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Female Reproductive Behavior
Part 1
Biology 178
Instructor
Melina Acosta
Outline of Todays 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
Females stimulus value (attractiveness) for a particular
male (how hot is she?)
Measured by males 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
Females 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
Females 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 recd.
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.
ONeill 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.
ONeill 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 Todays 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
Lo
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