately one week following parturition
Female Rat as a Model
Key differences between hormonal and nonhormonal phases on maternal behavior:
•
at parturition, the drop in progesterone allows the rise in estrogen to stimulate
numerous processes including maternal behavior (stimulating the synthesis and
release of hormones and the expression of their receptors)
•
once young are born, gonadal steroid levels are relatively low during nursing (even
though female engages in maternal behavior)
•
stimuli from pups can maintain maternal behavior in the absence of high levels of
estrogen
– Ex. somatosensory stimuli associated with suckling at the nipple activates a
neuroendocrine reflex leading to increased release of PRL and oxytocin within the
bloodstream, and increased release of PRL within the MPOA
MPOA
other
stimuli
?
Maternal
Behavior
HYPO
other
stimuli
PRL Neuron
PRF Neuron
Oxytocin Neuron
PRF
PITUITARY
Anterior
Posterior
oxytocin
PRL
suckling
at nipple
suckling
at nipple
MAMMARY GLAND
Ring Dove as a Model
Both male and female ring doves engage in parental behavior.
•
Parental behavior:
– nest building, laying of eggs (by female), incubation of eggs, and brooding (care of
hatchlings--warmth, protection, feeding)
– feeding involves producing and regurgitating “crop milk”
•
Hormones play a major role in parental behavior in both sexes:
– during courtship and nest building, the levels of estrogen and progesterone are high in
female ring doves, and the level of testosterone is high in male ring doves
– as levels of gonadal steroids drop following courtship and nest building, the female will
lay eggs, and both the male and female ring doves initiate incubation behavior
– rise in prolactin during incubation behavior is important for maintenance of incubation
behavior and for initiation of brooding
– somatosensory cues associated with incubating eggs stimulate prolactin synthesis and
release within bloodstream and brain-->development of the crop gland, production of crop
milk, and display of behaviros to care for young once hatched
Ring Dove as a Model
During courtship and nest building:
•
gonadal steroids are high
•
gonadal steroids stimulate formation of a brood patch:
– brood patch is a defeathered, highly vascularized and edemic (fluid-filled) area
– this region will contact eggs during incubation, providing warmth to egg (important for
development of embryo)
– this region will also provide the parent with somatosensory stimulation important for
maintaining release of PRL
– a brood patch will be seen in male and female ring doves, as they both engage in
incubation behavior
•
there are bird species in which neither the mother nor the father incubate eggs
– Ex. brown-headed cowbird
– considered parasitic as female lays her eggs in the nests of other birds
– no brood patch is formed in either the mother or father brown-headed cowbird
Ring Dove as a Model
Both male and female ring doves incubate eggs--incubation behavior.
•
incubation behavior is initiated as gonadal steroids decline and after eggs are layed
•
prolactin levels rise midway during incubation:
– maintain incubation behavior
– prepare Mom and Pop for the next stage--brooding: 1) development of crop gland, and 2)
production of “crop milk”
Both male and female ring doves show brooding behavior.
•
prolactin levels are high at initiation of brooding behavior
– prolactin maintains crop gland and production of “crop milk”
– prolactin stimulates feeding the young --regurgitation of ”crop milk”
– prolactin stimulates “sitting” on hatchlings to provide warmth
Ring Dove as a Model
Initiation and maintenance of incubation behavior:
remove eggs
from nest
drop in gonadal
steroids, and
laying of eggs
decrease in
prolactin levels
(initiation)
incubation
behavior
(sitting on eggs)
“somatosensory
stimulation”
prolactin
synthesis
and release
(maintenance)
decrease in
incubation
behavior
administer
prolactin
Comparison--Female Rat and Ring Dove
Interesting parallels between female rat and male and female ring doves:
Female Rat
Male & Female Ring Dove
estrogen and progesterone
prime the brain to respond
to estrogen and PRL to
initiate maternal behavior
at parturition
rise in gonadal steroids
prime the brain to
initially show
incubation behavior
after laying eggs
shift in control of maternal
behavior (nursing, pup
retrieveal, licking) from
gonadal steroids to stimuli
associated with pups (e.g.,
suckling at nipple)
tactile stimulation from
eggs is important for
maintaining incubation
behavior and for
stimulating brooding
responses
PRL plays critical role
PRL plays critical role