Hormones and Behavior Worksheet

Lecture 9:
Female Reproductive Behavior
Part 1
Biology 178
Instructor
Melina Acosta
Outline of Today’s Lecture
1. Overview of Female Reproductive Behavior
2. The Human Menstrual Cycle
a) The Follicular Phase
b) Ovulation
c) The Luteal Phase and Early Pregnancy
3. Hormones and Female Reproductive Behavior in Primates
2
Learning Objectives
1. Define and describe the major components of female sexual behavior.
2. Describe the changes in the hypothalamic-pituitary-ovarian axis that
occur over the course of the human menstrual cycle and explain how
these changes relate to concurrent changes in the brain, ovaries, and
uterus.
3. Describe how sexual behavior in female primates, including women, is
influenced by, or correlates with, hormonal changes across the ovarian
cycle.
3
Female Reproductive Behavior:
Overview
Female Sexual Behavior: Definitions
•
Estrous
– “In a frenzy,” “possessed by the gadfly”
– Willing to mate (“in heat”, “in estrus”)
– Behavioral term
•
Estrous cycle
– Cyclical pattern of estrous behavior
•
Menstrual cycle
– Cyclical pattern of hormonal changes characterized by
regular sloughing off of the endometrium (inner lining of
the uterus)
– Only in humans and some other primates
5
Female Sexual Behavior: Components
1. Attractivity
– Female’s stimulus value (attractiveness) for a particular
male (how hot is she?)
– Measured by male’s behavior
– Can involve behavioral & non-behavioral cues (e.g.,
olfactory or visual cues) from the female
6
Female Sexual Behavior: Components
1. Attractivity
2. Proceptivity
– Female’s behavioral role in initiating copulation
– Can include approaches, contact, solicitation, mounting,
etc.
– Can overlap with attractivity
7
Female Sexual Behavior: Components
2. Proceptivity (cont.)
Unusual proceptive behavior in capuchin monkeys

8
Female Sexual Behavior: Components
1. Attractivity
2. Proceptivity
3. Receptivity
– Female’s willingness to permit/facilitate copulation
– Can include postures, maintenance of contact, specific
behaviors
– Can overlap with proceptivity
9
Female
Rats
Female Sexual
Sexual Behavior:
Behavior: Rats
Behavioral estrus occurs every 4-5 nights
– Approaches to male
– Hopping, darting, ear-wiggling
– Lordosis (reflex)
Female pacing of copulation
– In nature, females control the patterning of
copulation (e.g., by approach/withdrawal)
10
Female Sexual Behavior: Primates
•
May or may not have clear estrous cycles.
•
May or may not have stereotyped copulatory behaviors.
•
Can be highly selective.
•
Can use “sexual behavior” for non-sexual purposes.
 Suggests greater emancipation (independence) of sexual
behavior from hormones in primates!
11
The Human Menstrual Cycle:
The Follicular Phase
Human Menstrual Cycle: Overview
• Follicular phase
~10-20 days (variable)
• Ovulation
1 day
• Luteal phase
14-16 days (consistent)
Ovarian
cycle –
occurs
simultaneously
with…
• Menstruation
~3-5
Starts on Day 1 of cycle (by definition)
Corresponds to early follicular phase
• Proliferative phase
~9-11 days
Corresponds to mid- to late follicular phase
• Secretory phase
~14 days
Corresponds to luteal phase
Uterine
cycle
13
Human Menstrual Cycle: Follicular Phase
The Ovarian Cycle
Follicular Phase
Day of
Cycle:
1
3
5
7
9
Ovulation
11
13
15
Luteal Phase
17
Menstruation Proliferative Phase
19
21
23
25
27
29
Secretory Phase
The Uterine Cycle
14
Human Menstrual Cycle: Follicular Phase
Follicular Phase
• First part of the ovarian cycle
• Dominated by developing follicles in the ovary
• Follicle: oocyte (egg cell) + surrounding cell layers
– Nourishes and protect oocytes
– Secretes hormones
15
Human Menstrual Cycle: Follicular Phase
Follicles
• Follicular cells surrounding the oocyte:
– Thecal cells:
Synthesize androgens under the influence of LH
– Granulosa cells:
Aromatize androgens to estrogens under the influence of FSH
16
Human Menstrual Cycle: Follicular Phase
Thecal and granulosa cells collaborate to produce estrogen.
Anterior
Pituitary
Estrogens
FSH
Granulosa
Cell
LH
Thecal
Cell
(Aromatase)
Ovary
Androgens
17
Human Menstrual Cycle: Follicular Phase
Thecal and granulosa cells collaborate to produce estrogen
AR = aromatase
18
Human Menstrual Cycle: Follicular Phase
Follicular Phase
Before birth
Cow follicle
Monthly
cycles
Ultrasound
Cross-section
thru follicle
19
Human Menstrual Cycle: Follicular Phase
Negative feedback
– Hypothalamus
Gonadotropin-releasing
hormone (GnRH)
– Anterior Pituitary
Luteinizing
hormone (LH)
Follicle-stim. –
hormone (FSH)
Follicles in Ovary
(devt./growth)
Estrogen
Inhibin
Endometrium
Brain/Behavior
Other Tissues
20
Human Menstrual Cycle: Follicular Phase
Hypothalamic-Pituitary-Ovarian Axis
• GnRH →  LH,FSH → follicular growth and development
• Developing follicles secrete increasing E, inhibin
• E, inhibin negative feedback →  GnRH,  LH  FSH
21
Human Menstrual Cycle: Follicular Phase
A single, dominant follicle emerges, matures fully, and suppresses
development of other follicles. How??
• The dominant follicle…
– Secretes large amounts of E and inhibin →
LH and FSH drop to very low levels.
– Increases its expression of LH and FSH receptors→
becomes highly sensitive to gonadotropins.
– Becomes more vascularized →
gets increased delivery of LH & FSH.
Atretic follicle
• Other follicles do not undergo these
changes → cannot survive under
conditions of very low LH and FSH →
undergo atresia (degeneration).
22
Human Menstrual Cycle: Follicular Phase
Subordinate
follicles
Dominant
follicle
23
Human Menstrual Cycle: Follicular Phase
Uterus
– Early follicular phase:
Low E, P → menstruation (days 1-~5)
– Mid- to late follicular phase:
Rising E → growth of endometrium
(proliferative phase) (~ days 6-14)
Menstrual
Phase
Proliferative
Phase
24
Human Menstrual
Cycle: Follicular
Phase
LH
Progesterone
Silverthorn 2009
25
The Human Menstrual Cycle:
Ovulation
Human Menstrual Cycle: Ovulation
The Ovarian Cycle
Follicular Phase
Day of
Cycle:
1
3
5
7
9
Ovulation
11
13
15
Luteal Phase
17
Menstruation Proliferative Phase
19
21
23
25
27
29
Secretory Phase
The Uterine Cycle
27
Human Menstrual Cycle: Ovulation
Ovulation
• Release of ovum from follicle
• Triggered by LH surge in response to E elevation (positive
feedback)
Pig ovary at ovulation
Ovum
Rupture site
28
Human Menstrual Cycle: Ovulation
Ovulation
29
Human Menstrual Cycle: Ovulation
Human ovulation, photographed during a hysterectomy
(lasted ~15 minutes)
1
2
3
4
30
Human Menstrual Cycle: Ovulation
Hypothalamic-Pituitary-Ovarian Axis
• Sustained high E from developing follicles exerts
positive feedback on hypothalamus and ant. pituitary:
→  GnRH release from hypothalamus
→  GnRH receptors in anterior pituitary
→  LH, FSH release from anterior pituitary
• LH surge triggers ovulation:
Dominant follicle ruptures; oocyte is ejected from
ovary and enters oviduct.
31
feedback
Positive
feedback
Negative
Human Menstrual Cycle: Ovulation
+– Hypothalamus
+– Anterior Pituitary
Gonadotropin-releasing
hormone (GnRH)
Luteinizing
hormone (LH)
Follicle-stim. ––
hormone (FSH)
Follicles in Ovary
(devt./growth)
Ovulation
Estrogen
Inhibin
Endometrium
Brain/Behavior
Other Tissues
32
Human Menstrual
Cycle: Ovulation
Progesterone
Silverthorn 2009
33
The Human Menstrual Cycle:
The Luteal Phase & Pregnancy
Human Menstrual Cycle: Luteal Phase
Luteal Phase
• After ovulation
• Corpus luteum (CL) develops from ovulated follicle.
– Histological and biochemical changes
– Vascularization
Pig ovaries
Hamster ovaries
With cigarette
smoke
Control
35
Human Menstrual Cycle: Luteal Phase
Human ovary with
fully developed
corpus luteum
36
Human Menstrual Cycle: Luteal Phase
Luteal Phase
Cow CL
CL
Ultrasound
Ovary cut
thru CL
37
Human Menstrual Cycle: Luteal Phase
Negative feedback
– Hypothalamus
Gonadotropin-releasing
hormone (GnRH)
– Anterior Pituitary
Luteinizing
hormone (LH)
Follicle-stim. –
hormone (FSH)
Corpus Luteum
in Ovary
Progesterone+
Inhibin
Estrogen
Endometrium
Brain/Behavior
Other Tissues
38
Human Menstrual Cycle: Luteal Phase
Hypothalamic-Pituitary-Ovarian Axis (non-conceptive cycle)
• LH surge causes ovulated follicle to develop into corpus luteum (CL)
• CL secretes P, E, and inhibin
• P, E, inhibin exert neg feedback →  GnRH,  LH,  FSH
39
Human Menstrual Cycle: Luteal Phase
Hypothalamic-Pituitary-Ovarian Axis (non-conceptive cycle)
– LH surge causes ovulated follicle to develop into corpus luteum
(CL)
– CL secretes P, E, and inhibin
– P, E, inhibin exert neg. feedback → GnRH, LH, FSH
– After ~14 days, CL regresses (if no conception)
–  P,  E,  inhibin →
 GnRH,  LH,  FSH
–  LH,  FSH → development
Start of next follicular phase
of
new cohort of follicles
40
Human Menstrual Cycle: Luteal Phase
Negative feedback
– Hypothalamus
Gonadotropin-releasing
hormone (GnRH)
– Anterior Pituitary
Luteinizing
hormone (LH)
Follicle-stim. –
hormone (FSH)
Corpus
Luteum
Development
of
in Ovary
New
Follicles
Progesterone+
Inhibin
Estrogen
Endometrium
Endometrium
breaks down 
Brain/Behavior
Menstruation
Other Tissues
41
Human Menstrual Cycle: Luteal Phase
Uterus (non-conceptive cycle)
– P + E → endometrium prepares for pregnancy
(secretory phase)
– End of luteal phase/beginning of next follicular phase:
 P,  E → endometrium sloughs off (menstruation)
Menstrual
Phase
Proliferative
Phase
Secretory
Phase
42
Human Menstrual
Cycle: Luteal
Phase
Silverthorn 2009
43
Human Menstrual Cycle: Summary
44
Human Menstrual Cycle: Timing of Fertility
• Maximum fertility
– Sperm can live in the female reproductive tract
up to 8 days (usually 1-5 days).
– Maximum fertility: 4-5 days before through 1-2
days after ovulation.
• Calculating the timing of ovulation
– Luteal phase (ovulation to menstruation):
usually 14-16 days (consistent within women).
– Follicular phase (menstruation to ovulation):
more variable.
– So, timing of maximum fertility can be determined
retroactively but not proactively!
45
Human Menstrual Cycle: Ovulation
The Ovarian Cycle
Follicular Phase
Day of
Cycle:
1
3
5
7
9
Ovulation
11
13
15
Luteal Phase
17
Menstruation Proliferative Phase
19
21
23
25
27
29
Secretory Phase
The Uterine Cycle
46
Human Menstrual Cycle: Early Pregnancy
• If conception occurs…
– Blastocyst secretes human chorionic gonadotropin
(hCG) – structurally and functionally similar to LH.
– hCG “rescues” the CL.
– CL survives & secretes P for ~ 7 weeks.
– P maintains endometrium.
47
Hormones and Female
Reproductive Behavior in
Primates
Hormonal
Correlates of
Female Sexual
Behavior in
Primates: The
Ovarian Cycle
Latency to gain
access to male
(Proceptivity)
Mounts rec’d.
per minute
(Attractivity)
Day of ovulation
Number of
ejaculations
Time to barpress 250X
(Receptivity)
(Proceptivity)
Minutes until
ejaculation
(Receptivity)
Day of ovulation
Rhesus
monkeys
49
Hormonal Correlates of Female Sexual Behavior in
Primates: The Ovarian Cycle
Attractivity
(Sexual behavs. received from males)
Japanese
macaques
Mount
receive
Hold
receive
Other
receive
Follic.
O’Neill et al. 2005
Periovul.
Luteal
50
Hormonal Correlates of Female Sexual Behavior in
Primates: The Ovarian Cycle
Japanese
macaques
Proceptivity
(Sexual behavs. performed to males)
Mount
direct
Other Estrous
direct
call
Hold
direct
Follic.
O’Neill et al. 2005
Periovul.
Luteal
51
Hormonal Correlates of Female Sexual Behavior in
Primates: The Ovarian Cycle
• Studies of women in long-term relationships have found that
sexual behavior…
1. Does not change across the menstrual cycle, OR
2. May peak around ovulation, OR
Fertile period
3. May show a smaller peak
around menstruation.
• Erotic thoughts, masturbation
peak around ovulation
Seems to be caused by
changes in proceptivity,
not attractivity.
Wilcox et al.
2004
52
Hormonal Correlates of Female Sexual Behavior in
Primates: The Ovarian Cycle
Around the time of ovulation, women…
• Engage in more “extra-pair” flirtation
• Show increased preferences for masculine men (based on faces,
bodies, behavior, voices, or odors)
53
Hormonal Correlates of Female Sexual Behavior in
Primates: The Ovarian Cycle
Around the time of ovulation, women…
• Dress more provocatively
Estrogen:
Progesterone
ratio
Probability
of wearing
red
Eisenbruch
et al. 2015
54
Hormonal Correlates of Female Sexual Behavior in
Primates: The Ovarian Cycle
Around the time of ovulation, women…
• Smell better to men than at other times
• Receive more “mate-guarding” by their partners
Around the time of ovulation, lap dancers…
• Make more money in tips!
Miller et al.
2007
55
Hormonal Correlates of Female Sexual Behavior in
Primates: Estrogen
Sexual behavior is usually enhanced by the steroid hormone milieu
occurring around the time of peak fertility: ovulation.
• Estrogen levels peak just before ovulation.
• Estrogens typically enhance attractivity, receptivity, and
proceptivity.
Ovariectomized marmosets
Dixson
1998
56
Hormonal Correlates of Female Sexual Behavior in
Primates: Androgens
Androgens can increase female sexual behavior in
women, rhesus monkeys, and some other species.
Androgens…
• Are secreted by the ovaries or adrenal cortex and peak during
the preovulatory period.
• Correlate with sexual desire and sexual thoughts in women.
• May restore sexual desire in ovariectomized or
postmenopausal women.
57
Hormonal Correlates of Female Sexual Behavior in
Primates: Conclusions
• Attractivity, proceptivity, and receptivity may be enhanced by
the steroid hormonal milieu occurring around the time of peak
fertility: ovulation.
– Sex steroids can increase sexual motivation and attractivity.
– Sex steroids are not necessary for sexual motivation,
attractivity, or performance.
58
End of Lecture 9
59
Lecture 10:
Female Reproductive Behavior
Part 2
Biology 178
Instructor
Melina Acosta
Outline of Today’s Lecture
1. The Estrous Cycle and Hormonal Influences on Female
Sexual Behavior in Rats
2. The Neural Basis of Lordosis in Rats
3. Social Influences on Female Reproductive Cycles
2
Learning Objectives
1. Describe the hormonal changes that occur across the rat estrous cycle and
pseudopregnancy, and explain how these changes affect attractivity,
receptivity, and proceptivity.
2. Compare and contrast primates and rodents with respect to hormonal
changes across the ovarian cycle and how these changes relate to sexual
behavior.
3. Describe the neural circuitry underlying lordosis in rats, and explain
how estrogen and progesterone act on this circuitry to activate lordosis.
4. Give some examples of how female reproductive cycles can be affected
by the social environment in rodents, humans, and cooperative
breeders.
3
Estrous Cycles in Rodents
The Rat Estrous Cycle
• 4-5 days long
• Stages:
Diestrus I (metestrus), II (& III) – Follicular phase
Proestrus – Late follicular phase (LH surge)
Estrus – Ovulation
*
* Ovulation
*
5
The Rat Estrous Cycle
• Metestrus/Diestrus:
 GnRH (1x/day) →  LH,  FSH →
Follicular development →  Estrogen (E) (over 2-3 days)
• Afternoon of proestrus:
  E →    GnRH,   LH,   FSH →   Progesterone (P)
• Early morning of
estrus:
Ovulation
Estrous behavior
→ Both are
stimulated by E+P
Miller &
Takahashi,
2014
6
The Rat Estrous Cycle
Induced Luteal Function
• If mating occurs:
Physical stimulation from mating (intromission) →
prolactin secretion from anterior pituitary for ~ 10 days →
Prolactin “rescues” corpus lutea (luteotrophic effect)
-If female conceives: pregnancy (21 days)

-If female does not conceive (but mating occurs)
Pseudopregnancy-CLs are maintained for ~10 days
• If no mating occurs:
No  in prolactin secretion →
CLs do not form fully (no spontaneous luteal phase) →
 Progesterone →
New cycle begins
7
The Rat Estrous Cycle
Induced Luteal Function:
Intromission →
 Prolactin →
Maintenance of CLs for ~10 days→
 Progesterone for ~10 days
8
Hormonal Correlates of Female Reproductive
Behavior in Rodents
• Rodents and many other species:
– Ovariectomized females will not mate.
– Intact females are attractive, proceptive, and receptive
only around the time of ovulation (estrus).
– Estrogen is necessary for attractivity, sexual motivation,
and sexual performance.
9
Hormonal Correlates of Female Reproductive
Behavior in Rodents: Progesterone
Progesterone can exert biphasic effects on sexual behavior:
• In some species
(including rats), P rises
shortly before
ovulation.
• P may be necessary for activation of sexual behavior in
these species.
• High P levels (after ovulation) can later terminate sexual
behavior (by downregulating receptors for E & P).
10
Variation in Female Reproductive Cycles
• Spontaneous vs. induced behavioral estrus
Estrus may be induced by cues from male
(e.g., courtship displays, chemosignal)
Example: prairie vole
• Spontaneous vs. induced (reflex) ovulation
Ovulation may be induced by stimuli associated
with mating
Example: cat, rabbit
• Spontaneous vs. induced pseudopregnancy
Maintenance of CL (in non-conceptive cycles) may be
induced by stimuli associated with mating
Example: rat
11
Neural and Hormonal
Mechanisms of Lordosis in Rats
Neural & Hormonal Control of Lordosis
Lordosis is…
• A stereotyped behavior (reflex) that occurs in response
to specific sensory cues and distinct hormonal
regulation.
• The first mammalian behavior with the underlying
neural circuitry and hormonal basis mapped.
13
Neural & Hormonal Control of Lordosis
Ovarian steroids (estrogen [E] and progesterone [P]) act…
1. Via socially mediated effects (attractivity)
2. On sensory system
3. On integrative systems in the brain
…to control the motor output of lordosis.
Nelson 2000
Hormone-dependent
integration in brain
Motor output to
muscles in back
Sensory input
from flanks
14
Lordosis: Sensory Input
Sensory input eliciting lordosis:
• Tactile (touch/pressure) stimulation around flanks:
Necessary to elicit lordosis.
• Visual, olfactory, etc. cues:
Unnecessary.
• Tactile input from male stimulates sensory receptors on
flanks, rump, and perineum.
• Receptors send info through the spinal cord to the medullary
reticular formation in the brainstem and to the central gray area
(=periaqueductal gray) in the midbrain.
15
Lordosis: Sensory Input
Estrogen →
•  Size of receptive fields of sensory neurons in flanks
•  Excitability of neurons in spine, medullary reticular
formation, and midbrain central gray that respond to
lordosis-triggering stimuli
Anestrous rat
Estrous rat
16
Lordosis: Motor Output
Medullary reticular formation (in brainstem):
• Output: Sends motor neurons down the spinal cord to innervate
muscles in the back.
• Input: Receives…
– Ascending sensory info directly from the spinal cord
– Descending info from higher, estrogen- (E-) sensitive brain regions
(hypothalamus, MPOA) via midbrain central gray
E-sensitive
regions in
forebrain
Sensory input: flanks →
spinal cord → brain
17
Lordosis: Hormonal Influences
Descending input from E-sensitive hypothalamic regions is
necessary for lordosis:
• Ventromedial nucleus of hypothalamus (VMN)
• Medial preoptic area (MPOA)
• Medial anterior hypothalamus (MAH)
Motor output:
brain →
spinal cord →
muscles
E-sensitive
regions in
forebrain
Sensory input: flanks →
spinal cord → brain
18
Lordosis: Hormonal Influences
Estrogenic influences on the motor output system:
• Ventromedial nucleus of hypothalamus (VMH)
– Stimulates lordosis
– Is stimulated by E
• Medial preoptic area (MPOA)
– Inhibits lordosis
– Inhibits reward pathway
– Is inhibited by E
Motor output:
brain →
spinal cord →
muscles
E-sensitive
regions in
forebrain
Sensory input: flanks →
spinal cord → brain
19
Lordosis: Hormonal Influences
Summary:
• Estrogen is necessary for the expression of lordosis in female rodents:
1. Main effect: Activates VMN to stimulate lordosis.
E → stimulates VMN → stimulates midbrain central gray →
stimulates med. reticular formation →
stimulates motor neurons in brainstem & spinal cord →
activates muscles in flanks and lower back →
lordosis!
2. Inhibits MPOA to disinhibit lordosis.
3. Increases responsiveness to tactile cues from males.
4. Increases females’ attractivity to males.
 How does E exert these effects within the
brain (especially the VMN)?
20
Lordosis: Hormonal Influences
Estrogen priming:
• E alone or E+P (more potent) facilitates lordosis in
ovariectomized rats.
• Initial E exposure must be followed ~ 24 hours later by P (or E)
treatment to induce lordosis (lordosis occurs ~4 hours after P
treatment).
• Same effect if the E and/or P is implanted in the VMN → E
priming effect depends on VMN.
• Requires both
classical (slow,
genomic) and nonclassical effects of E.
21
Lordosis: Hormonal Influences
Estrogen priming in VMN affects…
• P and E receptors
• Neurotransmitter receptors
• Dendritic spines
• Electrophysiological properties
Progesterone in VMN affects…
• Neurotransmitters
• Neurotransmitter receptors
• Later, P downregulates E & P receptors to terminate sexual behavior.
0 hrs
24 hrs
Estrogen Priming
E
treatment
28 hrs
P Effects
P
treatment
Lordosis!
22
Lordosis: Hormonal Influences
The Cascade Hypothesis:
• Initial E exposure causes a cascade of events in the central
nervous system (especially VMN), including structural,
electrophysiological, and neurochemical changes, that prime the
CNS for subsequent P exposure.
• This cascade of events occurs over a number of hours and permits
later P (or E) exposure to stimulate lordosis in response to
appropriate sensory (tactile) cues.
• P is necessary for proceptive behavior but not for lordosis.
 Two-stage hormonal effects – analogous to
organizational/activational effects, but over a much
shorter time scale!
23
Lordosis & The Reward Pathway
Interactions between the neural circuitry of lordosis and the
reward pathway:
• Engaging in copulatory behavior has long-term effects on the
reward pathway (especially the nucleus accumbens and ventral
tegmental area).
• Reward pathway influences sexual motivation (“liking” and
“wanting”sex).
• In the absence of E, the reward pathway is inhibited by the
MPOA.
• E removes this inhibition by the MPOA.
 Interactions between the lordosis circuitry and
the reward pathway can lead to effects of
experience on sexual motivation.
24
Social Influences on Female
Reproductive Cycles
Social Influences on Reproductive Cycles in
Mice
Pheromones:
• Chemical signals produced by one individual that can alter
physiology and/or behavior of another individual
• Signaling/Releaser Pheromones
Elicit an immediate behavioral response
• Primer Pheromones
Elicit a longer-term physiological
or developmental change
• Detected by VNO → AOB →
amygdala → hypothalamus
26
Social Influences on Reproductive Cycles in
Mice
1. The Lee-Boot Effect
– Group female mice ≥4 per cage (no males) →
extended estrous cycles (pseudopregnancy).
2. The Whitten Effect
– Group female mice >20 per cage (no males) →
estrous cycles cease.
– Introduce male or male odor →
synchronized ovulation after 3-4 days.
27
Social Influences on Reproductive Cycles in
Mice
3. The Bruce Effect
–
Expose pregnant mouse to unfamiliar male for >48 hours →
female aborts or resorbs fetuses.
–
Female mates with new male
later.
–
Is thought to have evolved in
infanticide by unfamiliar males.
3-6 days
response to
Pregnancy
Pregnancy block
(Bruce Effect)
28
Social Influences on Reproductive Cycles in
Mice
3. The Bruce Effect
Pheromone from unfamiliar male → → →
↓Prolactin →
CLs regress →
↓Progesterone →
Pregnancy ends
29
Social Influences on Reproductive Cycles in
Mice
4. The Vandenbergh Effect
– Adult males accelerate puberty in young females
– Adult females delay puberty in young females
Uterus
Saline
Flanagan et al. 2011
Male
Urine
Body
Mass
Saline
Uterine
Mass
Male
Urine
Saline Male
Urine
30
Social Influences on Reproductive Cycles in
Mice
Male Accelerating Pheromone
• Androgen-dependent; in males’ urine
• Stimulates GnRH, LH and estrogen secretion in recipient:
– Young females: accelerates puberty
– Suppressed females: initiates cycles
– Pregnant females: ends pregnancy, stimulates ovulation
31
Asaba et al. 2014
Social Influences on Reproductive Cycles in
Mice
Female Inhibitory Pheromone
• In females’ urine?
• Inhibits GnRH, LH and estrogen secretion in recipient
– Young females: delays puberty
– Cycling females: inhibits cycling and ovulation
32
Social
Influences
onReproductive
Reproductive Cycles
Social
Influences
on
Cycles
in
in Women
Women
Do humans have pheromones?
• Evidence that some pheromones are produced in the
axillary region (armpit).
• Human VNO is vestigial and probably non-functional.
• Pheromones might be detected by nasal epithelium.
➔ What do they do?
33
Social Influences on Reproductive Cycles in
Women
1. Menstrual synchrony
• Has been reported among roommates, close friends, related women
living together.
• Demonstrated scientifically by McClintock in 1971.
• Not found in most subsequent studies.
34
Social Influences on Reproductive Cycles in
Women
2. Normalization of cycles by males
Male axillary secretions →
•  LH pulse frequency
• Normalize cycle
length in women
with irregular cycles
Latency to Next LH Pulse
Control
Male
secretions
Preti et al., 2003
35
Social Suppression of Ovulation in Cooperative
Breeders
• Cooperative breeders, individuals routinely provide care for other
animals’ offspring.
• Frequently, only the dominant female breeds.
• Ovulation may be inhibited in subordinate females.
36
Social Suppression of Ovulation in Cooperative
Breeders- Marmoset Monkeys
37
Social Suppression of Ovulation in Cooperative
Breeders- Marmoset Monkeys
38
Social Suppression of Ovulation in Cooperative
Breeders- Marmoset Monkeys
39
Environmental Influences on Reproduction
• Seasonality
Proximate cues:
– Photoperiod (daylength)
– Food
– Plant compounds
• Energetics/food intake
–
Intense athletic training
–
Anorexia nervosa
–
Famine
–
Etc.
• Psychological stress
40
End of Lecture 10
41
Lecture 11:
Parental Behavior
Part 1
Biology 178
Instructor
Melina Acosta
Outline of Today’s Lecture
1. Parental Behavior in Vertebrates: Overview
2. Parental Behavior in Birds
a) Hormonal Correlates
b) Paternal Behavior
c) Neural Mechanisms
3. Parental Behavior in Mammals
a. Overview
b. Hormonal Influences on Parental Behavior in Rodents
2
Learning Objectives
1. Describe the major categories of parental care in birds, including what
kinds of care are provided and who provides the care.
2. Describe the sequence of events in the reproductive cycle of ring doves
and explain how these events interact with hormones.
3. Explain how testosterone and prolactin correlate with and influence
parental care in birds.
4. Briefly describe the neural control of parental care in birds.
5. List the major types and categories of parental care in mammals
6. Explain how both hormones and experiences with pups influence the
onset of parental behavior in rodents.
3
Parental Behavior in Vertebrates:
Overview
Parental Behavior in Vertebrates
• Definition: Any behavior that directly enhances the
survival of fertilized eggs or offspring that have left the
body of the female
• Essential for successful reproduction in some taxa (esp.
birds, mammals) and therefore under intensive natural
selection.
• In some taxa, parents (usually mothers) must engage in
appropriate parental behaviors immediately after
birth/hatching of offspring in order for offspring to
survive.
5
Parental Behavior in Vertebrates
• Maternal behavior is initiated under specific hormonal
conditions associated with egg-laying or pregnancy,
parturition (giving birth), and lactation.
• Hormonal control of the initiation of maternal behavior
is usually linked to hormonal control of reproduction.
• Maintenance of maternal behavior, after it begins, may
be less dependent on hormones.
6
Parental Behavior in Vertebrates
Fish, Amphibians, Reptiles:
•
Care of eggs by males and/or females in some species
•
Care of hatchlings by males and/or females in some
species
Birds, Mammals:
• Almost all species exhibit maternal behavior (by moms).
• Some (esp. birds) exhibit paternal behavior (by dads).
7
Parental Behavior in Birds
Parental Behavior in Birds
Components:
Nest-building
Incubating eggs
Brood patch
Feeding nestlings
Regurgitating food
Producing crop milk (pigeons and doves)
Protecting nestlings
Nest-defense behaviors
Broody behavior
(Incubating eggs)
Sitting on or over nestlings –
provides protection, warmth
9
Parental Behavior in Birds
Species Differences: Type of Nestlings
Altricial Young
• Helpless, immobile at hatching
• Require feeding, protection, brooding
• e.g., robins, starlings (most birds)
Precocial Young
• More developed, mobile at hatching
• Require protection & brooding but can self-feed
• e.g., chickens, ducks
10
Parental Behavior in Birds
Species Differences: Who’s Watching the Kids?
Maternal (Mom) + Paternal (Dad) Care
(“biparental)
Males may help with some or all parental
jobs
Maternal Care Only
Paternal Care Only
Alloparents (“helpers at the nest”)
Cooperative breeders
Often involves older brothers
“Foster family”
Nest parasites : lay eggs in nest of another species;
parental care is provided by foster family
11
Parental Behavior in Birds
Nest Parasites (e.g., some cuckoos, cowbirds)
• Female lays an egg in nest of another species; might
remove resident eggs.
• Parasite chick hatches first and ejects or kills eggs or
hatchlings of foster parents.
• Foster parents feed parasite chick.
12
Parental Behavior in Birds
Nest Parasites:

13
Hormonal Correlates of Parental
Behavior in Birds
Hormonal Correlates of Parental Behavior in Ring Doves
Ring doves (studied by Lehrman et al.):
• Stereotyped sequence of reproductive behaviors in males and
females; correlates with sequence of hormonal changes in
both sexes:
– Male brings nest material to female.
– Female builds nest.
– Both male and female incubate eggs.
– Both male and female produce crop
milk.
– Later, both male and female feed squabs
with seeds and insects.
15
The Crop Sac and Crop Milk
Esophagus
Crop
16
Hormonal Correlates of Parental Behavior in Ring Doves
• Sex steroids, LH, FSH
Are elevated during, and stimulate, courtship, nest-building and
egg-laying
• Prolactin
Rises during egg-laying, as steroid levels fall; peaks during
incubation
Stimulates parental behavior and development of crop sac in
both sexes
Behavioral and
hormonal
events during
the breeding
season of
temperate-zone
birds
17
Hormonal Correlates of Parental Behavior in Ring Doves
Male
Female
18
Hormonal Correlates of Parental Behavior in (Female)
Ring Doves
Initiation of incubation (females):
• Progesterone levels are high.
• Prolactin is beginning to rise.
 Progesterone in the presence of eggs stimulates the
onset of incubation behavior.
19
Hormonal Correlates of Parental Behavior in (Female)
Ring Doves
Maintenance of incubation:
• Incubation behavior →  progesterone,  prolactin.
• Prolactin → maintains incubation behavior.
• Prolactin → development of crop sac (in both parents).
• Removal of eggs → rapid  in prolactin and incubation
 Prolactin stimulates the
maintenance of incubation
behavior, which in turn
maintains high prolactin levels.
20
Hormonal Correlates of Parental Behavior in (Female)
Ring Doves
Broody behavior and feeding of nestlings:
• Prolactin levels are high at time of hatching.
• Prolactin → onset of broody behavior (both parents).
• Tactile and visual stimulation from squabs →
 prolactin in both parents → crop milk.
 Prolactin stimulates the initiation
of parental feeding behavior.
21
Hormonal Correlates of Parental Behavior in (Female)
Ring Doves
Termination of parental behavior:
By 20 days post-hatching…
• Male and female begin a new cycle of courtship and nest-building.
• Females: Prolactin secretion and feeding of squabs stop.
• Males: Prolactin secretion and feeding of squabs
continue.
 Prolactin seems to determine
the maintenance and
termination of parental feeding
behavior.
22
Hormonal Correlates of Parental Behavior in
Emperor Penguins
• Emperor penguins (and some other penguin species) whose
egg or chick doesn’t survive often kidnap other penguins’
chicks.

(Attempted chick-kidnapping in macaroni penguins)
23
Hormonal Correlates of Parental Behavior in
Emperor Penguins
• Emperor penguins whose egg or chick doesn’t survive often kidnap
other penguins’ chicks.
• Parents’ prolactin can remain high after death of egg or chick →
high prolactin might stimulate kidnapping.
Prolactin Before Treatment
Angelier et al. 2006
Probability of Starting to Kidnap
Dopamine agonist
– lowers PRL
24
Hormonal Correlates of Parental Behavior in Hosts of
Nest Parasites
Hosts (foster parents) of nest parasites:
Female European blackbirds:
• Experimentally lowering prolactin levels increases likelihood of
ejecting parasite eggs
25
Hormonal Correlates of Paternal
Behavior in Birds and Neural Control
of Parental Behavior in Birds
Testosterone and Paternal Behavior in Birds
In many birds, androgens are low during paternal care.
Plasma T and DHT Concentrations
Androgen
concentrations are
high during courtship
and low
during incubation and
brooding.
Courtship
Baseline 1
Incubation
Squabs
Courtship
Baseline 2
Feder et al., 1977 (ring doves)
27
Testosterone and Paternal Behavior in Birds
• T can inhibit paternal behavior in some species!
• In free-living male birds, treatment with exogenous T can
lead to…
 courtship,  number of mates (polygyny)
 territory size,  patrolling of territory
 foraging,  feeding of young
 survival of young
28
Testosterone and Paternal Behavior in Birds
Example: Van Roo, 2004
• Used free-living blue-headed vireos –
monogamous; extensive paternal care
• Gave males subcutaneous implants containing
testosterone (T), flutamide (F; androgen receptor
antagonist), or nothing (C).
• Observed nests ~10 days later.
29
Testosterone and Paternal
Behavior in Birds
Paternal behavior is
inhibited by T, but not
affected by flutamide, in
male blue-headed vireos.
Van Roo, 2004
30
Time nest unattended
Feeding of nestlings
by male
F
C
T
Testosterone and Paternal
Behavior in Birds
Singing is stimulated by T,
but not affected by
flutamide, in male blueheaded vireos.
% of time spent singing
# song phrases/min
F
C
T
Van Roo, 2004
31
Neural Control of Parental Behavior in Birds
Preoptic area
• PRL receptors in POA correlate with parental behavior.
• Engaging in parental behavior elevates fos (immediate-early gene)
expression in POA.
• POA lesions block PRL-induced parental behavior.
Fos-labeled
neurons in
the POA
32
Buntin et al., 2006
Neural Control of Parental Behavior in Birds
Example: Slawski & Buntin, 1995
• Lesioned neuronal cell bodies in POA of male and
female ring doves.
• Injected PRL twice daily for 7 days.
• Tested each bird with a foster squab.
• Killed birds and verified
POA lesions.
33
Neural Control of Parental Behavior in Birds
Slawski & Buntin, 1995
Parental feeding
invitations
Regurgitations
Parental feeding
bouts
Squab weight
change
POA lesions decrease parental feeding behavior in
male and female ring doves.
34
Neural Control of Parental Behavior in Birds
Preoptic area
• PRL receptors in POA correlate with parental behavior.
• Engaging in parental behavior elevates fos (immediate-early
gene) expression in POA.
• POA lesions block PRL-induced parental behavior.
 So the POA is critical for parental behavior in birds and
mediates the effects of prolactin.
 BUT… how does PRL get into the brain?
35
The Blood Brain Barrier (BBB)
• Specialized system of capillary endothelial cells
• Protects brain from harmful substances in blood
• Limits entry into the brain
of large and/or hydrophilic
molecules (e.g., proteins)
36
The Blood Brain Barrier (BBB)
• Components of the blood-brain barrier:
– Tight junctions between endothelial cells
– Astrocytes between capillaries and neurons
– Enzymes
• Includes specialized transport
mechanisms for some
including prolactin.
37
substances,
Parental Behavior in Mammals:
Overview
Parental Behavior in Mammals: Overview
Components:
39
•
Nest-building
•
Thermoregulation
•
Feeding young
– Lactation
– Provisioning with other foods
•
Transporting young
•
Grooming young
•
Protecting young
– Maternal aggression
Maternal Care Patterns in Eutherian Mammals
1. Nesting Pattern: Altricial Young
• Newborns blind, deaf; can’t thermoregulate; can’t
feed themselves
• Mother visits nest frequently
• Mothers may:
– lick infants to stimulate defecation and urination
– retrieve wandering infants
– perform maternal aggression
• e.g., carnivores, most rodents
40
Maternal Care Patterns in Eutherian Mammals:
Nest Behaviors in Rats
Licking
Nursing
Retrieving
41
Maternal Care Patterns in Eutherian Mammals
2. Leading-Following Pattern: Precocial Young
Hiders:
• Young are hidden at nest site for 7-10 days, then
begin to follow mother
• Mother visits nest to nurse offspring
• e.g., white-tailed deer, cattle
Followers:
• Young follow mother from birth
• e.g., elephants, whales, sheep
42
Maternal Care Patterns in Eutherian Mammals
3. Clinging-Carrying Pattern: Semi-Precocial Young
• Helpless at birth, but can see, hear, cling to
mother and thermoregulate
• Carried by or cling to mother
• e.g., humans, many other primates
43
Paternal Care Patterns in Eutherian Mammals
• Rare in mammals
• Usually associated with pair-bonds (“monogamy”) or
cooperative breeding
• Occurs in some rodents, carnivores, primates
44
Parental Behavior in Rodents:
Hormonal Influences
Hormonal Influences on Parental Behavior in Rodents
Standard test paradigm for determining influences of
experience and hormones on parental behavior:
Present “foster pups” to female (or male) and determine
her behavioral response:
46
–
Avoidance?
–
Aggression?
–
Maternal behavior?
Initiation of Maternal Behavior in Rats
Pup-induced parental behavior (sensitization):
• Nulliparous adult females:
– Present pups for several hours each day
– After 5-6 days, female behaves maternally
– Show all maternal behaviors except maternal
aggression
• Adult males:
– Show sensitization, but more slowly and less
robustly than females.
• Late-pregnant females:
– Show rapid onset of maternal behavior.
Not
dependent
on
hormones
Dependent
on
hormones
 Hormones are not necessary for the expression of maternallike behavior, but can influence how quickly the onset of this
behavior occurs.
47
Initiation of Maternal Behavior in Rats
48
Initiation of Maternal Behavior in Rats
New mothers:
• Behave maternally immediately after giving birth
• Must interact with pups shortly after birth in order to show
normal onset of maternal behavior
Experienced mothers:
• Rapid onset of maternal behavior, even during mid-pregnancy
• Maternal behavior is independent of hormones
• Requires “maternal memory” from experience with newborn pups
49
Initiation of Maternal Behavior in Rats
PRL
50
Late pregnancy in rats is characterized by:
1. Rising estrogen levels
2. A steep drop in progesterone levels
3. A sharp rise in prolactin levels
Initiation of Maternal Behavior in Rats
How do pregnancy hormones facilitate maternal behavior?
• Pregnancy-termination studies (Rosenblatt et al.):
Hysterectomy (remove uterus, fetuses, placenta)
at day 16-19 →
– Causes  progesterone,  estrogen,  prolactin
(similar to hormonal profile just before parturition)
– Leads to rapid onset of maternal behavior
51
Initiation of Maternal Behavior in Rats
How do pregnancy hormones facilitate maternal behavior?
(cont.)
• Hormonal treatment of ovariectomized females:
E (11 days) + P (days 6-9) + PRL (days 9-11)
– Leads to maternal behavior after 35 hours
– Much slower than naturally occurring onset
of maternal behavior after parturition
– What’s missing?
Oxytocin.
52
Initiation of Maternal Behavior in Rats
How do pregnancy hormones facilitate maternal behavior?
(cont.)
Oxytocin:
• Released from posterior pituitary as a hormone
– During parturition (uterine contractions)
– Postpartum (milk letdown)
… But doesn’t cross the blood-brain barrier!
• Released within the brain as a neurotransmitter
– Rising E, declining P →  OT,  OT receptors
53
Initiation of Maternal Behavior in Rats: Oxytocin
Act on neurons
Hypothalamus
Magnocellular
neurons
Posterior
pituitary
Paraventricular
nucleus (PVN)
+
Supraoptic
nucleus (SON)
Other brain
regions
Parvocellular +
magnocellular
neurons (dendrites)
Released into blood
54
Hormonal functions:
– Uterine contractions
– Milk letdown
Neurotransmitter/neuromodu
lator functions:
– Behavior
– Anxiety
– Social bonding – Etc.
Initiation of Maternal
Behavior in Rats:
Oxytocin
55
Baribeau &
Anagnostou, 2015
Initiation of Maternal Behavior in
Rats: Oxytocin
Rat
• OT typically doesn’t cross the
blood-brain barrier
• To evaluate effects of OT on
brain/behavior, it must be placed
in specific brain regions or in the
cerebral ventricles (series of fluidfilled spaces within the brain).
• Intracerebroventricular (ICV)
treatment allows drug to reach
multiple brain regions.
56
Human
Initiation of Maternal Behavior in Rats
How do pregnancy hormones facilitate maternal behavior?
• ICV OT → maternal behavior (in ovariectomized, E-primed
rats).
• ICV OT antagonist → blocks onset of maternal behavior in
new moms.
Pup Abandonment in Oxytocin
Receptor Knockout Mice
• OT receptor knockout
mice abandon pups
more frequently.
57
OTR
knockouts
Rich et al.
2014
Wildtype
Initiation of Maternal Behavior in Rats
How do pregnancy hormones facilitate maternal behavior?
Conclusions:
1. Estrogen
• Priming + triggering effects.
• Pre-partum E  is essential.
2. Progesterone
• Early pregnancy:
Priming effect (with E) –
stimulates later expression
of maternal behavior.
• Mid/late pregnancy:
58
Inhibits maternal behavior
Pre-partum P  is important.
Initiation of Maternal Behavior in Rats
How do pregnancy hormones facilitate maternal behavior?
Conclusions:
3. Prolactin/Placental Lactogen (prolactin homolog
released during pregnancy)
•
Synergize with E.
•
Pre-partum PRL  is important (stimulated by E).
4. Oxytocin
59
•
Plays a critical role in
maternal behavior.
•
Probably stimulates
maternal behavior by
acting intracerebrally.
End of Lecture 11
60
Lecture 12:
Parental Behavior
Part 2
Biology 178
Instructor
Melina Acosta
Outline of Today’s Lecture
1. Neural Mechanisms of Maternal Behavior in Rodents
2. Intergenerational Transmission of Maternal Behavior in
Rodents
3. Hormonal Influences on Maternal Behavior in Sheep
4. Hormonal Correlates of Maternal Behavior in Primates
5. Hormonal Correlates of Paternal Behavior in Mammals
Learning Objectives
1. Describe the neural circuitry underlying maternal behavior in rodents, and
explain how hormones act on this circuitry to activate maternal behavior.
2. Explain the processes by which maternal behavior is transmitted across
generations in rats.
3. Describe the hormonal and sensory bases of maternal responsiveness
and selectivity in sheep.
4. Describe evidence that maternal behavior is influenced by hormones in
humans.
5. Summarize what is known about hormonal influences on paternal
behavior in mammals.
Neural Mechanisms of Maternal
Behavior in Rodents
Neural Mechanisms of Rodent
Maternal Behavior: Medial Preoptic Area
Correlational evidence that the MPOA influences maternal behavior
in rodents:
• Interaction with pups →  expression of Fos (protein
product of c-fos immediate-early gene) in MPOA
• MPOA receptors for prolactin and E  during pregnancy
• MPOA undergoes structural changes during pregnancy or
estrogen + progesterone treatment
5
Neural Mechanisms
Rodent Behavior:
Neural Mechanisms
of RodentofMaternal
Maternal Behavior:
Medial Area
Preoptic Area
Medial Preoptic
Correlational evidence that the MPOA influences maternal behavior in rodents:
Structural changes during pregnancy or E+P treatment:
Mean # of Basal Dendritic
Branches in MPOA Neurons
Mean area of
Neuronal Cell Bodies
Cortex
(control)
Ovx
6
MPOA
Di- Ovx+ Late- PPestrus E&P Preg. Lact.
“Ovx” = ovariectomized
Keyser-Marcus et al., 2001
Neural Mechanisms of Rodent Maternal Behavior:
Medial Preoptic Area
Experimental evidence that the MPOA influences maternal behavior
in rodents:
• MPOA lesions → abolish maternal behavior
Pup-licking by Postpartum Females
Bar-pressing by Postpartum Females
Sham
lesion
Sham lesion
MPOA
lesion
MPOA lesion
Days from Birth
7
Days from Birth
Neural Mechanisms of Rodent Maternal Behavior:
Medial Preoptic Area
Experimental evidence that the MPOA influences maternal behavior in rodents:
• E, prolactin, or placental lactogen into MPOA → maternal behavior in
ovariectomized or nulliparous females
• Antiestrogen (tamoxifen) implants in MPOA →  maternal behavior
Vehicle
Latency (Days) to
Maternal Behavior
in Steroid-primed,
Nulliparous
Female Rats
8
Bridges & Freemark 1995
Placental
lactogen
Neural Mechanisms of Rodent Maternal Behavior:
Medial Preoptic Area
→ The MPOA is critical for maternal
behavior in rats.
→ The MPOA mediates effects of estrogen,
progesterone and prolactin / placental
lactogen on maternal behavior in rats.
9
Neural Mechanisms of Rodent Maternal Behavior:
Motivation
• E →  oxytocin receptors in MPOA (mediate effects of central
OT, not peripheral).
• Individual diffs. in MPOA OT receptors correlate with differences
in maternal behavior.
Champagne
et al. 2001
→
10
The MPOA mediates effects of oxytocin on maternal behavior in rats.
Neural Mechanisms of Rodent Maternal Behavior:
Motivation
• The onset of maternal behavior requires:
1. Attraction to infants & motivation to behave maternally
2. Inhibition of competing motivational systems (fear, aggression, avoidance)
• Both may be mediated by the MPOA
–
Experience
with pups
MPOA
Maternal
hormones
11
Fear, aggression,
avoidance
+
Attraction, parental
motivation
Neural Mechanisms of Rodent Maternal Behavior:
Motivation
Estrogen
MPOA
Progesterone
Maternal Behavior!
12
Oxytocin
Prolactin
Placental lactogen
Neural Mechanisms of Rodent Maternal Behavior:
Motivation
Nasal epithelium
Vomeronasal organ
Main olf. bulbs
Accessory olf. bulbs
Amygdala
Bed nucleus of stria terminalis
Estrogen
MPOA
Progesterone
Maternal Behavior!
13
Oxytocin
Prolactin
Placental lactogen
Neural Mechanisms of Rodent Maternal Behavior:
Olfaction
Pup odor is usually repulsive to adult rats.
• Lesion VNO + nasal epithelium →
 maternal responsiveness in nulliparous females
• Lesion VNO nerve, medial nucleus of amygdala, or stria terminalis →
 maternal responsiveness in nulliparous females
14
Neural Mechanisms of Rodent Maternal Behavior:
Olfaction
• In the absence of maternal
experience and “pregnancy
hormones,” pup odor inhibits
maternal behavior
• Maternal experience or
pregnancy hormones remove
the aversion to pup odors.
15
Neural Mechanisms of
Rodent Maternal
Behavior: Motivation
Nasal epithelium
Main olf. bulbs
Vomeronasal organ
Accessory olf. bulbs
Amygdala
Bed nucleus of stria terminalis
Estrogen
–
MPOA
Progesterone
Maternal Behavior!
16
Oxytocin
Prolactin
Placental lactogen
Neural Mechanisms of Rodent Maternal Behavior:
Motivation
Olfactory
pathway
–
Fear, aggression,
avoidance
Experience
with pups
MPOA
Attraction, parental
motivation
Maternal
hormones
+
Reward
pathway
17
Neural Mechanisms of Rodent Maternal Behavior:
Motivation
Conclusions:
Hormones and pup stimuli act on neural
circuitry to:
1. Stimulate maternal motivation via the
reward pathway.
2. Inhibit competing motivational systems
(e.g., aggression, fear) in response to
olfactory cues from pups.
18
Intergenerational Transmission of
Maternal Behavior in Rats
Intergenerational Transmission of Mammalian
Maternal Behavior
• Rat mothers (dams) who perform high levels of licking/grooming
(LG) of their pups have daughters who perform high LG toward
their own pups
• Female pups who are born to low-LG (“bad”) dams but raised by
high-LG (“good”) dams become high-LG dams.
• So, the transmission of maternal behavior from mothers to
daughters isn’t based solely on genetics but also on experience.
How does this occur?
→ Epigenetic modification of gene expression.
20
Intergenerational Transmission of Mammalian
Maternal Behavior
Epigenetic modification of gene expression:
• Changes in gene expression that are NOT mediated by
changes in nucleotide sequences
• Induced by environment/experience
• Can be transmitted to future generations
• Major types:
– DNA methylation → decreases gene expression
– Histone modification → increases gene expression
21
Intergenerational Transmission of Mammalian
Maternal Behavior
Epigenetic modification of gene expression
22
Intergenerational Transmission of Mammalian
Maternal Behavior
• Rat dam (“High LG”)
– High levels of licking/grooming (LG) of pups →
• Daughters of high-LG dam:
– Low methylation of promotor region for estrogen receptor a
(ERa) gene in MPOA →
– High estrogen receptor ERa expression in MPOA →
– High oxytocin receptor (OTR) expression in MPOA →
– In adulthood, high LG toward own pups
23
Intergenerational
Transmission of
Mammalian
Maternal
Behavior
Inter-Individual Variation in
Maternal Care
Low
LG
High
LG
Maternal Licking/Grooming
Oxytocin
Receptor
Expression
Methylation of the ER
Promoter Region
ERa Expression in the MPOA
Champagne 2008, 2011
24
Hormonal Influences on Maternal
Behavior in Sheep
Hormonal Influences on Maternal Behavior In
Sheep
Differences from rats:
• Live in flocks
• Seasonal breeders (give birth only in spring)
Risk of providing care
to an unrelated lamb
• Form special attachments to their own lambs; reject other
lambs
• Do not show sensitization (infant-induced parental care)
26
Hormonal Influences on Maternal Behavior In
Sheep
Onset of maternal responsiveness toward any lamb:
Typically requires…
• High progesterone levels followed by decline
• High estrogen levels
• Vaginocervical stimulation (during
parturition) – stimulates oxytocin secretion
•Olfactory cues from lamb (especially amniotic
fluid)
•Activity in medial preoptic area
27
Hormonal Influences on Maternal Behavior In
Sheep
Onset of maternal responsiveness toward any lamb:
28
Hormonal Influences on Maternal Behavior In
Sheep
Onset of maternal selectivity toward any lamb:
Requires…
• Exposure to lamb’s odor during first few hours after parturition
• Memorization of lamb’s individual odor
29
Hormonal Correlates of Maternal
Behavior in Primates
Hormonal Correlates of Maternal Behavior In
Non-Human Primates
Relatively few studies:
• Maternal behavior in primates has often been
thought to be determined by experience, not
hormones
Recent studies:
• Indicate that hormones can play a role
in primate maternal behavior.
31
Hormonal Correlates of Maternal Behavior In
Non-Human Primates
Rhesus macaques (Holman & Goy 1980):
• Infant was placed in cage with nulliparous or multiparous
(ovary-intact, ovariectomized, or menopausal) female.
• Multiparous females retrieved infant, regardless of hormonal
condition.
• Nulliparous females never retrieved or held infant.
Suggests that experience, not hormones, plays a
critical role in the onset of maternal behavior.
32
Hormonal Correlates of Maternal Behavior In
Non-Human Primates
Macaques (Maestripieri & Zehr 1998):
• Observed rates of infant-handling among females in large
naturalistic groups
• Infant-handling increased across pregnancy and correlated with
the E:P ratio
33
Hormonal Correlates of Maternal Behavior In
Non-Human Primates
34
Hormonal Correlates of Maternal Behavior In
Non-Human Primates
Macaques (Maestripieri & Zehr 1998):
• E-treatment increased infant-handling in ovariectomized females
• BUT even untreated, ovariectomized females showed some
interest in infants
Suggests that E2 can increase
maternal behavior in
primates but isn’t essential
for it!
35
Hormonal Correlates of Maternal Behavior In
Humans
Caveats:
• No universal set of maternal behaviors.
• Identical maternal behaviors (except lactation)
may be provided by other caregivers.
• Can’t experimentally manipulate hormones
(except by intranasal oxytocin).
• Most studies are correlational – can’t determine
causal relationships.
36
Hormonal Correlates of Maternal Behavior In
Humans
• Plasma estrogen and progesterone levels during pregnancy correlate
with mothers’ subsequent…
– Attachment to the infant
– Feelings of well-being
• Plasma oxytocin levels correlate with some aspects of maternal
behavior, such as…
– Affectionate contact
– Gazing into the baby’s eyes
• Plasma cortisol levels correlate with some aspects
of maternal behavior.
37
Hormonal Correlates of Maternal Behavior In
Humans
Prepartum Estrogen:Progesterone Ratio
Sensitivity to Infant 1 Year Postpartum
High
sensitivity
Low
sensitivity
Glynn et al. 2016
“Sensitivity” – measured by mother’s
responsiveness to infant’s mood/affect.
38
Associated with quality of mother-infant
attachment.
Hormonal Correlates of Maternal Behavior In
Humans
Postpartum Plasma Oxytocin
Touch vs. Plasma OT
AffectionateContact
Contact
Affectionate
High OT
Low OT
Aptner-Levi et al. 2014
Feldman et al. 2012
39
Hormonal Correlates of Maternal Behavior In
Humans
Conclusions:
40
•
Components of maternal behavior correlate with
prepartum estrogen and progesterone levels.
•
Components of maternal behavior correlate with
postpartum oxytocin levels (in the blood).
•
Components of maternal behavior / responsiveness to
infant cues correlate with cortisol levels.
•
Hormone-behavior interactions may be modulated by
maternal experience.
•
Unclear if and how these hormones influence maternal
behavior.
Hormonal Correlates of Paternal
Behavior in Mammals
Hormonal Correlates of Mammalian Paternal Behavior
• Rats:
– Paternal behavior (after sensitization) is not associated with
any distinct hormonal changes.
• BUT…
– Rats don’t normally engage in paternal behavior!
– Studies of species in which males
do engage in paternal behavior
(biparental species) are much more
informative!
42
Hormonal Correlates of Mammalian Paternal Behavior
• Organizational effects:
In many rodent species:
Perinatal androgen exposure →
 parental responsiveness
• Activational effects:
In adulthood, paternal behavior is usually
associated with…
– Elevated prolactin levels
– Decreased testosterone levels
43
Hormonal Correlates of Mammalian Paternal Behavior
California Mouse
PRL
44
Common Marmoset
PRL
Paternal behavior correlates with
prolactin levels in fathers in
biparental species.
T
Hormonal Correlates of Paternal Behavior in Humans
Fleming et al. 2002:
• Played calls of baby cries (pain, hunger) to new first-time
fathers, experienced fathers, and non-fathers.
• Fathers were more sympathetic to babies than non-fathers.
• Fathers had lower T levels than non-fathers (also found in many
other studies).
• Prolactin rose in response to baby cries…
but only in experienced fathers.
• Responsiveness to baby cries
was associated with low T and
high prolactin.
45
Hormonal Correlates
of Paternal Behavior
in Humans
Need to Respond
Sympathy
46
Fleming et al. 2002
Hormonal
Hormonal
Correlates
Correlates
of Paternal
Behavior
of Paternal
inBehavior
Humansin
Humans
• Fathers’ salivary
testosterone levels are
negatively associated
with paternal behavior
toward their infants.
Affectionate Touch
Gaze to Infant’s Body
Motherese
Weisman et al. 2014
47
Father’s Testosterone
Hormonal Correlates of Mammalian Paternal Behavior
• Activational effects –
In adulthood, paternal behavior is usually associated with…
– Elevated prolactin levels
– Decreased testosterone levels
• BUT…
– Prolactin manipulations don’t generally
alter paternal behavior.
– Testosterone manipulations have
variable effects on paternal behavior.
• SO…
– Activational effects on paternal behavior
are not understood and might differ
across species!
48
Hormonal Correlates of Paternal Behavior in Humans
• Intranasal oxytocin treatment changes fathers’ behavior towards their
toddlers during play sessions.
Stucture =
supportiveness
of child’s
learning &
exploration
Nabor et al. 2010
49
Placebo
OT
Hormonal Correlates of Paternal Behavior in Humans
Conclusions:
Paternal behavior in humans correlates negatively with
testosterone.
Paternal behavior in humans correlates positively with
oxytocin and prolactin.
Associations between paternal behavior and hormones
may be modulated by experience.
Based mostly on correlational studies! More experimental
studies are needed!
50
End of Lecture 12
Lecture 12:
Parental Behavior
Part 2
Biology 178
Instructor
Melina Acosta
Outline of Today’s Lecture
1. Neural Mechanisms of Maternal Behavior in Rodents
2. Intergenerational Transmission of Maternal Behavior in
Rodents
3. Hormonal Influences on Maternal Behavior in Sheep
4. Hormonal Correlates of Maternal Behavior in Primates
5. Hormonal Correlates of Paternal Behavior in Mammals
Learning Objectives
1. Describe the neural circuitry underlying maternal behavior in rodents, and
explain how hormones act on this circuitry to activate maternal behavior.
2. Explain the processes by which maternal behavior is transmitted across
generations in rats.
3. Describe the hormonal and sensory bases of maternal responsiveness
and selectivity in sheep.
4. Describe evidence that maternal behavior is influenced by hormones in
humans.
5. Summarize what is known about hormonal influences on paternal
behavior in mammals.
Neural Mechanisms of Maternal
Behavior in Rodents
Neural Mechanisms of Rodent
Maternal Behavior: Medial Preoptic Area
Correlational evidence that the MPOA influences maternal behavior
in rodents:
• Interaction with pups →  expression of Fos (protein
product of c-fos immediate-early gene) in MPOA
• MPOA receptors for prolactin and E  during pregnancy
• MPOA undergoes structural changes during pregnancy or
estrogen + progesterone treatment
5
Neural Mechanisms
Rodent Behavior:
Neural Mechanisms
of RodentofMaternal
Maternal Behavior:
Medial Area
Preoptic Area
Medial Preoptic
Correlational evidence that the MPOA influences maternal behavior in rodents:
Structural changes during pregnancy or E+P treatment:
Mean # of Basal Dendritic
Branches in MPOA Neurons
Mean area of
Neuronal Cell Bodies
Cortex
(control)
Ovx
6
MPOA
Di- Ovx+ Late- PPestrus E&P Preg. Lact.
“Ovx” = ovariectomized
Keyser-Marcus et al., 2001
Neural Mechanisms of Rodent Maternal Behavior:
Medial Preoptic Area
Experimental evidence that the MPOA influences maternal behavior
in rodents:
• MPOA lesions → abolish maternal behavior
Pup-licking by Postpartum Females
Bar-pressing by Postpartum Females
Sham
lesion
Sham lesion
MPOA
lesion
MPOA lesion
Days from Birth
7
Days from Birth
Neural Mechanisms of Rodent Maternal Behavior:
Medial Preoptic Area
Experimental evidence that the MPOA influences maternal behavior in rodents:
• E, prolactin, or placental lactogen into MPOA → maternal behavior in
ovariectomized or nulliparous females
• Antiestrogen (tamoxifen) implants in MPOA →  maternal behavior
Vehicle
Latency (Days) to
Maternal Behavior
in Steroid-primed,
Nulliparous
Female Rats
8
Bridges & Freemark 1995
Placental
lactogen
Neural Mechanisms of Rodent Maternal Behavior:
Medial Preoptic Area
→ The MPOA is critical for maternal
behavior in rats.
→ The MPOA mediates effects of estrogen,
progesterone and prolactin / placental
lactogen on maternal behavior in rats.
9
Neural Mechanisms of Rodent Maternal Behavior:
Motivation
• E →  oxytocin receptors in MPOA (mediate effects of central
OT, not peripheral).
• Individual diffs. in MPOA OT receptors correlate with differences
in maternal behavior.
Champagne
et al. 2001
→
10
The MPOA mediates effects of oxytocin on maternal behavior in rats.
Neural Mechanisms of Rodent Maternal Behavior:
Motivation
• The onset of maternal behavior requires:
1. Attraction to infants & motivation to behave maternally
2. Inhibition of competing motivational systems (fear, aggression, avoidance)
• Both may be mediated by the MPOA
–
Experience
with pups
MPOA
Maternal
hormones
11
Fear, aggression,
avoidance
+
Attraction, parental
motivation
Neural Mechanisms of Rodent Maternal Behavior:
Motivation
Estrogen
MPOA
Progesterone
Maternal Behavior!
12
Oxytocin
Prolactin
Placental lactogen
Neural Mechanisms of Rodent Maternal Behavior:
Motivation
Nasal epithelium
Vomeronasal organ
Main olf. bulbs
Accessory olf. bulbs
Amygdala
Bed nucleus of stria terminalis
Estrogen
MPOA
Progesterone
Maternal Behavior!
13
Oxytocin
Prolactin
Placental lactogen
Neural Mechanisms of Rodent Maternal Behavior:
Olfaction
Pup odor is usually repulsive to adult rats.
• Lesion VNO + nasal epithelium →
 maternal responsiveness in nulliparous females
• Lesion VNO nerve, medial nucleus of amygdala, or stria terminalis →
 maternal responsiveness in nulliparous females
14
Neural Mechanisms of Rodent Maternal Behavior:
Olfaction
• In the absence of maternal
experience and “pregnancy
hormones,” pup odor inhibits
maternal behavior
• Maternal experience or
pregnancy hormones remove
the aversion to pup odors.
15
Neural Mechanisms of
Rodent Maternal
Behavior: Motivation
Nasal epithelium
Main olf. bulbs
Vomeronasal organ
Accessory olf. bulbs
Amygdala
Bed nucleus of stria terminalis
Estrogen
–
MPOA
Progesterone
Maternal Behavior!
16
Oxytocin
Prolactin
Placental lactogen
Neural Mechanisms of Rodent Maternal Behavior:
Motivation
Olfactory
pathway
–
Fear, aggression,
avoidance
Experience
with pups
MPOA
Attraction, parental
motivation
Maternal
hormones
+
Reward
pathway
17
Neural Mechanisms of Rodent Maternal Behavior:
Motivation
Conclusions:
Hormones and pup stimuli act on neural
circuitry to:
1. Stimulate maternal motivation via the
reward pathway.
2. Inhibit competing motivational systems
(e.g., aggression, fear) in response to
olfactory cues from pups.
18
Intergenerational Transmission of
Maternal Behavior in Rats
Intergenerational Transmission of Mammalian
Maternal Behavior
• Rat mothers (dams) who perform high levels of licking/grooming
(LG) of their pups have daughters who perform high LG toward
their own pups
• Female pups who are born to low-LG (“bad”) dams but raised by
high-LG (“good”) dams become high-LG dams.
• So, the transmission of maternal behavior from mothers to
daughters isn’t based solely on genetics but also on experience.
How does this occur?
→ Epigenetic modification of gene expression.
20
Intergenerational Transmission of Mammalian
Maternal Behavior
Epigenetic modification of gene expression:
• Changes in gene expression that are NOT mediated by
changes in nucleotide sequences
• Induced by environment/experience
• Can be transmitted to future generations
• Major types:
– DNA methylation → decreases gene expression
– Histone modification → increases gene expression
21
Intergenerational Transmission of Mammalian
Maternal Behavior
Epigenetic modification of gene expression
22
Intergenerational Transmission of Mammalian
Maternal Behavior
• Rat dam (“High LG”)
– High levels of licking/grooming (LG) of pups →
• Daughters of high-LG dam:
– Low methylation of promotor region for estrogen receptor a
(ERa) gene in MPOA →
– High estrogen receptor ERa expression in MPOA →
– High oxytocin receptor (OTR) expression in MPOA →
– In adulthood, high LG toward own pups
23
Intergenerational
Transmission of
Mammalian
Maternal
Behavior
Inter-Individual Variation in
Maternal Care
Low
LG
High
LG
Maternal Licking/Grooming
Oxytocin
Receptor
Expression
Methylation of the ER
Promoter Region
ERa Expression in the MPOA
Champagne 2008, 2011
24
Hormonal Influences on Maternal
Behavior in Sheep
Hormonal Influences on Maternal Behavior In
Sheep
Differences from rats:
• Live in flocks
• Seasonal breeders (give birth only in spring)
Risk of providing care
to an unrelated lamb
• Form special attachments to their own lambs; reject other
lambs
• Do not show sensitization (infant-induced parental care)
26
Hormonal Influences on Maternal Behavior In
Sheep
Onset of maternal responsiveness toward any lamb:
Typically requires…
• High progesterone levels followed by decline
• High estrogen levels
• Vaginocervical stimulation (during
parturition) – stimulates oxytocin secretion
•Olfactory cues from lamb (especially amniotic
fluid)
•Activity in medial preoptic area
27
Hormonal Influences on Maternal Behavior In
Sheep
Onset of maternal responsiveness toward any lamb:
28
Hormonal Influences on Maternal Behavior In
Sheep
Onset of maternal selectivity toward any lamb:
Requires…
• Exposure to lamb’s odor during first few hours after parturition
• Memorization of lamb’s individual odor
29
Hormonal Correlates of Maternal
Behavior in Primates
Hormonal Correlates of Maternal Behavior In
Non-Human Primates
Relatively few studies:
• Maternal behavior in primates has often been
thought to be determined by experience, not
hormones
Recent studies:
• Indicate that hormones can play a role
in primate maternal behavior.
31
Hormonal Correlates of Maternal Behavior In
Non-Human Primates
Rhesus macaques (Holman & Goy 1980):
• Infant was placed in cage with nulliparous or multiparous
(ovary-intact, ovariectomized, or menopausal) female.
• Multiparous females retrieved infant, regardless of hormonal
condition.
• Nulliparous females never retrieved or held infant.
Suggests that experience, not hormones, plays a
critical role in the onset of maternal behavior.
32
Hormonal Correlates of Maternal Behavior In
Non-Human Primates
Macaques (Maestripieri & Zehr 1998):
• Observed rates of infant-handling among females in large
naturalistic groups
• Infant-handling increased across pregnancy and correlated with
the E:P ratio
33
Hormonal Correlates of Maternal Behavior In
Non-Human Primates
34
Hormonal Correlates of Maternal Behavior In
Non-Human Primates
Macaques (Maestripieri & Zehr 1998):
• E-treatment increased infant-handling in ovariectomized females
• BUT even untreated, ovariectomized females showed some
interest in infants
Suggests that E2 can increase
maternal behavior in
primates but isn’t essential
for it!
35
Hormonal Correlates of Maternal Behavior In
Humans
Caveats:
• No universal set of maternal behaviors.
• Identical maternal behaviors (except lactation)
may be provided by other caregivers.
• Can’t experimentally manipulate hormones
(except by intranasal oxytocin).
• Most studies are correlational – can’t determine
causal relationships.
36
Hormonal Correlates of Maternal Behavior In
Humans
• Plasma estrogen and progesterone levels during pregnancy correlate
with mothers’ subsequent…
– Attachment to the infant
– Feelings of well-being
• Plasma oxytocin levels correlate with some aspects of maternal
behavior, such as…
– Affectionate contact
– Gazing into the baby’s eyes
• Plasma cortisol levels correlate with some aspects
of maternal behavior.
37
Hormonal Correlates of Maternal Behavior In
Humans
Prepartum Estrogen:Progesterone Ratio
Sensitivity to Infant 1 Year Postpartum
High
sensitivity
Low
sensitivity
Glynn et al. 2016
“Sensitivity” – measured by mother’s
responsiveness to infant’s mood/affect.
38
Associated with quality of mother-infant
attachment.
Hormonal Correlates of Maternal Behavior In
Humans
Postpartum Plasma Oxytocin
Touch vs. Plasma OT
AffectionateContact
Contact
Affectionate
High OT
Low OT
Aptner-Levi et al. 2014
Feldman et al. 2012
39
Hormonal Correlates of Maternal Behavior In
Humans
Conclusions:
40
•
Components of maternal behavior correlate with
prepartum estrogen and progesterone levels.
•
Components of maternal behavior correlate with
postpartum oxytocin levels (in the blood).
•
Components of maternal behavior / responsiveness to
infant cues correlate with cortisol levels.
•
Hormone-behavior interactions may be modulated by
maternal experience.
•
Unclear if and how these hormones influence maternal
behavior.
Hormonal Correlates of Paternal
Behavior in Mammals
Hormonal Correlates of Mammalian Paternal Behavior
• Rats:
– Paternal behavior (after sensitization) is not associated with
any distinct hormonal changes.
• BUT…
– Rats don’t normally engage in paternal behavior!
– Studies of species in which males
do engage in paternal behavior
(biparental species) are much more
informative!
42
Hormonal Correlates of Mammalian Paternal Behavior
• Organizational effects:
In many rodent species:
Perinatal androgen exposure →
 parental responsiveness
• Activational effects:
In adulthood, paternal behavior is usually
associated with…
– Elevated prolactin levels
– Decreased testosterone levels
43
Hormonal Correlates of Mammalian Paternal Behavior
California Mouse
PRL
44
Common Marmoset
PRL
Paternal behavior correlates with
prolactin levels in fathers in
biparental species.
T
Hormonal Correlates of Paternal Behavior in Humans
Fleming et al. 2002:
• Played calls of baby cries (pain, hunger) to new first-time
fathers, experienced fathers, and non-fathers.
• Fathers were more sympathetic to babies than non-fathers.
• Fathers had lower T levels than non-fathers (also found in many
other studies).
• Prolactin rose in response to baby cries…
but only in experienced fathers.
• Responsiveness to baby cries
was associated with low T and
high prolactin.
45
Hormonal Correlates
of Paternal Behavior
in Humans
Need to Respond
Sympathy
46
Fleming et al. 2002
Hormonal
Hormonal
Correlates
Correlates
of Paternal
Behavior
of Paternal
inBehavior
Humansin
Humans
• Fathers’ salivary
testosterone levels are
negatively associated
with paternal behavior
toward their infants.
Affectionate Touch
Gaze to Infant’s Body
Motherese
Weisman et al. 2014
47
Father’s Testosterone
Hormonal Correlates of Mammalian Paternal Behavior
• Activational effects –
In adulthood, paternal behavior is usually associated with…
– Elevated prolactin levels
– Decreased testosterone levels
• BUT…
– Prolactin manipulations don’t generally
alter paternal behavior.
– Testosterone manipulations have
variable effects on paternal behavior.
• SO…
– Activational effects on paternal behavior
are not understood and might differ
across species!
48
Hormonal Correlates of Paternal Behavior in Humans
• Intranasal oxytocin treatment changes fathers’ behavior towards their
toddlers during play sessions.
Stucture =
supportiveness
of child’s
learning &
exploration
Nabor et al. 2010
49
Placebo
OT
Hormonal Correlates of Paternal Behavior in Humans
Conclusions:
Paternal behavior in humans correlates negatively with
testosterone.
Paternal behavior in humans correlates positively with
oxytocin and prolactin.
Associations between paternal behavior and hormones
may be modulated by experience.
Based mostly on correlational studies! More experimental
studies are needed!
50
End of Lecture 12
Lecture 9:
Female Reproductive Behavior
Part 1
Biology 178
Instructor
Melina Acosta
Outline of Today’s Lecture
1. Overview of Female Reproductive Behavior
2. The Human Menstrual Cycle
a) The Follicular Phase
b) Ovulation
c) The Luteal Phase and Early Pregnancy
3. Hormones and Female Reproductive Behavior in Primates
2
Learning Objectives
1. Define and describe the major components of female sexual behavior.
2. Describe the changes in the hypothalamic-pituitary-ovarian axis that
occur over the course of the human menstrual cycle and explain how
these changes relate to concurrent changes in the brain, ovaries, and
uterus.
3. Describe how sexual behavior in female primates, including women, is
influenced by, or correlates with, hormonal changes across the ovarian
cycle.
3
Female Reproductive Behavior:
Overview
Female Sexual Behavior: Definitions
•
Estrous
– “In a frenzy,” “possessed by the gadfly”
– Willing to mate (“in heat”, “in estrus”)
– Behavioral term
•
Estrous cycle
– Cyclical pattern of estrous behavior
•
Menstrual cycle
– Cyclical pattern of hormonal changes characterized by
regular sloughing off of the endometrium (inner lining of
the uterus)
– Only in humans and some other primates
5
Female Sexual Behavior: Components
1. Attractivity
– Female’s stimulus value (attractiveness) for a particular
male (how hot is she?)
– Measured by male’s behavior
– Can involve behavioral & non-behavioral cues (e.g.,
olfactory or visual cues) from the female
6
Female Sexual Behavior: Components
1. Attractivity
2. Proceptivity
– Female’s behavioral role in initiating copulation
– Can include approaches, contact, solicitation, mounting,
etc.
– Can overlap with attractivity
7
Female Sexual Behavior: Components
2. Proceptivity (cont.)
Unusual proceptive behavior in capuchin monkeys

8
Female Sexual Behavior: Components
1. Attractivity
2. Proceptivity
3. Receptivity
– Female’s willingness to permit/facilitate copulation
– Can include postures, maintenance of contact, specific
behaviors
– Can overlap with proceptivity
9
Female
Rats
Female Sexual
Sexual Behavior:
Behavior: Rats
Behavioral estrus occurs every 4-5 nights
– Approaches to male
– Hopping, darting, ear-wiggling
– Lordosis (reflex)
Female pacing of copulation
– In nature, females control the patterning of
copulation (e.g., by approach/withdrawal)
10
Female Sexual Behavior: Primates
•
May or may not have clear estrous cycles.
•
May or may not have stereotyped copulatory behaviors.
•
Can be highly selective.
•
Can use “sexual behavior” for non-sexual purposes.
 Suggests greater emancipation (independence) of sexual
behavior from hormones in primates!
11
The Human Menstrual Cycle:
The Follicular Phase
Human Menstrual Cycle: Overview
• Follicular phase
~10-20 days (variable)
• Ovulation
1 day
• Luteal phase
14-16 days (consistent)
Ovarian
cycle –
occurs
simultaneously
with…
• Menstruation
~3-5
Starts on Day 1 of cycle (by definition)
Corresponds to early follicular phase
• Proliferative phase
~9-11 days
Corresponds to mid- to late follicular phase
• Secretory phase
~14 days
Corresponds to luteal phase
Uterine
cycle
13
Human Menstrual Cycle: Follicular Phase
The Ovarian Cycle
Follicular Phase
Day of
Cycle:
1
3
5
7
9
Ovulation
11
13
15
Luteal Phase
17
Menstruation Proliferative Phase
19
21
23
25
27
29
Secretory Phase
The Uterine Cycle
14
Human Menstrual Cycle: Follicular Phase
Follicular Phase
• First part of the ovarian cycle
• Dominated by developing follicles in the ovary
• Follicle: oocyte (egg cell) + surrounding cell layers
– Nourishes and protect oocytes
– Secretes hormones
15
Human Menstrual Cycle: Follicular Phase
Follicles
• Follicular cells surrounding the oocyte:
– Thecal cells:
Synthesize androgens under the influence of LH
– Granulosa cells:
Aromatize androgens to estrogens under the influence of FSH
16
Human Menstrual Cycle: Follicular Phase
Thecal and granulosa cells collaborate to produce estrogen.
Anterior
Pituitary
Estrogens
FSH
Granulosa
Cell
LH
Thecal
Cell
(Aromatase)
Ovary
Androgens
17
Human Menstrual Cycle: Follicular Phase
Thecal and granulosa cells collaborate to produce estrogen
AR = aromatase
18
Human Menstrual Cycle: Follicular Phase
Follicular Phase
Before birth
Cow follicle
Monthly
cycles
Ultrasound
Cross-section
thru follicle
19
Human Menstrual Cycle: Follicular Phase
Negative feedback
– Hypothalamus
Gonadotropin-releasing
hormone (GnRH)
– Anterior Pituitary
Luteinizing
hormone (LH)
Follicle-stim. –
hormone (FSH)
Follicles in Ovary
(devt./growth)
Estrogen
Inhibin
Endometrium
Brain/Behavior
Other Tissues
20
Human Menstrual Cycle: Follicular Phase
Hypothalamic-Pituitary-Ovarian Axis
• GnRH →  LH,FSH → follicular growth and development
• Developing follicles secrete increasing E, inhibin
• E, inhibin negative feedback →  GnRH,  LH  FSH
21
Human Menstrual Cycle: Follicular Phase
A single, dominant follicle emerges, matures fully, and suppresses
development of other follicles. How??
• The dominant follicle…
– Secretes large amounts of E and inhibin →
LH and FSH drop to very low levels.
– Increases its expression of LH and FSH receptors→
becomes highly sensitive to gonadotropins.
– Becomes more vascularized →
gets increased delivery of LH & FSH.
Atretic follicle
• Other follicles do not undergo these
changes → cannot survive under
conditions of very low LH and FSH →
undergo atresia (degeneration).
22
Human Menstrual Cycle: Follicular Phase
Subordinate
follicles
Dominant
follicle
23
Human Menstrual Cycle: Follicular Phase
Uterus
– Early follicular phase:
Low E, P → menstruation (days 1-~5)
– Mid- to late follicular phase:
Rising E → growth of endometrium
(proliferative phase) (~ days 6-14)
Menstrual
Phase
Proliferative
Phase
24
Human Menstrual
Cycle: Follicular
Phase
LH
Progesterone
Silverthorn 2009
25
The Human Menstrual Cycle:
Ovulation
Human Menstrual Cycle: Ovulation
The Ovarian Cycle
Follicular Phase
Day of
Cycle:
1
3
5
7
9
Ovulation
11
13
15
Luteal Phase
17
Menstruation Proliferative Phase
19
21
23
25
27
29
Secretory Phase
The Uterine Cycle
27
Human Menstrual Cycle: Ovulation
Ovulation
• Release of ovum from follicle
• Triggered by LH surge in response to E elevation (positive
feedback)
Pig ovary at ovulation
Ovum
Rupture site
28
Human Menstrual Cycle: Ovulation
Ovulation
29
Human Menstrual Cycle: Ovulation
Human ovulation, photographed during a hysterectomy
(lasted ~15 minutes)
1
2
3
4
30
Human Menstrual Cycle: Ovulation
Hypothalamic-Pituitary-Ovarian Axis
• Sustained high E from developing follicles exerts
positive feedback on hypothalamus and ant. pituitary:
→  GnRH release from hypothalamus
→  GnRH receptors in anterior pituitary
→  LH, FSH release from anterior pituitary
• LH surge triggers ovulation:
Dominant follicle ruptures; oocyte is ejected from
ovary and enters oviduct.
31
feedback
Positive
feedback
Negative
Human Menstrual Cycle: Ovulation
+– Hypothalamus
+– Anterior Pituitary
Gonadotropin-releasing
hormone (GnRH)
Luteinizing
hormone (LH)
Follicle-stim. ––
hormone (FSH)
Follicles in Ovary
(devt./growth)
Ovulation
Estrogen
Inhibin
Endometrium
Brain/Behavior
Other Tissues
32
Human Menstrual
Cycle: Ovulation
Progesterone
Silverthorn 2009
33
The Human Menstrual Cycle:
The Luteal Phase & Pregnancy
Human Menstrual Cycle: Luteal Phase
Luteal Phase
• After ovulation
• Corpus luteum (CL) develops from ovulated follicle.
– Histological and biochemical changes
– Vascularization
Pig ovaries
Hamster ovaries
With cigarette
smoke
Control
35
Human Menstrual Cycle: Luteal Phase
Human ovary with
fully developed
corpus luteum
36
Human Menstrual Cycle: Luteal Phase
Luteal Phase
Cow CL
CL
Ultrasound
Ovary cut
thru CL
37
Human Menstrual Cycle: Luteal Phase
Negative feedback
– Hypothalamus
Gonadotropin-releasing
hormone (GnRH)
– Anterior Pituitary
Luteinizing
hormone (LH)
Follicle-stim. –
hormone (FSH)
Corpus Luteum
in Ovary
Progesterone+
Inhibin
Estrogen
Endometrium
Brain/Behavior
Other Tissues
38
Human Menstrual Cycle: Luteal Phase
Hypothalamic-Pituitary-Ovarian Axis (non-conceptive cycle)
• LH surge causes ovulated follicle to develop into corpus luteum (CL)
• CL secretes P, E, and inhibin
• P, E, inhibin exert neg feedback →  GnRH,  LH,  FSH
39
Human Menstrual Cycle: Luteal Phase
Hypothalamic-Pituitary-Ovarian Axis (non-conceptive cycle)
– LH surge causes ovulated follicle to develop into corpus luteum
(CL)
– CL secretes P, E, and inhibin
– P, E, inhibin exert neg. feedback → GnRH, LH, FSH
– After ~14 days, CL regresses (if no conception)
–  P,  E,  inhibin →
 GnRH,  LH,  FSH
–  LH,  FSH → development
Start of next follicular phase
of
new cohort of follicles
40
Human Menstrual Cycle: Luteal Phase
Negative feedback
– Hypothalamus
Gonadotropin-releasing
hormone (GnRH)
– Anterior Pituitary
Luteinizing
hormone (LH)
Follicle-stim. –
hormone (FSH)
Corpus
Luteum
Development
of
in Ovary
New
Follicles
Progesterone+
Inhibin
Estrogen
Endometrium
Endometrium
breaks down 
Brain/Behavior
Menstruation
Other Tissues
41
Human Menstrual Cycle: Luteal Phase
Uterus (non-conceptive cycle)
– P + E → endometrium prepares for pregnancy
(secretory phase)
– End of luteal phase/beginning of next follicular phase:
 P,  E → endometrium sloughs off (menstruation)
Menstrual
Phase
Proliferative
Phase
Secretory
Phase
42
Human Menstrual
Cycle: Luteal
Phase
Silverthorn 2009
43
Human Menstrual Cycle: Summary
44
Human Menstrual Cycle: Timing of Fertility
• Maximum fertility
– Sperm can live in the female reproductive tract
up to 8 days (usually 1-5 days).
– Maximum fertility: 4-5 days before through 1-2
days after ovulation.
• Calculating the timing of ovulation
– Luteal phase (ovulation to menstruation):
usually 14-16 days (consistent within women).
– Follicular phase (menstruation to ovulation):
more variable.
– So, timing of maximum fertility can be determined
retroactively but not proactively!
45
Human Menstrual Cycle: Ovulation
The Ovarian Cycle
Follicular Phase
Day of
Cycle:
1
3
5
7
9
Ovulation
11
13
15
Luteal Phase
17
Menstruation Proliferative Phase
19
21
23
25
27
29
Secretory Phase
The Uterine Cycle
46
Human Menstrual Cycle: Early Pregnancy
• If conception occurs…
– Blastocyst secretes human chorionic gonadotropin
(hCG) – structurally and functionally similar to LH.
– hCG “rescues” the CL.
– CL survives & secretes P for ~ 7 weeks.
– P maintains endometrium.
47
Hormones and Female
Reproductive Behavior in
Primates
Hormonal
Correlates of
Female Sexual
Behavior in
Primates: The
Ovarian Cycle
Latency to gain
access to male
(Proceptivity)
Mounts rec’d.
per minute
(Attractivity)
Day of ovulation
Number of
ejaculations
Time to barpress 250X
(Receptivity)
(Proceptivity)
Minutes until
ejaculation
(Receptivity)
Day of ovulation
Rhesus
monkeys
49
Hormonal Correlates of Female Sexual Behavior in
Primates: The Ovarian Cycle
Attractivity
(Sexual behavs. received from males)
Japanese
macaques
Mount
receive
Hold
receive
Other
receive
Follic.
O’Neill et al. 2005
Periovul.
Luteal
50
Hormonal Correlates of Female Sexual Behavior in
Primates: The Ovarian Cycle
Japanese
macaques
Proceptivity
(Sexual behavs. performed to males)
Mount
direct
Other Estrous
direct
call
Hold
direct
Follic.
O’Neill et al. 2005
Periovul.
Luteal
51
Hormonal Correlates of Female Sexual Behavior in
Primates: The Ovarian Cycle
• Studies of women in long-term relationships have found that
sexual behavior…
1. Does not change across the menstrual cycle, OR
2. May peak around ovulation, OR
Fertile period
3. May show a smaller peak
around menstruation.
• Erotic thoughts, masturbation
peak around ovulation
Seems to be caused by
changes in proceptivity,
not attractivity.
Wilcox et al.
2004
52
Hormonal Correlates of Female Sexual Behavior in
Primates: The Ovarian Cycle
Around the time of ovulation, women…
• Engage in more “extra-pair” flirtation
• Show increased preferences for masculine men (based on faces,
bodies, behavior, voices, or odors)
53
Hormonal Correlates of Female Sexual Behavior in
Primates: The Ovarian Cycle
Around the time of ovulation, women…
• Dress more provocatively
Estrogen:
Progesterone
ratio
Probability
of wearing
red
Eisenbruch
et al. 2015
54
Hormonal Correlates of Female Sexual Behavior in
Primates: The Ovarian Cycle
Around the time of ovulation, women…
• Smell better to men than at other times
• Receive more “mate-guarding” by their partners
Around the time of ovulation, lap dancers…
• Make more money in tips!
Miller et al.
2007
55
Hormonal Correlates of Female Sexual Behavior in
Primates: Estrogen
Sexual behavior is usually enhanced by the steroid hormone milieu
occurring around the time of peak fertility: ovulation.
• Estrogen levels peak just before ovulation.
• Estrogens typically enhance attractivity, receptivity, and
proceptivity.
Ovariectomized marmosets
Dixson
1998
56
Hormonal Correlates of Female Sexual Behavior in
Primates: Androgens
Androgens can increase female sexual behavior in
women, rhesus monkeys, and some other species.
Androgens…
• Are secreted by the ovaries or adrenal cortex and peak during
the preovulatory period.
• Correlate with sexual desire and sexual thoughts in women.
• May restore sexual desire in ovariectomized or
postmenopausal women.
57
Hormonal Correlates of Female Sexual Behavior in
Primates: Conclusions
• Attractivity, proceptivity, and receptivity may be enhanced by
the steroid hormonal milieu occurring around the time of peak
fertility: ovulation.
– Sex steroids can increase sexual motivation and attractivity.
– Sex steroids are not necessary for sexual motivation,
attractivity, or performance.
58
End of Lecture 9
59
Lecture 10:
Female Reproductive Behavior
Part 2
Biology 178
Instructor
Melina Acosta
Outline of Today’s Lecture
1. The Estrous Cycle and Hormonal Influences on Female
Sexual Behavior in Rats
2. The Neural Basis of Lordosis in Rats
3. Social Influences on Female Reproductive Cycles
2
Learning Objectives
1. Describe the hormonal changes that occur across the rat estrous cycle and
pseudopregnancy, and explain how these changes affect attractivity,
receptivity, and proceptivity.
2. Compare and contrast primates and rodents with respect to hormonal
changes across the ovarian cycle and how these changes relate to sexual
behavior.
3. Describe the neural circuitry underlying lordosis in rats, and explain
how estrogen and progesterone act on this circuitry to activate lordosis.
4. Give some examples of how female reproductive cycles can be affected
by the social environment in rodents, humans, and cooperative
breeders.
3
Estrous Cycles in Rodents
The Rat Estrous Cycle
• 4-5 days long
• Stages:
Diestrus I (metestrus), II (& III) – Follicular phase
Proestrus – Late follicular phase (LH surge)
Estrus – Ovulation
*
* Ovulation
*
5
The Rat Estrous Cycle
• Metestrus/Diestrus:
 GnRH (1x/day) →  LH,  FSH →
Follicular development →  Estrogen (E) (over 2-3 days)
• Afternoon of proestrus:
  E →    GnRH,   LH,   FSH →   Progesterone (P)
• Early morning of
estrus:
Ovulation
Estrous behavior
→ Both are
stimulated by E+P
Miller &
Takahashi,
2014
6
The Rat Estrous Cycle
Induced Luteal Function
• If mating occurs:
Physical stimulation from mating (intromission) →
prolactin secretion from anterior pituitary for ~ 10 days →
Prolactin “rescues” corpus lutea (luteotrophic effect)
-If female conceives: pregnancy (21 days)

-If female does not conceive (but mating occurs)
Pseudopregnancy-CLs are maintained for ~10 days
• If no mating occurs:
No  in prolactin secretion →
CLs do not form fully (no spontaneous luteal phase) →
 Progesterone →
New cycle begins
7
The Rat Estrous Cycle
Induced Luteal Function:
Intromission →
 Prolactin →
Maintenance of CLs for ~10 days→
 Progesterone for ~10 days
8
Hormonal Correlates of Female Reproductive
Behavior in Rodents
• Rodents and many other species:
– Ovariectomized females will not mate.
– Intact females are attractive, proceptive, and receptive
only around the time of ovulation (estrus).
– Estrogen is necessary for attractivity, sexual motivation,
and sexual performance.
9
Hormonal Correlates of Female Reproductive
Behavior in Rodents: Progesterone
Progesterone can exert biphasic effects on sexual behavior:
• In some species
(including rats), P rises
shortly before
ovulation.
• P may be necessary for activation of sexual behavior in
these species.
• High P levels (after ovulation) can later terminate sexual
behavior (by downregulating receptors for E & P).
10
Variation in Female Reproductive Cycles
• Spontaneous vs. induced behavioral estrus
Estrus may be induced by cues from male
(e.g., courtship displays, chemosignal)
Example: prairie vole
• Spontaneous vs. induced (reflex) ovulation
Ovulation may be induced by stimuli associated
with mating
Example: cat, rabbit
• Spontaneous vs. induced pseudopregnancy
Maintenance of CL (in non-conceptive cycles) may be
induced by stimuli associated with mating
Example: rat
11
Neural and Hormonal
Mechanisms of Lordosis in Rats
Neural & Hormonal Control of Lordosis
Lordosis is…
• A stereotyped behavior (reflex) that occurs in response
to specific sensory cues and distinct hormonal
regulation.
• The first mammalian behavior with the underlying
neural circuitry and hormonal basis mapped.
13
Neural & Hormonal Control of Lordosis
Ovarian steroids (estrogen [E] and progesterone [P]) act…
1. Via socially mediated effects (attractivity)
2. On sensory system
3. On integrative systems in the brain
…to control the motor output of lordosis.
Nelson 2000
Hormone-dependent
integration in brain
Motor output to
muscles in back
Sensory input
from flanks
14
Lordosis: Sensory Input
Sensory input eliciting lordosis:
• Tactile (touch/pressure) stimulation around flanks:
Necessary to elicit lordosis.
• Visual, olfactory, etc. cues:
Unnecessary.
• Tactile input from male stimulates sensory receptors on
flanks, rump, and perineum.
• Receptors send info through the spinal cord to the medullary
reticular formation in the brainstem and to the central gray area
(=periaqueductal gray) in the midbrain.
15
Lordosis: Sensory Input
Estrogen →
•  Size of receptive fields of sensory neurons in flanks
•  Excitability of neurons in spine, medullary reticular
formation, and midbrain central gray that respond to
lordosis-triggering stimuli
Anestrous rat
Estrous rat
16
Lordosis: Motor Output
Medullary reticular formation (in brainstem):
• Output: Sends motor neurons down the spinal cord to innervate
muscles in the back.
• Input: Receives…
– Ascending sensory info directly from the spinal cord
– Descending info from higher, estrogen- (E-) sensitive brain regions
(hypothalamus, MPOA) via midbrain central gray
E-sensitive
regions in
forebrain
Sensory input: flanks →
spinal cord → brain
17
Lordosis: Hormonal Influences
Descending input from E-sensitive hypothalamic regions is
necessary for lordosis:
• Ventromedial nucleus of hypothalamus (VMN)
• Medial preoptic area (MPOA)
• Medial anterior hypothalamus (MAH)
Motor output:
brain →
spinal cord →
muscles
E-sensitive
regions in
forebrain
Sensory input: flanks →
spinal cord → brain
18
Lordosis: Hormonal Influences
Estrogenic influences on the motor output system:
• Ventromedial nucleus of hypothalamus (VMH)
– Stimulates lordosis
– Is stimulated by E
• Medial preoptic area (MPOA)
– Inhibits lordosis
– Inhibits reward pathway
– Is inhibited by E
Motor output:
brain →
spinal cord →
muscles
E-sensitive
regions in
forebrain
Sensory input: flanks →
spinal cord → brain
19
Lordosis: Hormonal Influences
Summary:
• Estrogen is necessary for the expression of lordosis in female rodents:
1. Main effect: Activates VMN to stimulate lordosis.
E → stimulates VMN → stimulates midbrain central gray →
stimulates med. reticular formation →
stimulates motor neurons in brainstem & spinal cord →
activates muscles in flanks and lower back →
lordosis!
2. Inhibits MPOA to disinhibit lordosis.
3. Increases responsiveness to tactile cues from males.
4. Increases females’ attractivity to males.
 How does E exert these effects within the
brain (especially the VMN)?
20
Lordosis: Hormonal Influences
Estrogen priming:
• E alone or E+P (more potent) facilitates lordosis in
ovariectomized rats.
• Initial E exposure must be followed ~ 24 hours later by P (or E)
treatment to induce lordosis (lordosis occurs ~4 hours after P
treatment).
• Same effect if the E and/or P is implanted in the VMN → E
priming effect depends on VMN.
• Requires both
classical (slow,
genomic) and nonclassical effects of E.
21
Lordosis: Hormonal Influences
Estrogen priming in VMN affects…
• P and E receptors
• Neurotransmitter receptors
• Dendritic spines
• Electrophysiological properties
Progesterone in VMN affects…
• Neurotransmitters
• Neurotransmitter receptors
• Later, P downregulates E & P receptors to terminate sexual behavior.
0 hrs
24 hrs
Estrogen Priming
E
treatment
28 hrs
P Effects
P
treatment
Lordosis!
22
Lordosis: Hormonal Influences
The Cascade Hypothesis:
• Initial E exposure causes a cascade of events in the central
nervous system (especially VMN), including structural,
electrophysiological, and neurochemical changes, that prime the
CNS for subsequent P exposure.
• This cascade of events occurs over a number of hours and permits
later P (or E) exposure to stimulate lordosis in response to
appropriate sensory (tactile) cues.
• P is necessary for proceptive behavior but not for lordosis.
 Two-stage hormonal effects – analogous to
organizational/activational effects, but over a much
shorter time scale!
23
Lordosis & The Reward Pathway
Interactions between the neural circuitry of lordosis and the
reward pathway:
• Engaging in copulatory behavior has long-term effects on the
reward pathway (especially the nucleus accumbens and ventral
tegmental area).
• Reward pathway influences sexual motivation (“liking” and
“wanting”sex).
• In the absence of E, the reward pathway is inhibited by the
MPOA.
• E removes this inhibition by the MPOA.
 Interactions between the lordosis circuitry and
the reward pathway can lead to effects of
experience on sexual motivation.
24
Social Influences on Female
Reproductive Cycles
Social Influences on Reproductive Cycles in
Mice
Pheromones:
• Chemical signals produced by one individual that can alter
physiology and/or behavior of another individual
• Signaling/Releaser Pheromones
Elicit an immediate behavioral response
• Primer Pheromones
Elicit a longer-term physiological
or developmental change
• Detected by VNO → AOB →
amygdala → hypothalamus
26
Social Influences on Reproductive Cycles in
Mice
1. The Lee-Boot Effect
– Group female mice ≥4 per cage (no males) →
extended estrous cycles (pseudopregnancy).
2. The Whitten Effect
– Group female mice >20 per cage (no males) →
estrous cycles cease.
– Introduce male or male odor →
synchronized ovulation after 3-4 days.
27
Social Influences on Reproductive Cycles in
Mice
3. The Bruce Effect
–
Expose pregnant mouse to unfamiliar male for >48 hours →
female aborts or resorbs fetuses.
–
Female mates with new male
later.
–
Is thought to have evolved in
infanticide by unfamiliar males.
3-6 days
response to
Pregnancy
Pregnancy block
(Bruce Effect)
28
Social Influences on Reproductive Cycles in
Mice
3. The Bruce Effect
Pheromone from unfamiliar male → → →
↓Prolactin →
CLs regress →
↓Progesterone →
Pregnancy ends
29
Social Influences on Reproductive Cycles in
Mice
4. The Vandenbergh Effect
– Adult males accelerate puberty in young females
– Adult females delay puberty in young females
Uterus
Saline
Flanagan et al. 2011
Male
Urine
Body
Mass
Saline
Uterine
Mass
Male
Urine
Saline Male
Urine
30
Social Influences on Reproductive Cycles in
Mice
Male Accelerating Pheromone
• Androgen-dependent; in males’ urine
• Stimulates GnRH, LH and estrogen secretion in recipient:
– Young females: accelerates puberty
– Suppressed females: initiates cycles
– Pregnant females: ends pregnancy, stimulates ovulation
31
Asaba et al. 2014
Social Influences on Reproductive Cycles in
Mice
Female Inhibitory Pheromone
• In females’ urine?
• Inhibits GnRH, LH and estrogen secretion in recipient
– Young females: delays puberty
– Cycling females: inhibits cycling and ovulation
32
Social
Influences
onReproductive
Reproductive Cycles
Social
Influences
on
Cycles
in
in Women
Women
Do humans have pheromones?
• Evidence that some pheromones are produced in the
axillary region (armpit).
• Human VNO is vestigial and probably non-functional.
• Pheromones might be detected by nasal epithelium.
➔ What do they do?
33
Social Influences on Reproductive Cycles in
Women
1. Menstrual synchrony
• Has been reported among roommates, close friends, related women
living together.
• Demonstrated scientifically by McClintock in 1971.
• Not found in most subsequent studies.
34
Social Influences on Reproductive Cycles in
Women
2. Normalization of cycles by males
Male axillary secretions →
•  LH pulse frequency
• Normalize cycle
length in women
with irregular cycles
Latency to Next LH Pulse
Control
Male
secretions
Preti et al., 2003
35
Social Suppression of Ovulation in Cooperative
Breeders
• Cooperative breeders, individuals routinely provide care for other
animals’ offspring.
• Frequently, only the dominant female breeds.
• Ovulation may be inhibited in subordinate females.
36
Social Suppression of Ovulation in Cooperative
Breeders- Marmoset Monkeys
37
Social Suppression of Ovulation in Cooperative
Breeders- Marmoset Monkeys
38
Social Suppression of Ovulation in Cooperative
Breeders- Marmoset Monkeys
39
Environmental Influences on Reproduction
• Seasonality
Proximate cues:
– Photoperiod (daylength)
– Food
– Plant comp…
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