Neuroscience and Biobehavioral Reviews, Vol. 16, pp.

131-144, 1992
Printed in the USA. All rights reserved.

0149-7634/92 $5.00 + .00

Copyright .t~ 1992 Pergamon Press Ltd.

Oxytocin and Sexual Behavior

C. S U E C A R T E R

Department of Zoology, University of Mao'land, College Park, MD 20742

R e c e i v e d 27 D e c e m b e r 1990
C A R T E R , C. S. Oxytocin and sexual behavior. N E U R O S C I B I O B E H A V REV 16(2) 131-144, 1 9 9 2 . - - T h e n e u r o h y p o p h y s e a l

hormone oxytocin has been implicated in many aspects of reproduction including sexual behavior. This review considers the hypotheses that oxytocin and/or the neural events surrounding the release of oxytocin may have behavioral effects during sexual
arousal, orgasm, sexual satiety and other aspects of sociosexual interactions.
Oxytocin

Sexual behavior

Arousal

Orgasm

Satiety

IN humans and other primates all components of sexual behavior can be expressed in gonadally inactive individuals with very
low levels of steroid hormones (8, 85, 90, 177). However, little
is known regarding the neurobiological substrate of the human
sexual experience. In the last decade there has been an explosion of new knowledge in the neurosciences. This research has
implicated a variety of endogenous chemicals, including hormones and neurotransmitters, in the control of sexual behavior
in animals.
The present review will describe selected components of the
animal and human literature to examine the possibility that neural events surrounding the central release of oxytocin could play
a role in sexual behavior. The phenomenology of human sexual
behavior and contemporary theories regarding the hormonal control of sexual behavior will be summarized. Direct experimental
evidence is not available regarding the role of oxytocin in human behavior. In the absence of such evidence the present review will summarize animal research relevant to the mechanisms
responsible for the release of oxytocin and the behavioral effects
of oxytocin. The release and actions of oxytocin may be regulated by steroid hormones and a variety of other neurochemicals
that also have been implicated in sexual behavior; this research
also will be summarized. These observations will be used to
generate specific, and admittedly speculative, hypotheses regarding possible roles for oxytocin in the phenomenology of sexual
excitement, orgasm, sexual satiety and other aspects of sociosexual behavior.

Human

Species comparisons

ical release from sexually stimulated vasocongestion or myotonia, accompanied by a "subjective perception of a peak of
physical reaction to sexual stimuli." The resolution phase was
defined as a reverse reaction in which individuals returned
through plateau and excitement levels to the unstimulated state.
In males and, less predictably, in females the resolution phase
also was characterized as a refractory period when sexual stimuli were ineffective in reinitiating the response cycle. Uterine
contractions or ejaculatory contractions typically are observed
within a few seconds following the onset of the subjective component of orgasm.
The subjective experience of orgasm does not lend itself
readily to scientific study. For the purpose of this review, however, it is useful to note that the phenomenology of orgasm is
described in similar terms by men and women (174). Kinsey and
associates noted that "'orgasm in the female matches the orgasm
of the male in every physiologic detail except for the fact that it
occurs without ejaculation" (85).

Neural Correlates of the Sexual Response

A "coital reflex," which is triggered by mechanical stimulation of the urethra, has been identified in rats (33). This reflex
was seen following spinal transection in anesthetized and gonadectomized males or females. The reflexive responses recorded
were similar in both sexes and resembled those seen during
ejaculation but were not elicited in either sex prior to transection
of the spinal tract.
Although the existence of spinal, sexual reflexes is well documented, little is known regarding the central, neural events responsible for the experiences described during human orgasm.
EEG recorded during orgasm shows a "'slowing of the electrical
activity with increase in voltage, until there are paroxysmal three
per second waves which are mixed with rhythmic alternating
muscular discharges" (115). More recently, EEG hemispheric
asymmetry has been described during both masturbation (38) and
nocturnal penile tumescence (138). Central neural activity could
reflect feedback from peripheral reflexes. There are reports,
however, that orgasmic experiences are possible in individuals
with complete spinal cord lesions (41, 84, 85).
Central neural events (normally, but not always, occurring in
the context of genital stimulation) presumably are essential for

HUMAN SEXUAL BEHAVIOR

Phenomenology of Human Sexual Behavior and Orgasm

Kinsey and associates (85) described human sexual behavior
as a pattern of increased muscular tdnsion which may culminate
in muscular spasms and concurrent alterations in consciousness;
these physical and psychological events were identified as orgasm or the "after-effects" of orgasm. Masters and Johnson
(98) partitioned the human sexual response into four phases: excitement, plateau, orgasm and resolution. Excitement was described as an increase in sexual tension. The plateau phase was
characterized by an enhancement of sexual tension, including
vasocongestion and myotonia. Orgasm was described as a phys-

131

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CARTER

the experience of orgasm. Damage to the central nervous system, including epilepsy, can interfere with normal sexual functions (17, 51, 72, 87, 144).
Most theories regarding the physiology of orgasm have emphasized peripheral autonomic and neuromuscular events (55,
80, 84, 85, 98, 154). Davidson (41) proposed that two systems
were responsible for orgasm. One system, which affects genitopelvic tissues, would participate in seminal emissions or uterine
contractions. The second, which acts upon the nervous system,
including the cerebral cortex, would account for loss of arousal,
altered states of consciousness and other cognitive components
of orgasm. In 1980, Davidson hypothesized that a mediating
substrate, which he termed "the organ of orgasm," would normally coordinate these systems (41).

Hormones and Sexual Behavior

Sex steroids of gonadal origin are not essential for human
sexual behavior (8, 43, 84, 85, 90). However, social interactions (177) and specific components of sexual experience may
be modulated by gonadal steroid. In general, in most mammals,
including nonhuman primates and humans, it appears that estrogens (130,177) and/or androgens (8, 41--44, 128, 139, 141, 155,
156) facilitate sexual behavior, while chronic exposure to progesterone (9, 15, 16, 128) inhibits sexual activity. The effects
of various steroid hormones on the capacity to experience orgasm have not been adequately studied.
Based primarily on animal research and limited clinical and
anecdotal findings in humans (148), it is likely that a variety of
nonsteroidal hormones and neurotransmitters influence sexual
behavior. The present review will focus on a possible role for
one polypeptide, oxytocin.
OXYTOCIN

General Features of Oxytocin

Oxytocin is a nonapeptide characterized by a six amino acid
ring structure with a three amino acid tail (65). Oxytocin is produced primarily in the supraoptic (SON) and paraventricular
(PVN) nuclei of the hypothalamus (143, 159, 164). Pulses of
oxytocin are released into the systemic circulation at the posterior pituitary (neurohypophysis). Arginine vasopressin, which
differs from oxytocin by two amino acids, is also produced in
the SON and PVN, and is released by the posterior pituitary.
Oxytocin and vasopressin are secreted into the circulation in
conjunction with their carder proteins (neurophysins) (65). The
half-life of peripheral or centrally injected oxytocin is species
specific and the half-time for clearance in CSF is approximately
19 minutes in rats (103). Both oxytocin and vasopressin also are
released into the central nervous system where they presumably
affect neuronal activity (164,176). Oxytocin does not pass easily
through the blood-brain barrier, but there is evidence of bidirectional transport of small amounts of oxytocin between the general circulation and cerebrospinal fluid (103). Whether this transport
is of biological significance remains uncertain (52,92). The ability of systemically administered oxytocin to reach the central
nervous system may help to explain reports (described below) of
behavioral changes following peripheral injections of oxytocin.
Genes for oxytocin and vasopressin have been isolated and
sequenced, and it has been shown that the genes responsible for
oxytocin and vasopressin share extensive homologies (65). Pharmacological evidence suggests some overlap of functions between oxytocin and vasopressin. Under physiological conditions
the release of oxytocin and vasopressin are often coordinated,

although these hormones can have opposing functions (65).

Localization of Oxytocin
Most of the centrally located oxytocin is found in large magnocellular neurons located in the PVN and SON; these cells
project to the posterior pituitary gland where oxytocin is stored
and secreted into the systemic circulation (10). Smaller, parvocellular cell bodies containing oxytocin also have been identified
in the PVN. Oxytocinergic fibers originating in the parvocellular neurons extend into other parts of the nervous system including the caudal brain stem and spinal cord (19, 111, 143, 159,

160, 164).
Oxytocin receptors have been identified in a variety of neural
tissues, including the ventromedial hypothalamus (VMH), bed
nucleus of the stria terminalis (BNST), central amygdala, anterior olfactory nucleus, lateral septum, ventral subiculum, and
dorsal motor nucleus of the vagus (60, 65, 164, 171). Patterns
of oxytocin receptors and relative concentrations of these receptors are species specific [reviewed (76)]. The functions of these
receptors remain to be described (2), but correlational evidence
links species differences to patterns of social organization and
reproduction (76, 88, 186).
Several aspects of oxytocin's action appear to be influenced
by steroid hormones, including estrogen, progesterone, and the
androgens. Both the gene for oxytocin and oxytocin receptor induction may be regulated by steroid hormones (65). In rats, steroid receptors show a pattern of neuroanatomical distribution that
coincides with that of oxytocin in the bed nucleus of the stria
terminalis and ventromedial hypothalamus (VMH) (76, 135137). The concentrations of some, but not all, oxytocin receptors are steroid hormone-dependent. A number of studies in rats
have documented the steroid dependence of oxytocin receptors
within the VMH (75-79, 145, 146, 160, 164). The response of
oxytocin receptors to steroid hormones, however, can differ across species. For example, in prairie voles, in which reproduction is highly dependent on chemical communication,
oxytocin receptors within the anterior olfactory nucleus are regulated by estrogen in a pattern that correlates with female sexual receptivity. In contrast, in prairie voles manipulations of endogenous or exogenous estrogens did not alter the concentrations
of oxytocin receptors within other brain areas including the
VMH (186).
Oxytocin, the gene for oxytocin expression, and oxytocin receptors also have been found in nonneural tissues (96) including
the corpus lutea (71,179) and testis (120). It has been suggested
that oxytocin is involved in steroidogenesis (120) and corpus luteum regression (71). Thus, it appears that oxytocin may have
regulatory functions at many levels within the hypothalamic-hypophyseal-gonadal axis.

Factors Regulating the Release of Oxytocin

Using the rat as a model, factors responsible for the release
of oxytocin have been studied extensively in the analysis of
mechanisms underlying lactation (175) and parturition (32, 61,
64). In these contexts, breast and genital stimulation are potent
releasers of oxytocin and/or the milk ejection reflex. In addition,
the release of oxytocin can be induced, even in anesthetized
male rats, by light touch, pinch or electrical stimulation of the
vagus nerve (161). Olfactory tract stimulation and olfactory
stimuli can release oxytocin in some species (77-79). Oxytocin
release also can become conditioned, permitting release by cognitive stimuli, at least during lactation (93). In rats, olfactory
input also has been implicated in anatomical changes within the

OXYTOCIN AND SEXUAL BEHAVIOR

133

TABLE 1
OXYTOCINLEVELSDURINGMALESEXUALACTIVITY(MEAN + S.E.M, fmol/ml)
Sampling Condition

Species

Baseline

Rat
Rabbit

9.1 __. 0.8

13.0 - 3.0*
8.6 +--2.1

Human

1.4 --- 0.3

Postejaculation (rain)

Mount and
Thrust

19.5 --- 4.0*

(Arousal)
2 --- 0.4*

0-5

20

18.3 --- 3.3

45.5 --- 13.0"
46.9 --. 8.5

27.4 +- 4.2

7.3 -- 2.6

30

Ref

14.5 2.0*

(73)
(162)
(17o)
(117)

*Extrapolated from graphed data.

SON that accompany lactation (104, 157, 190).

Oxytocin can stimulate its own release in rats (54, 59, 60,
110, 113, 165). Positive feedback of oxytocin may contribute to
the pulsatile release which is characteristic of this hormone. Activity in oxytocinergic neurons and the release of oxytocin depends upon the interaction of a variety of other hormones and
neurochemicals (175). Steroid hormones, and in particular estrogen and testosterone, may facilitate the activity of the oxytocinergic neurons at many levels, including the induction of oxytocin
receptors (77-79, 145, 146); progesterone, in contrast, appears
to be inhibitory (129). The opiates, serotonin and gamma aminobutyric acid (GABA), may inhibit the release of oxytocin (13,
14, 160). The catecholamines and acetylcholine are more likely
to induce activation in the oxytocinergic system, although this
effect may be receptor specific (40,83).

trical activity recorded from cells was synchronized with the

spontaneous activity of adjacent neurons, and dye coupling among
cells was observed (69, 189-191). Even in virgin female rats,
exposure to pups is capable of inducing neuroanatomical changes.
Virgin females that cohabitated with pups for several days began to show maternal behavior and exhibited significant increases in several parameters of dendritic morphology within the
SON (140). Yang and Hatton (190) also observed in lactating
females that electrical coupling in brain slices increased within
10 minutes when electrical stimulation was provided via the lateral olfactory tract. Thus, the potential exists for rapid functional
changes within this system following sensory stimulation. This
neuronal plasticity, in turn, presumably provides a mechanism
for the physiological and environmental regulation of the pulsatile release of oxytocin (11, 95, 175).

Unique Properties of Oxytocinergic Cells

Oxytocin amt Behavior

Oxytocin is released in pulses during labor (61) and before

each milk ejection reflex in female rats (175). Both the release
of oxytocin and the electrical activity of oxytocinergic cells are
pulsatile (95,175). Oxytocinergic neurons display explosive firing patterns 9 to 12 seconds before each milk ejection, and each
burst apparently represents the synchronous firing of many neurons. It is assumed that the 9- to 12-second latency represents
the time that it takes for oxytocin to be released, carded systemically to the mammary gland and to act on myoepithelial cells
of the breast to produce milk ejection. Vasopressin cells within
the same nuclei show a phasic, rather than explosive, pattern of
electrical activity (95, 132, 163).
The morphology of the SON and PVN provides a substrate
for the pulsatile release of oxytocin in rats. Ultrastructural analyses of magnocelhilar neurons in the PVN and SON (69, 70,
104, 112-114, 165-169, 172, 173, 189-191)indicate that oxytocin-containing cells occur in clusters, and that these cells are
capable of direct neuronal contacts (gap junctions) which could
permit synchronous electrical discharges. Astroglial processes
normally isolate these cells from eaoh other. Prior to parturition
and during lactation, the glial processes are retracted between
oxytocinergic cells. Glial withdrawal has not been reported between vasopressinergic cells (69,166). These unisolated, oxytocin-containing cells in lactating or hormone-treated animals show
increased cell-cell contact, a large number of double or multiple
synapses, and the formation of dendritic bundles.
Electrophysiological analyses in rats, including data from
brain slices, have provided further evidence for direct contact
and synchronous firing among SON cells (68, 163, 191); elec-

Oxytocin, secreted by the posterior pituitary, has powerful

contractile effects on smooth muscle such as that found in the
uterus and breast. Oxytocin was described first as a "female"
reproductive hormone with critical actions in parturition and lactation (153,175). As recently as 1987, Murphy and associates
( l l 7 ) stated that "although men and women have similar concentrations of immunoreactive and bioactive oxytocin in the circulation, cerebrospinal fluid and hypothalamus, oxytocin has no
known function in men."
A broader role for oxytocin in "interpersonal reproductive
acts" including behavior was suggested originally by Newton
(118,119), but it is only recently that oxytocin has been implicated directly in behavior [reviewed (2)]. For example, oxytocin
may regulate maternal behavior in rats (75, 82, 125-127) and
mother-infant bonding in sheep (81-83), adult social bond formation in prairie voles (27, 28, 182), female sexual behavior in
rats (5, 21, 66), and male sexual behavior in rats (3, 4, 7, 73,
100, 101, 162).
Early reports that milk ejection (or oxytocin release) in women
could be induced during orgasm (23) were confirmed using radioimmunoassay (24,58). Recent studies (Table 1) indicate that
oxytocin increases slightly during sexual arousal in humans
(24,117) and shows a marked increase during the orgasmic (or
ejaculatory) phase of sexual behavior in humans, bulls, rams and
rabbits (24, 63, 116, 117, 123, 150-152, 170). It has been suggested for several species that contractions in the reproductive
tract, caused by peripherally released oxytocin, may facilitate
sperm transport (56, 57, 121) and could play a role in sexual
satiety in both sexes (24, 41, 73, 97, 162, 187).

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TABLE 2
EFFECTSOF OXYTOCIN(OT) OR OXYTOCINANTAGONIST(OTA) ON MALESEXUALBEHAVIORIN RATS

Drug

Dosage

Site of
Administration

Effect on
Sexual Behavior

OT
OT
OT
OT
OT
OTA

1.6-2.5 p,g
200 ng
I ng
30 ng
3-9 ng
2.5-50 ng

IV
IP
ICV
ICV
PVN
ICV

'~
T
I"
~"
'['
,~

OTA

10-100 ng

ICV

250-500 ng

ICV

OT

~,

Comments
Fewer intromissions to ejaculation
Shorter lat. to first
ejaculation ~ PEI
Penile erection frequency
Penile erection frequency
Decreased mounts; eliminated most
ejaculations
Dose-dependent decrease in OT or
apomorphine-increased penile erections
Increased latency to first mount and
intromission and length of PEI

Ref
162
7
3
101
4
3
162

IV = Intravenous; IP = intraperitoneal; ICV = intracerebroventricular; PVN = paraventricular nucleus: PEI = postejaculatory

interval prior to resumption of mounting.

OXYTOCINAND SEXUALBEHAVIOR

Sexual Stimulation
Sexual arousal and subsequent copulatory behavior can be
elicited by a variety of sensory stimuli. For example, somatosensory stimuli play a major role in sexual activity (84, 85, 98).
Genital and breast stimulation is particularly powerful in inducing the release of oxytocin (175). In rats, oxytocin also is released by touch (161). Oxytocin release can be regulated by
cognitive stimuli and can be conditioned to occur in the absence
of direct physical stimulation (62,99). The morphology of cells
releasing oxytocin, the release of oxytocin and oxytocin receptors may be affected by steroid hormones (77-79, 145, 146). In
addition, tactile sensitivity, including genital sensitivity, may be
influenced by hormones (20,89). As described above, steroid
hormones influence virtually all aspects of sexual behavior and
reproductive function. In addition, various neurotransmitters,
neuromodulators and anatomical sites that have been implicated
in sexual behavior, also may influence the release or actions of
oxytocin [reviewed (65. 67, 82, 83, 175)].

Facilitation of Male Sexual Behavior

Several experiments have indicated that oxytocin can enhance
male sexual behavior (Table 2). In 1955, Wilhelmi and associates (181) reported that oxytocin treatment facilitated the spawning reflex in the Killifish (Fundulus heteroclitus). More recent
studies have shown evidence of roles for related neurohypophyseal hormones in several nonmammalian species (108). In 1963,
Melin and Kihlstr6m (100) observed in rabbits that intravenous
administration of oxytocin hastened the onset of an initial ejaculation and increased the number of ejaculations within a fixed
(30 minute) test period. Arletti and associates (7) found in rats
that both central (intracerebroventricular, ICV, 1 ng) and peripheral (intraperitoneal, IP, 200 ng) injections of oxytocin shortened
the latency from first intromission to first ejaculation and the
postejaculatory interval leading to the resumption of intromission. [Attempts to elicit sexual behavior in previously nonresponsive male rats were not successful (7)]. Stoneham and
associates (162) also found that relatively large intravenous
(1.6-12.5 I.tg, IV) injections reduced the number of intromissions preceding ejaculation in male rats.
The pharmacology of penile erections in singly-caged rats has

been studied in detail by Argiolas, Gessa and their associates

[reviewed (2)]. Although a number of substances can influence
penile erections, oxytocin apparently plays a central role in the
regulation of these responses. The dose response curve for ICV
oxytocin's effects on penile erections is "bell-shaped." Argiolas
and Gessa (2) have reported that 5 ng of oxytocin (ICVI is the
minimal effective dose, with maximal facilitation of penile erections observed between 10 and 60 rig. Penile erections are most
readily induced in males that are primed with either endogenous
or exogenous testosterone. Hypophysectomy reduced the behavioral effects of oxytocin in this model, and testosterone replacement partially restored the ability of exogenous oxytocin to
facilitate erections. Although secretions from the pituitary-gonadal axis may be permissive in penile erections, these results
indicate that hypophyseal oxytocin is not essential. Oxytocin injections directly into the paraventricular nucleus, and to a lesser
extent in the hippocampal CA1 field, also produced a dosedependent (3 to 9 ng) increase in penile erections; injections
in a variety of other brain regions, including the supraoptic area,
lateral septum, preoptic area and ventromedial hypothalamus
did not affect penile erections (101). Argiolas and Gessa (2)
suggest that low doses of oxytocin may act within the paraventricular nucleus to activate the subsequent release of endogenous
oxytocin.
Apomorphine and other dopaminergic agonists also can stimulate erections, and Argiolas and Gessa (2) suggest that these
behavioral effects are due indirectly to the capacity of dopamine
to release oxytocin. Penile erections induced by ICV oxytocin
(30 rig), as well as erections induced by apomorphine, were
blocked by ICV injections of a potent oxytocin antagonist
d(CHz)sTry(Me)-OrnS-vasotocin (OTA) (2,3). The ability of apomorphine to induced erections was blocked by dopaminergic antagonists, although these agents did not interfere with the capacity
of oxytocin to induce penile erections. In rats, OTA markedly
increased intromission latencies and eliminated ejaculatory behaviors when given at high dosages (25 or 50 ng); a lower dosage of OTA (2.5 ng) eliminated ejaculations in 60 percent of
the rats and increased intromission latency in those animals that
did eventually ejaculate (41.

hlhibition of Male Sexual Behavior

There also is evidence that oxytocin may inhibit male sexual

OXYTOCIN AND SEXUAL BEHAVIOR

behavior [(2), Table 2]. Argiolas and Gessa (2) report that high
doses of oxytocin inhibit penile erections. In male rats, Stoneham and associates (162) observed a dose-dependent inhibition
of mount and intromission latencies following ICV infusions of
oxytocin (250 ng or greater); in this study males that stopped
mating emitted ultrasonic vocalizations like those characteristic
of the postejaculatory refractory period. The latter study was interpreted as evidence for a possible role for oxytocin in male
sexual satiety. We also have observed that oxytocin (300 ng,
ICV and 500 ng, IP) can inhibit male sexual behavior in prairie
voles (97). Data on a broader range of oxytocin dosages are not
available for species other than rats.
Hughes and associates (73) produced selective lesions in the
lateral and posterior parvocellular PVN, thus eliminating cell
bodies which contribute to centrally released oxytocin. These lesions spared the magnocellular regions responsible for the secretion of peripheral oxytocin. Behavioral studies of these animals
indicated that lesions in the parvocellular PVN were followed
by a more rapid return to sexual activity following ejaculation.
These results again are consistent with the hypothesis that oxytocin, and specifically, centrally acting oxytocin, might be part
of a neural system responsible for postcopulatory sexual satiety.
Oxytocin does not cross the blood-brain barrier (BBB) with
ease. Oxytocin does penetrate BBB-free regions of the nervous
system, and Ermisch and associates (52) conclude that physiologically effective amounts might reach the nervous system " i f
high pharmacological amounts of peptides are injected peripherally." The reported capacity of peripherally administered oxytocin to influence sexual behavior may indicate that some of the
behavioral effects of oxytocin are due to direct or indirect actions outside of the BBB. Alternatively, exogenous oxytocin
may cross the BBB. Even small amounts of exogenous oxytocin
might in turn trigger the release of endogenous peptide (54,110),
In summary, the results of several studies in rats suggest the
hypothesis that small amounts of centrally administered oxytocin, or somewhat larger dosages of peripherally administered
oxytocin, may facilitate the onset or pacing of male sexual behavior. In contrast, centrally administered, larger dosages apparently are more likely to inhibit penile erections and male sexual
behavior, possibly creating a physiological state analogous to
sexual satiety. The behavioral effects of a broad dose range of
oxytocin are available only for penile erections (2). Studies of
other components of male sexual behavior, within a consistent
paradigm, and using a broader range of dosages, are necessary
to examine the above hypotheses. In addition, systematic comparisons are needed of the effects of oxytocin on motivational
versus copulatory or reflexive components of behavior. Even
less is known regarding the behavioral effects of oxytocin in
species other than domestic rats. Data from prairie voles indicate that exogenous oxytocin at relatively high dosages can inhibit male sexual behavior in that species (97), although in voles
studies of the behavioral effects of low doses of oxytocin are
not yet available.
Female Sexual Behavior
One of the earliest reports of a behavioral effect for the posterior pituitary hormones in females comes from research showing that vasotocin enhanced the willingness of female frogs to
accept male clasping (48). Recent research examining the behavioral effects of oxytocin in females has focused on the capacity
of oxytocin to facilitate lordosis in female rats (5, 21, 66, 145,
146). In female rats, the effects of oxytocin are most readily observed following either a sequential treatment with estradiol plus
progesterone or in females primed with relatively large amounts

135

of estradiol alone. Oxytocin is further implicated in lordosis by

the recent finding that treatment with an oxytocin antagonist
(OTA, given concurrently with progesterone) reduced lordosis
behavior in estradiol-treated female rats (185).
Oxytocin injections can facilitate lordosis in female rats, and
it is generally assumed that this is due to actions of oxytocin
within the nervous system. A recent study, however, has reported that facilitative effects of oxytocin were no longer measured after removal of the uterus, leaving open the suggestion
that at least some of the effects of oxytocin in female rats are
due to feedback from its peripheral actions (107).
Oxytocin injections localized to the ventromedial hypothalamus (VMH) did not facilitate lordosis in female rats receiving
threshold treatments with estradiol and progesterone. However,
in female rats, oxytocin treatments injected into the VMH or
ICV were followed by reduced rejection of male advances and
increased physical contact with male partners. These results suggest that oxytocin may increase the tolerance of the female rat
for tactile stimulation (184,185).
In another rodent, the prairie vole, attempts to demonstrate a
facilitatory role for oxytocin (ICV or IP) in female sexual behavior have been unsuccessful (187). ICV treatment with 1 to
1000 ng of oxytocin did facilitate contact behaviors and reduce
male-directed aggression in estradiol-primed female prairie voles.
More recently, Williams and associates (27,182) have demonstrated that the formation of heterosexual social preferences in
ovariectomized female prairie voles can be hastened by oxytocin
infusion (ICV). These data suggest the possibility that oxytocin
could influence sexual behavior indirectly, through actions on
afflliative behaviors leading to, or associated with, sexual behavior.
In estrous prairie voles, ICV oxytocin at dosages of 300 ng
and above produced an immediate and long-lasting inhibition of
female sexual behavior. In contrast, peripherally administered
high dosages (1 to 10 I.tg) of oxytocin were without behavioral
effects in this species (187). Studies of the long-term effects of
oxytocin on female sexual behavior in rats have not been reported. The results from studies of the prairie vole indicate that
oxytocin can produce inhibitions of female sexual behavior that
last well beyond the half-life of the chemical, and suggest the
possibility that relatively large pulses of oxytocin, or a refractory state induced by exposure to such pulses, might mediate or
signal sexual satiety (187). Davidson (41) also speculated that
coitally induced release of oxytocin (24) acting to induce uterine
contractions could contribute to sexual satiation in human
females.
Ventromedial Hypothalamus
Recent studies of the central effects of oxytocin and the sex
steroids have focused on the VMH. The facilitatory effects of
oxytocin on female sexual behavior in rats are usually steroidhormone dependent (21,66). The VMH contains high levels of
oxytocin receptors. In both male and female rats, VMH oxytocin receptor levels are steroid-dependent (77-79, 145, 146). In
contrast, in prairie voles, at least in females, oxytocin receptors
are concentrated in the VMH, but the levels of VMH-oxytocin
receptors are not estrogen-dependent (186). There also is no evidence in prairie voles that oxytocin is capable of facilitating or
enhancing sexual behavior (187). In both male (97) and female
(187) prairie voles, ICV oxytocin injections produce immediate
inhibitions in sexual activity. Exposure to large pulses of oxytocin may inhibit sexual behavior, and the inhibitory effects of
oxytocin might be either steroid-independent or due to interactions with the inhibitory effects of progesterone. The inhibitory
effects of oxytocin might involve receptors in the VMH. How-

136

CARTER

ever, we are not aware of any direct examinations of the role of

the VMH or oxytocin in sexual satiety in rats.
The VMH has been implicated in a variety of behavioral
functions including "motivation" (105,129). ICV oxytocin treatments also inhibit food consumption in rats (6). Destruction to
the VMH results in hyperphagia, which has classically been described as a failure of a satiety mechanism. The possibility that
the VMH and oxytocin may have a broad role in "motivational" processes, including the reduction of "drives" (105) or integrative or sensory processes regulating behavior deserves further
consideration.
SPECIES DIFFERENCES

There are several indications of species differences in the

neural and behavioral effects of oxytocin. As described above,
the relative steroid dependence of VMH oxytocin receptors is
species specific (76, 77, 79, 186). Species differences also have
been reported in the behavioral effects of steroid hormones. Although estrogen facilitates sexual behavior in both rats and
voles, the behavioral effects of progesterone are species specific
(25,26). Female rats (15,16) and hamsters (25), but not voles
(26), exhibit a biphasic (facilitation followed by inhibition) response to progesterone.
Attempts to examine species differences in the behavioral effects of oxytocin also should attend to species differences in behavioral patterns that may correlate with oxytocin release. Data
suitable for making quantitative comparisons are not available.
There is, however, interspecific variability in mammalian lactational patterns, which may, in turn, correlate with patterns of
oxytocin release. As an example of the extreme variations that
may occur, prairie vole pups attach almost continually to the
maternal nipple, receive extensive maternal care, and presumably receive rather continuous nutrition while the female is in
the nest (149). Female rats nurse in discrete bouts throughout
the day, while rabbits may enter the nest and deliver milk only
once a day (175). Patterns of sexual behavior also show crossspecies variation (46,47). If there are shared neural factors responsible for lactation and sexual behavior, it is possible that
these will manifest in correlations among mating patterns and
nursing patterns. Male prairie voles may continue to show intermittent sexual behavior over a day or longer (188). Mating in
rats typically lasts a few hours (46), while mating in rabbits may
be terminated after a single ejaculation (39).
Mating systems or social organization also may correlate with
the behavioral effects of oxytocin or its pattern of release. Concentrations of oxytocin receptors apparently correlate with monogamy or polygyny in voles and deer mice (76,186). As
described above, oxytocin has been implicated in a variety of
species-specific behavioral patterns, including pair-bond formation (27, 28, 182), which may contribute to the expression of
social systems. These observations suggest the testable hypothesis that interspecific differences in patterns of oxytocin release
and action may be reflected in, or perhaps even cause, species
differences in patterns of reproductive behavior.
SUMMARY

Oxytocin is released following tactile stimulation in rats, and

slight elevations have been measured following preejaculatory
behaviors including mounting in male rabbits (162) and during
sexual arousal in humans (24). Oxytocin is released during ejaculation in several species (Table 1). The results of the studies
described here suggest that treatment with relatively low levels
of exogenous oxytocin can facilitate or accelerate the onset of

ejaculatory behavior in sexually-active male rats and rabbits. In

contrast, large amounts of oxytocin may inhibit sexual behavior.
The behavioral actions of oxytocin may be dosage- and/or timedependent. High levels of, or chronic exposure to, oxytocin
could have inhibitory effects on sexual behavior, while lower
levels or acute treatment may facilitate sexual activity. It has
been reported that lesions of the lateral parvocellular PVN reduce the postejaculatory refractory period (73). Since parvocellular neurons project intracerebrally rather than to the
neurohypophysis, this finding offers support for the possibility
that endogenously released oxytocin also participates in male
postcopulatory sexual satiety. Thus, it is possible that endogenously released oxytocin might function to both enhance male
sexual arousal or other preejaculatory components of sexual behavior and to later inhibit sexual behavior.
The presence of an ejaculatory event permits analogies between sexual activity in human males and other vertebrate species. It is more difficult to draw parallels from studies of female
sexual behavior in rodents to the sexual response in human females. Preliminary findings in both voles and rats suggest the
possibility that oxytocin might enhance social contact. In addition, the neural actions and behavioral effects of oxytocin may
be species specific (76). Experiments examining the effects of
oxytocin on motivational, autonomic and/or sensory processes,
within a cross-species context, will help to clarify these issues.
Additional understanding of potential interactions among steroid
hormones and oxytocin is needed, although it is possible that at
least some of the behavioral effects of oxytocin are steroid-hormone independent. Research in rats has suggested the VMH as
a possible site for behavioral effects of oxytocin (145, 146, 184);
however, the behavioral role of VMH oxytocinergic receptors
remains to be specified.
AUTONOMIC PATHWAYS, SEXUAL BEHAVIOR
AND OXYTOCIN RELEASE

The autonomic nervous system plays a role in milk ejection

[reviewed (102, 143, 164)]. It has been known for many years
that stress could inhibit milk let down (118), and most of the
studies dealing with functional interactions among oxytocin, autonomic processes and milk ejection have focused on the sympathetic nervous system and adrenal. However, oxytocin also
influences parasympathetic activity, probably through effects on
the central nervous system (143,164). Oxytocin receptors are
concentrated in areas that have been implicated in parasympathetic function, such as the dorsal motor nucleus of the vagus
and nucleus of the solitary tract (171).
The autonomic nervous system regulates genital functions,
including vasocongestion in both sexes and, in males, seminal
emission and ejaculation. This regulation involves complex interactions between the sympathetic and parasympathetic nervous
systems and may involve various neurotransmitters including vasoactive intestinal polypeptide (VIP). Erection and seminal emission require an intact parasympathetic nervous system. Sympathetic
innervation of the penis is not essential for the development of
erections; however, the sympathetic nervous system apparently
influences penile detumescence [reviewed (12)]. Oxytocin also
has been implicated in increased seminal emission (56,57), and
receptors for oxytocin are found throughout the male reproductive system in rats (96).
The peripheral physiology of female sexual responses is not
well described. Myoepithelial tissue also is found in the clitoris
(22). Genital myoepithelial tissue might share response characteristics with mammary tissue, including responses to oxytocin
and the autonomic nervous system.

OXYTOCIN AND SEXUAL BEHAVIOR

Both the psychological and physiological phenomena associated with human sexuality have autonomic components, including not only genital events, but dramatic changes in cardiovascular
and respiratory function. Heart rate in humans usually increases
during sexual arousal, becomes maximal at orgasm, reaching in
some cases rates of 120 to 180 beats per minute, and then drops
rapidly during resolution (18, 93, 98). In women, changes in
heart rate have been related to the subjective intensity of
orgasm (93).
As mentioned above, extrahypothalamic oxytocinergic and
vasopressinergic fibers project to neural areas associated with
autonomic functions (143). Infusions of oxytocin have complex
effects on heart rate, suggesting a role for oxytocin in both sympathetic (192) and parasympathetic (133) control of cardiovascular functions. For example, in rats, intrathecal oxytocin produced
a gradual increase in heart rate, while peripheral (IV) injection
of oxytocin produced an immediate decrease in heart rate and an
increase in blood pressure which lasted 5 to 10 minutes (192).
Centrally active oxytocin, reaching the level of the spinal cord,
might participate in the gradual increase in heart rate that accompanies sexual arousal, while systemically released oxytocin
from the posterior pituitary (present following orgasm) might
play a role in postcoital bradycardia.
Both oxytocin and vasopressin could participate in the coordination of autonomic and behavioral phenomena associated with
sexual arousal and orgasm. It is likely that these compounds act
within both the central and peripheral nervous system, and affect the sympathetic and parasympathetic control of genital and
extragenital responses. Pharmacological studies and the complex
neurochemistry of the paraventricular and supraoptic nuclei support the hypothesis that oxytocin and vasopressin interact with
each other and a myriad of other neurochemicals to regulate autonomic function (65,164).
OTHERNEUROCHEMICALSIMPLICATEDIN
SEXUALBEHAVIORANDOXYTOCINRELEASE

137

induce or facilitate orgasmic-like sensations [reviewed (148)].

Apomorphine treatment in normal men can stimulate erection
(91). In animals, dopaminergic agonists also tend to accelerate
or enhance sexual activity. Everitt (53) specifically has implicated dopamine in appetitive versus copulatory components of
sexual behavior. These effects are complex and may vary according to the brain region and type of dopamine receptor that
is affected (53, 74, 178).
Dopamine plays an important role in milk production via its
inhibitory effects on prolactin (98). In addition, dopamine may
have a facilitatory effect on oxytocin release and mill ejection
in rats. Dopamine injections, given centrally, can excite pulsatile oxytocin (and vasopressin) release in rats (109). High dosages of dopamine produce a sustained release of hormones from
the posterior pituitary (37). Dopaminergic synapses have been
identified in conjunction with oxytocin (19). Dopamine also may
inhibit the release of oxytocin, indicating that the interactions
among dopaminergic and oxytocinergic processes are complex.

Norepinephrine
Norepinephfine plays a role in mate sexual behavior, and alpha-adrenergic receptors have been implicated in this response
(34-36). Research in rats suggests that alpha-1 adrenergic receptors facilitate and alpha-2 adrenergic receptors inhibit male sexual behavior. Norepinephrine can act at alpha-adrenergic receptors
to activate the release of oxytocin and may inhibit the milk-ejection reflex at beta-adrenergic receptors (175). Both steroid hormones and norepinephrine also have been indirectly implicated
in the release of oxytocin (40). The effects of catecholamines
are presumably multifaceted and may include interactions with
other hormones, neurotransmitters or neuromodulators or their
enzymes or receptors. For example, norepinephrine, via alphaadrenergic receptors, can modulate the concentration of estrogen
receptors (15,16). Opiates and monoamines also may interact to
regulate sexual behavior (50).

Opiates
Chronic opioid exposure inhibits various aspects of reproduction, including sexual behavior (1, 131, 180), maternal behavior
(79,122), and milk ejection (175). Oxytocin release also is inhibited by the endogenous opiates (13, 14, 94, 147). The endogenous opiates have complex functions and may participate in
the fine tuning of behavioral interactions such as those associated with sexual behavior and social bonding (82, 83, 86, 124).
An abundance of evidence implicates the endogenous opiates in
processes associated with social behavior, tactile sensitivity and
pain (50).
Acute opiate use has been associated with orgasmic-like experiences, but reports of this association are based upon anecdotes (131,148). There also have been cor~tradictory reports
regarding the behavioral effects of opioid antagonists (116,131 ).
Murphy and associates (ll6) have recently reported a doubleblind cross-over study of the effects of naloxone infusion on
male sexual behavior and concurrent oxytocin release. Naloxone
infusion blocked the peripheral release of oxytocin usually present
at orgasm. Naloxone-treated men also reported reductions in
subjective arousal and reported lower levels of pleasure during
orgasm. Murphy and associates suggest that the inhibitory effects of naloxone in their study involve "central nervous system
arousal mechanisms."

Dopamine
There are anecdotal reports that the intravenous use of stimulants, such as amphetamines, which release catecholamines, may

GABA
Oxytocin release is tonically inhibited by gamma-aminobutyric acid (GABA). GABAergic innervation has been implicated
in the timing of glial retraction that is believed to regulate the
pulsatile release of oxytocin (167). GABA also may inhibit sexual behavior, at least in rats (129,130). The possibility exists that
shared mechanisms underlie these observations.

Other Neurochemicals
The neurochemistry of sexual behavior is complex and beyond the scope of this review. Various neurotransmitters and
brain regions that have been implicated in sexual behavior (45,
49, 139) appear to have relatively parallel functions in the regulation of oxytocin release and milk ejection (175).
HYPOTHESESREGARDINGTHE ROLEOF
OXYTOCININ SEXUALBEHAVIOR
Oxytocin has been implicated in many aspects of sexual behavior. Circumstantial evidence suggests the general hypothesis
that relationships exist among the neural events associated with
the release of oxytocin and those associated with orgasm. The
coordinated central, spinal and peripheral release of oxytocin
makes this hormone a particularly attractive candidate for a role
in the mediation of the sequential events in the sexual behavior.
In the absence of evidence to the contrary, multiple functions
for oxytocin are hypotbesized. At this stage in our understand-

138

CARTER

ing of the behavioral effects of oxytocin, these hypotheses are

admittedly untested and highly speculative. The broad behavioral
actions of the steroid hormones offer precedent for the possibility that oxytocin may have multiple behavioral actions. The following hypotheses are drawn primarily from studies of laboratory
animals. Based on species differences in behavior and reproductive functions, and again on precedent from the steroid hormones, we also anticipate species differences in the behavioral
effects of oxytocin. It is assumed here that all effects of oxytocin are present within the context of other hormones and neurotransmitters.

paraventricular and/or supraoptic nuclei). Transition from the

plateau stage to the experience of orgasm in humans might be
triggered by neurochemical events that specifically induce the
pulsatile release of oxytocin. In their studies of penile erection,
Argiolas and Gessa (2) have provided evidence for a positive
feedback of oxytocin within the paraventricular nucleus. Additional studies of sexual behavior, which take into account the
research on neuroanatomical events during oxytocin release (69,
104, 114), may provide insights into the plausibility of this
hypothesis.

Hypothesis 3
SPECIFIC HYPOTHESES

Oxytocin could participate at several levels in the sexual response: 1) The initial central release of relatively small amounts
of oxytocin might prime or stimulate preorgasmic sexual activity. 2) The initial release of oxytocin also might initiate a subsequent pulsatile release of endogenous central and/or peripheral
oxytocin. 3) The pulsatile release of oxytocin could play a direct and/or indirect role in the experience of orgasm. 4) Physiological events following the release of oxytocin, including transitory
central depletion of oxytocin and/or the aftermath of exposure to
high levels of central and/or peripheral oxytocin might constitute
components of sexual satiety or the postorgasmic refractory
state. 5) Sex differences in oxytocinergic activity and steroid
hormones might contribute to sex differences in sexual responsivity or patterns of sexual satiety.

Hypothesis 1
Small amounts of oxytocin or initial exposure to oxytocin
could facilitate precopulatory events, including sexual arousal or
excitement. Initial release of oxytocin could be facilitated by
sexually arousing stimuli including nongenital touch (161), genital or breast stimulation, and cognitively conditioned events
(175). Vasopressin, which increases measurably during sexual
arousal (117), also might participate in the events leading to orgasm or other aspects of sexual behavior (45). Oxytocin release
has been measured after mounting in rabbits (170) and prairie
voles (Winslow, Williams, Hastings, Insel and Carter, unpublished data). Carmichael and associates (24) reported gradual increases in peripheral oxytocin during self-stimulation in both
men and women, and a slight increase in oxytocin was measured
in men during the excitement phase of the sexual response cycle
by Murphy and associates [(117): Table 1]. A more recent report from Murphy (116), however, does not show increases in
peripheral levels of oxytocin in samples taken after arousal to
the point of erection (prior to self-stimulation). Methodological
differences or individual differences may explain these results.
It is possible that different paradigms were differentially stressful, possibility contributing to the preorgasmic release of oxytocin under some, but not all, test conditions. In addition, the
relationship between central and peripheral oxytocinergic events
during male sexual behavior remains undescribed. Hypothesis 1
focuses on central neural events associated with the release of
oxytocin, although research on this problem, at least in males,
has been limited to studies measuring serum levels of oxytocin.

Hypothesis 2
Oxytocin, released centrally during early stages of sexual excitement could, through positive feedback, prime the nervous
system to permit a larger, pulsatile release of oxytocin. Among
the events leading to the pulsatile release of oxytocin might be a
coupling of oxytocinergic neurons (presumably within the

When adequate priming has been achieved, electrical coupling among oxytocin-producing cells would be possible (69).
The pulsatile release of oxytocin might in turn influence electrical activity within the central nervous system, which could be
manifest as measurable changes in EEG, "altered states of consciousness" and other behavioral and autonomic events described above (38, 41, 85, 89). It is interesting to note that, in
the context of milk ejection in rats, Wakerley and associates
(176) report that centrally administered oxytocin produced synchronization of the cortical EEG. After milk ejection, which was
facilitated by this treatment, desynchronization of the EEG was
observed. Because milk ejection can occur in some cases without changes in the EEG, these authors suggest that cortical EEG
reflects "'an underlying common control and not part of the direct regulation of the milk ejection reflex."
The peripheral release of oxytocin might coordinate the phenomenology of orgasm with contractions of the male and female
reproductive tracts and, thus, facilitate sperm transport. Failure
to achieve adequate priming due to interference with this process at one or more levels could be associated with anorgasmia.
The ability to achieve orgasm, or variability in the subjective
experience of orgasm, could reflect variability in the release of
oxytocin or other neural events including those responsible for
or associated with the release of oxytocin.
A variety of neurochemical processes support the pulsatile
release of oxytocin; drugs, stress or other processes that interfere with the release of oxytocin might inhibit sexual excitement.
For example, endogenous opiates (endorphins), GABA or progesterone could inhibit, or selectively permit the release of, both
oxytocin and sexual excitement/orgasm. Events associated with
the release of oxytocin, for example, catecholaminergic activity,
might play a role in the release of oxytocin and/or in the subjective or rewarding experience of orgasm. Peripheral autonomic
events coordinated in part by the release of oxytocin, could produce changes in heart rate, blood pressure, and respiration which
would be experienced as components of sexual arousal and orgasm.

Hypothesis 4
Several authors have suggested that oxytocin might be involved in sexual "satiety." Oxytocin injections, especially in
large dosages, can inhibit sexual activity in rodents (97, 162,
170). Elevations in peripheral oxytocin or the aftermath of exposure to large oxytocin pulses might be experienced as a physical state such as that which follows orgasm. Exposure to a large
pulse or high levels of oxytocin also might inhibit subsequent
oxytocin release or otherwise alter the function of cells that release or respond to oxytocin.
Hughes and associates (73) found that lesions to the parvocellular PVN, which spared the ability of the magnocellular elements to produce peripheral oxytocin, were associated with a
more rapid resumption of sexual activity following ejaculation.

OXYTOCIN AND SEXUAL BEHAVIOR

139

This study implicates intracerebral oxytocin in sexual satiety,

since the peripheral release of oxytocin remained intact. The
PVN also is rich in other behaviorally active chemicals (143)
and the specificity of the effects of these lesions remains to be
demonstrated.
In general, research on sexual behavior has focused on its
induction and relatively little is known regarding the naturally
occurring events responsible for terminating sexual activity. Repeated sexual experience is usually associated with a transient
reduction in subsequent sexual behavior (or sexual satiety). Time
(a refractory period) might be required for the repletion of coitally released oxytocin. Other neural events, including the release of various hormones and neurotransmitters with potential
inhibitory effects, also could be responsible for sexual satiety. A
variety of other chemicals including, for example, serotonin,
opiates (49, 50, 116, 131, 139) and vasopressin (106,158), may
participate in the inhibition of sexual behavior and/or in sexual
satiety. Patterns of sexual behavior and satiety are species specific (25, 187, 188). The neurochemistry of these events also
may differ among species.

Hypothesis 5
Oxytocin released during or after coitus could influence the
development of subsequent social attachments. Research in prairie voles (27,187) and rats (184) has shown that intracranial injections of oxytocin produce increases in social contact. Keverne
and his associates (81-83) have implicated oxytocin in filial attachment in sheep. The release of oxytocin during sexual behavior also could function to reinforce social bonds between sexual
partners. Recent data from prairie voles, a species that develops
male-female pair bonds, suggest that either sexual experience or
oxytocin treatment may facilitate subsequent social bond formation (27),

H3pothesis 6
Sex and/or species difference in oxytocin and differential effects of steroid hormones could modulate sex differences, species differences and individual differences in sexual responses.
Oxytocinergic functions can differ among individuals and between males and females (142). In particular, there are sex differences in the stress-related release of oxytocin (29-31). In
addition, steroid hormones modulate the release of oxytocin and
oxytocin receptors. Oxytocin (109) and steroids (112) also have
direct effects on glial morphology in rats and, thus, may influence the pulsatile release of oxytocin. These findings suggest a
substrate that could explain, in part, interspecific differences, sex
differences, individual differences and within-individual variations in sexual responsivity.

pulses are not readily measured in human serum, especially in

samples from men (142). Thus, the finding that oxytocin is released during orgasm in both sexes has stimulated interest in the
possible functions of this hormone.
The behavioral effects of manipulations of central oxytocin
in humans remain to be described. Oxytocin (Syntocinon, Sandoz Pharmaceuticals) has been administered intranasally as an
aid to lactation, although little is known regarding the behavioral effects of such treatments. Intranasal or peripheral administration of oxytocin could be used in controlled studies to examine
the behavioral effects of this hormone in normal or sexually
dysfunctional men or women. Several of the hypotheses proposed here could be examined indirectly through correlational
studies of variations in human sexual function and dysfunction,
such as those that occur during the menstrual cycle, lactation,
aging and during hormone-replacement therapies. For example,
there are indications that lactation can inhibit sexual behavior in
human females (134). Assessment of the behavioral effects of
lactation on human behavior will require a much more detailed
individual analysis of patterns of lactation and oxytocin release
than is available in the current literature.
Animal research examining the role of oxytocin in sexual behavior is ongoing in several laboratories. The hypotheses described above, suggesting that low levels of or initial increases
in oxytocin may facilitate, while high levels or prolonged exposure to oxytocin may inhibit male sexual behavior in rats, were
derived from data scattered among several studies. Support for
this hypothesis comes from recent unpublished studies of penile
erections by Argiolas and Gessa [cited in (21]. Additional studies are needed to compare, within a consistent animal model,
the broader behavioral effects of different dosages, modes of administration, and so forth of oxytocin. Animal models would be
particularly useful to examine potential effects of oxytocin on
motivational versus ejaculatory processes in sexual behavior.
Behavioral effects of oxytocin extend beyond copulatory behavior and may influence processes such as social bond formation
(27, 28, 81-83, 182), aggression (187) and social dominance
(183), which could in turn influence sexual behavior. Animal
research is also needed to examine the possible behavioral effects of vasopressin and interactions among vasopressin, oxytocin and other behaviorally active neurochemicals. Differences
and similarities between the sexes and among species may be
particularly valuable in providing insights into the behavioral effects of oxytocin. In the absence of directly relevant research,
the hypotheses presented here remain largely untested. Relationships between oxytocin and sexual behavior may be due to direct actions of oxytocin or could be indirectly mediated by other
central neural events that influence both oxytocinergic activity
and sexual behavior.
ACKNOWLEDGEMENTS

Summao, and Critique

As described above, most of the research implicating oxytocin in sexual behavior has appeared within the last decade. At
present, the published research relating oxytocin to human sexual behavior is limited in scope and is primarily correlational
(24, 116, 117, 123). Aside from its release during birth (31) and
lactation (175), oxytocin levels are low in humans and oxytocin

I am grateful to the following for the generous contribution of ideas,

suggestions, and references which have been invaluable in the development of this paper: Stephen Porges. Diane Witt. Tom lnsel, Jessie
Williams, Julian Davidson, Barry Keverne, Stafford Lightman, Glenn
Hanon. Jack Caldwell, AI Johnson, Elaine Hull and two anonymous reviewers. Research described here as contributions from my laboratory
was supported by NSF (BNS 87197481.

REFERENCES
1. Almeida, O. F. X.; Nikolarakis, K. E.; Sirinathsinghji, D. J. S.;
Herz, A. Opioid-mediated inhibition of sexual behaviour and
luteinizing hormone secretion by corticotrophin releasing hormone.
In: Dyer, R. G.; Bicknell, R. J., eds. Brain opioid systems in re-

production. Oxford: Oxford University Press; 1989:149-164.

2. Argiolas, A.; Gessa. G. L. Central functions of oxytocin. Neurosci. Biobehav. Rev. 15:217-231: 1991.
3. Argiolas, A.; Melis, M. R.: Vargiu, L.; Gessa, G. L.

140

4.

5.
6.
7.

8.

9.

10.
11.

12.

13.

14.

15.
16.

17.
18.

19.

20.

21.

22.

23.
24.

25.

26.

27.

CARTER

d(CH_,)sTyr(Me)-[Orna]vasotocin, a potent oxytocin antagonist, antagonizes penile erection and yawning induced by oxytocin and
apomorphine, but not ACTH-(I-24). Eur. J. Pharmacol. 134:221224; 1987.
Argiolas, A.; Collu, M.; Gessa, G. L.; Melis, M. R.; Serra, G.
The oxytocin antagonist d(CH2)5Tyr(Me)-OrnS-vasotocin inhibits
male copulatory behaviour in rats. Eur. J. Pharmacol. 149:389392; 1988.
Arletti, R.; Bertolini, A. Oxytocin stimulates lordosis behavior in
female rats. Neuropeptides 6:247-253; 1985.
Arletti, R.; Benelli, A.; Bertolini, A. Influence of oxytocin on
feeding behavior in the rat. Peptides 10:89-93; 1989.
Arletti, R.; Bazzani, C.; Castelli, M.; Bertolini, A. Oxytocin improves male copulatory performance in rats. Horm. Behav. 19:1420; 1985.
Bancroft, J.; Wu, F. C. W. Changes in erectile responsiveness
during androgen replacement therapy. Arch. Sex. Behav. 12:5966; 1983.
Bancroft, J.; Tennent, T. G.; Loucas, K.; Cass, J. Control of deviant sexual behaviour by drugs: behavioural effects of oestrogens
and anti-androgens. Br. J. Psychiatry 125:310-315; 1974.
Bargmann, W.; Scharrer, E. The origin of the posterior pituitary
hormones. Am. Sci. 39:255-249; 1951.
Belis, V.; Moos, F. Paired recordings from supraoptic and
paraventricular oxytocin cells in suckled rats: recruitment and synchronization. J. Physiol. 377:369-390; 1986.
Benson, G. S. Male sexual function: erection, emission, and ejaculation. In: Knobil, E.; Neill, J. et al., eds. The physiology of
reproduction. New York: Raven Press; 1988:1121-1139.
Bicknell, R. J.; Leng, G. Endogenous opiates regulate oxytocin but
not vasopressin secretion from the neurohypophysis. Nature 298:
161-162; 1982.
Bicknell, R. J.; Zhao, B.-G. Secretory terminals of oxytocin neutones as a site of opioid modulation. In: Dyer, R. G.; Bicknell, R.
J., eds. Brain opioid systems in reproduction. Oxford: Oxford
University Press; 1989:288-306.
Blaustein, J. D. Steroid receptors and hormone action in the brain.
Ann. NY Acad. Sci. 474:400--414; 1986.
Blaustein, J. D.; Brown, T. J. Neural progestin receptors: regulation of progesterone-facilitated sexual behaviour in female guinea
pigs. In: Gilles, R.; Balthazart, J., eds. Neurobiology. Berlin:
Springer-Verlag; 1985:60-76.
Blumer, D. Changes of sexual behavior related to temporal lobe
disorders in man. J. Sex. Res. 6:173-180; 1970.
Bohlen, J. G.; Held, J. P.; Sanderson, M. L.; Patterson, R. P.
Heart rate, rate-pressure product, and oxygen uptake during four
sexual activities. Arch. Int. Med. 144:1745-1748; 1984.
Buijs, R. M.; De Vries, G. J.; Van Leeuwen, R. W.; Swaab, D.
F. Vasopressin and oxytocin: distribution and putative functions in
the brain. In: Cross, B. A.; Leng, G., eds. Structure, function,
and control, progress in brain research. Amsterdam: Elsevier; 1983:
115-122.
Bun-is, A. S.; Gracely, R. H.; Carter, C. S.; Sherins, R. J.; Davidson, J. M. Testosterone therapy is associated with reduced tactile
sensitivity in human males. Horm. Behav. 25:195-205; 1991.
Caldwell, J. D.; Prange, A. J., Jr.; Pedersen, C. A. Oxytocin facilitates the sexual receptivity of estrogen-treated female rats. Neuropeptides 7:175-189; 1986.
Campbell, B. Neurophysiology of the clitoris. In: Lowry, T. P.;
Lowry, T. S., eds. The clitoris. St. Louis: W. H. Green; 1976:
35-74.
Campbell, B.; Pedersen, W. E. Milk let down and the orgasm in
the human female. Hum. Biol. 25:165-168; 1953.
Carmichael, M. S.; Humbert, R.; Dixen, J.; Palmisano, G.; Greenleaf, W.; Davidson, J. Plasma oxytocin increases in the human
sexual response. J. Clin. Endocrinol. Metab. 64:27-31; 1987.
Carter, C. S. Female sexual behavior. In: Siegel, H. I., ed. The
hamster: Reproduction and behavior. New York: Plenum Press;
1985:173-189.
Carter, C. S.; Getz, L. L.; Cohen-Parsons, M. Relationships between social organization and behavioral endocrinology in a monogamous mammal. Adv. Study Behav. 16: 109-145; 1986.
Carter, C. S.; Williams, J. R.; Insel, T. R. Oxytocin and social

bonding. Ann. NY Acad. Sci., in press; 1992.

28. Carter, C. S.; Williams, J. R.; Witt, D. M. The biology of social
bonding in a monogamous mammal. In: Balthazart, J., ed. Hormones, brain and behavior. Basel: Karger; 1990:154-164.
29. Carter, D. A.; Lightman, S. L. Diurnal pattern of stress-evoked
neurohypophyseal hormone secretion: sexual dimorphism in rats.
Neurosci. Lett. 71:252-255; 1986.
30. Carter, D. A.; Lightman, S. L. Modulation of oxytocin secretion
by ascending noradrenergic pathways: sexual dimorphism in rats.
Brain Res. 406:313-316; 1987.
31. Carter, D. A.; Williams, D. M.; Lightman, S. L. A sex difference
in endogenous opioid regulation of the posterior pituitary response
to stress in the rat. J. Endocrinol. I I 1:239-244; 1986.
32. Challis, J. R. G.; Olson, D. M. Parturition. In: Knobil, E.; Neill,
J. et al., eds. The physiology of reproduction. New York: Raven
Press; 1988:2177-2216.
33. Chung, S. K.; McVary, K. T.; McKenna, K. E. Sexual reflexes
in male and female rats. Neurosci. Lett. 94:343-348; 1988.
34. Clark, J. T.; Smith, E. R.; Davidson, J. M. Enhancement of sexual motivation in male rats by yohimbine. Science 225:847-849;
1984.
35. Clark, J. T.; Smith, E. R.; Davidson, J. M. Evidence for the
modulation of sexual behavior by et-adrenoceptors in male rats.
Neuroendocrinology 41:36-43; 1985.
36. Clark, J. T.; Smith, E. R.; Davidson, J. M. Testosterone is not
required for the enhancement of sexual motivation by yohimbine.
Physiol. Behav. 35:517-521; 1985.
37. Clarke, G.; Lincoln, D. W.; Merrick, L. P. Dopaminergic control
of oxytocin release in lactating rats. J. Endocrinol. 83:409-420;
1979.
38. Cohen, H. D.; Rosen, R. C.; Goldstein, L. Electroencephalographic laterality changes during human sexual orgasm. Arch. Sex.
Behav. 5:189-199; 1976.
39. Contreras, J. L.; Beyer, C. A polygraphic analysis of mounting
and ejaculation in the New Zealand white rabbit. Physiol. Behav.
23:939-943; 1979.
40. Crowley, W. R.; O'Donahue, T. L.; George, J. M.; Jacobowitz,
D. M. Changes in pituitary oxytocin and vasopressin during the
estrous cycle and after ovarian hormones: evidence for the mediation of norepinephrine. Life Sci. 23:2579-2586; 1978.
41. Davidson, J. M. The psychobiology of sexual experience. In:
Davidson, J. M.; Davidson, R. J., eds. The psychobiology of consciousness. New York: Plenum Press; 1980:271-332.
42. Davidson, J. M.; Camargo, C.; Smith, E. R. Effects of androgen
on sexual behavior in hypogonadal men. J. Clin. Endocrinol.
Metab. 48:955-958; 1979.
43. Davidson, J. M.; Kwan, M.; Greenleaf, W. Hormonal replacement
and sexuality in men. In: Bancroft, J., ed. Clinics in endocrinology and metabolism, vol. II. London: Saunders; 1982:599-624.
44. Davidson, J. M.; Chen J. J.; Crapo, L.; Gray, G. D.; Greenleaf,
W. J.; Catania, J. A. Hormonal changes and sexual function in
aging men. J. Clin. Endocrinol. Metab. 57:71-77; 1983.
45. De Vries, G. J. Sex differences in neurotransmitter systems. J.
Neuroendocrinol. 2:1-13; 1990.
46. Dewsbury, D. A. Patterns of copulatory behavior in male mammals. Q. Rev. Biol. 47:1-33; 1972.
47. Dewsbury, D. A. The comparative psychology of monogamy. In:
Leger, D. W. Nebraska symposium on motivation. Lincoln, NE:
University of Nebraska Press; 1987:1-50.
48. Diakow, C. Hormonal basis for breeding behavior in female frogs:
vasotocin inhibits the release call of Rana pipiens. Science 199:
1456-1457; 1978.
49. Doman, W. A.; Malsbury, C. W. Neuropeptides and male sexual
behavior. Neurosci. Biobehav. Rev. 13:1-15; 1989.
50. Dyer, R. G.; Bicknell, R. J., eds. Brain opioid systems in reproduction. Oxford: Oxford University Press; 1989.
51. Epstein, A. W. The relationship of altered brain states to sexual
psychopathology. In: Zubin, J.; Money, J., eds. Contemporary
sexual behavior. Baltimore: Johns Hopkins University Press: 1973:
297-310.
52. Ermisch, A.; Barth, T.; Ruhle, H. J.; Okopkova, J.; Hrbas, P.;
Landgraf, H. On the blood-brain barrier to peptides: accumulation
of labelled vasopressin, desglyNH2-vasopressin and oxytocin by

OXYTOCIN

AND

SEXUAL

BEHAVIOR

brain regions. Endocrinol. Exp. 19:29-37; 1985.

53. Everitt, B. J. Sexual motivation: a neural and behavioural analysis
of the mechanisms underlying appetitive and copulatory responses
of male rats. Neurosci. Biobehav. Rev. 14:217-232; 1990.
54. Falke, N. Oxytocin stimulates oxytocin release from isolated nerve
termnals of rat neural lobes. Neuropeptides 14:269-274; 1989.
55. Fisher, S. The female orgasm. New York: Basic Books; 1973.
56. Fitzpatrick, R. J. The posterior pituitary gland and the male reproductive tract. In: Harris, G. W.; Donovan, B. T., eds. The pituitary gland, vol. 3: Pars intermedia and neurohypophysis. London:
Butterworths; 1966:505-516.
57. Fjellstrom, D.; Kihlstrom, J. E.; Melin, P. The effect of synthetic
oxytocin upon seminal characteristics and sexual behaviour in male
rabbits. J. Reprod. Fertil. 17:207-209; 1968.
58. Fox, C. A.; Knaggs, G. S. Milk-ejection activity (oxytocin) in peripheral venous blood in man during lactation and in association
with coitus. J. Endocrinol. 45:145-146; 1969.
59. Freund-Mercier, M.-J.; Richard, P. Electrophysiological evidence
for facilitatory control of oxytocin neurones by oxytocin during
suckling in the rat. J. Physiol. 352:447-466; 1984.
60. Freund-Mercier, M.-J.; Stoeckel, M. E.; Palacios, J. M.; Paxos,
A.; Reichhart, J. M.; Porte, A.; Richard, P. Pharmacological
characteristics and anatomical distribution of [3H] oxytocin-binding
sites in the Wistar rat brain studied by autoradiography. Neuroscience 20:599-614; 1987.
61. Fuchs, A.-R.; Dawood, M. Y. Oxytocin release and uterine activation during parturition in rabbits. Endocrinology 107:1117-1126;
1980.
62. Fuchs, A.-R.; Ayromlooi, J.; Rasmussen, A. B. Oxytocin response
to conditioned and nonconditioned stimuli in lactating ewes. Biol.
Reprod. 37:301-305; 1987.
63. Fuchs, A.-R.; Cubile, L.; Dawood, M. Y. Effects of mating on
levels of oxytocin and prolactin in the plasma of male and female
rabbits. J. Endocrinol. 90:245-253; 1981.
64. Fuchs, A.-R.; Fuchs, F.; Husslein, P.; Soloff, M. S.; Fenstrom,
M. J. Oxytocin receptors and human parturition: a dual role for
oxytocin in the initiation of labor. Science 215:1396-1398; 1982.
65. Gainer, H.; Altstein, M.; Whitnall, Wray, S. The biosynthesis and
secretion of oxytocin and vasopressin. In: Knobil, E.; Neill, J. et
al., eds. The physiology of reproduction. New York: Raven Press;
1988:2265-2281.
66. Gorzalka, B. B.; Lester, G. L. Oxytocin-induced facilitation of
lordosis behavior in rats is progesterone dependent. Neuropeptides
10:55-65; 1987.
67. Hansen, S.; Kohler, C. The importance of the peripeduncular nucleus in the neuroendocrine control of sexual behavior and milk
ejection in the rat. Neuroendocrinology 39:563-572; 1984.
68. Hashimoto, H.; Noto, T.; Nakajama, T. A study of the release
mechanism of vasopressin and oxytocin. Neuropeptides 12:199206; 1988.
69. Hatton, G. I. Cellular reorganization in neuroendocrine secretion.
In: Ganten, D.; Pfaff, D., eds. Current topics in neuroendocrinology, vol. 9. Berlin: Springer-Verlag; 1988:1-27.
70. Hatton, G. I.; Tweedle, C. D. Magnocellular neuropeptidergic
neurons in hypothalamus: Increases in membrane apposition and
number of specialized synapses from pregnancy to lactation. Brain
Res. Bull. 8:197-204; 1982.
71. Heap, R. B. New functions for oxytocin? Nature 301:113; 1983.
72. Hoenig, J.; Hamilton, D. Epilepsy and sexual orgasm. Acta Psychiatr. Neurol. Scand. 35:448-457; 1960.
73. Hughes, A. M.; Everitt, B. J.; Lightman, S. L.; Todd, K. Oxytocin in the central nervous system and sexual behavior in male rats.
Brain Res. 414:133-137; 1987.
74. Hull, E. M.; Bazzett, R. J.; Warner, R. K.; Eaton, R. C.;
Thompson, J. T. Dopamine receptors in the ventral tegmental area
modulate male sexual behavior in rats. Brain Res. 512:1-6; 1990.
75. Insel, T. R. Oxytocin and maternal behavior. In: Krasnegor, N.
A.; Bridges, R. S., eds. Mammalian parenting. New York: Oxford
University Press; 1990:260-280.
76. Insel, T. R. Oxytocin: A neuropeptide for affiliation--Evidence
from behavioral, receptor autoradiographic, and comparative studies. Psychoneuroendocrinology; in press.
77. Johnson, A. E.; Coirini, H.; Ball, G. F.; McEwen, B. S. Anatom-

141

78.

79.

80.
81.

82.

83.

84.
85.

86.
87.

88.

89.

90.

91.

92.

93.
94.

95.

96.

97.

98.
99.

ical localization of the effects of 17 b-estradiol on oxytocin receptor binding in the ventromedial hypothalamic nucleus. Endocrinology
124:207-211; 1989.
Johnson, A. E.; Coirini, H.; McEwen, B. S.; Insel, T. R. Testosterone modulates oxytocin binding in the hypothalamus of castrated
male rats. Neuroendocrinology 50:199-203; 1989.
Johnson, A. E.; Ball, G. R.; Coirini, H.; Harbaugh, C. R.;
McEwen, B. S.; Insel, T. R. Time course of the estradiol dependent induction of oxytocin receptor binding in the ventromedial
hypothalamic nucleus of the rat. Endocrinology 125:1414--1419;
1989.
Kaplan, H. S. The new sex therapy. New York: Brunner/Mazel;
1974.
Kendrick, K. M.; Keverne, E. B.; Baldwin, B. A.; Sharman, D.
F. Cerebrospinal fluid levels of acetylcholinesterase, monoamines
and oxytocin during labour, parturition, vaginocervical stimulation,
lamb separation and suckling in sheep. Neuroendocrinology 44:
149-156; 1986.
Keverne, E. B. Central mechanisms underlying the neural and
neuroendocrine determinants of maternal behaviour. Psychoneuroendocrinology 13:127-141; 1988.
Keverne, E. B.; Kendrick, K. M. Neurochemical changes accompanying parturition and their significance for maternal behavior. In:
Krasnegor, N. A.; Bridges, R. S., eds. Mammalian parenting.
New York: Oxford University Press; 1990:281-304.
Kinsey, A. C.; Pomeroy, W. B.; Martin, C. E. Sexual behavior in
the human male. Philadelphia: W. B. Saunders; 1948.
Kinsey, A. C.; Pomeroy, W. B.; Martin, C. E.; Gebhard, P. H.
Sexual behavior in the human female. Philadelphia: W. B. Saunders; 1953.
Klopfer, P. H. Mother love: What turns it on? Am. Sci. 59:404407; 1971.
Kluver, H.; Bucy, P. C. Preliminary analysis of functions of the
temporal lobes in monkeys. Arch. Neurol. Psychiatry 42:9791000; 1939.
Knobil, E.; Neill, J. D.; Ewing, L. L.; Greenwald, G. S.; Markert,
C. L.; Pfaff, D. W. The physiology of reproduction. New York:
Raven Press; 1988.
Komisaruk, B. R. The nature of the neural substrate of female
sexual behavior in mammals and its hormonal sensitivity: review
and speculations. In: Hutchison, J. B., ed. Biological determinants
of sexual behaviour. New York: Wiley; 1978:349-393.
Kwan, M.; Greenleaf, W. J.; Mann, J.; Crapo, L.; Davidson, J.
M. The nature of androgen action on male sexuality: A combined
laboratory-self report study on hypogonadal men. J. Clin. Endocrinol. Metab. 57:557-562; 1983.
Lal, S.; Ackman, D.; Thavundayil, J. X.; Kiely, M. E.; Etienne,
P. Effect of apomorphine, a dopamine receptor agonist, on penile
tumescence in normal subjects. Prog. Neuropsychopharmacol. Biol.
Psychiatry 8:695-699; 1984.
Landgraf, R.; Ermisch, A.; Heb, J. Indications for brain uptake of
labelled vasopressin and oxytocin and the problem of the bloodbrain barrier. Endokrinologie 73:77-81; 1979.
Levin, R. J.; Wagner, G. Heart rate change and subjective intensity of orgasm in women. IRCS Med. Sci. 13:885-886; 1985.
Lightman, S. L.; Young, W. S., III. Lactation inhibits sn'ess-mediated secretion of corticosterone and oxytocin and hypothalamic
accumulation of corticotropin-releasing factor and enkephalin messenger ribonucleic acids. Endocrinology 124:2358-2364; 1989.
Lincoln, D. W.; Fraser, H. M.; Lincoln, G. A.; Martin, G. B.;
McNeilly, A. S. Hypothalamic pulse generators. Rec. Prog. Horm.
Res. 41:369-411; 1985.
Maggi, M.; Makozowski, S.; Kassis, S.; Guardabassao, V.; Rodbard, D. Identification and characterization of two classes of receptors for oxytocin and vasopressin in porcine tunica albuginea,
epididymis, and vas deferens. Endocrinology 120:986-994; 1987.
Mahalati, K.; Okanoya, K.; Witt, D. M.; Carter, C. S. Oxytocin
inhibits male sexual behavior in prairie voles. Pharmacol. Biochem. Behav. 39:219-222; 1991.
Masters, W. H.; Johnson, V. E. Human sexual response. Boston:
Little, Brown; 1966.
McNeilly, A. S. Suckling and the control of gonadotropin secretion. In: Knobil, E.; Neill, J. et al., eds. The physiology of repro-

142

duction. New York: Raven Press; 1988:2323-2349.

I00. Melin, P.; Kihlstrrm, J. E. Influence of oxytocin on sexual behaviors in male rabbits. Endocrinology 73:433-435; 1963.
101. Melis, M. R.; Argiolas, A.; Gessa, G. L. Oxytocin-induced penile
erection and yawning: Site of action in the brain. Brain Res. 398:
259-265; 1986.
102. Mena, R.; Clapp, C.; Martinez-Escalera, G.; Pacheco, P.; Grosvenor, C. E. Integrative regulation of milk ejection. In: Amico, J.
A.; Robinson, A. G., eds. Oxytocin: clinical and laboratory studies. Amsterdam: Elsevier Science Publ.; 1985:179-199.
103. Mens, W. B. J.; Witter, A.; Van Wimersma Greidanus, T. B.
Penetration of neurohypophyseal hormones from plasma into cerebrospinal fluid (CSF): half-times of disappearance of these neuropeptides from CSF. Brain Res. 262:143-149; 1983.
104. Modney, B. K.; Hatton, G. I. Motherhood modifies magnocellular
neuronal interrelationships in functionally meaningful ways. In:
Krasnegor, N. A.; Bridges, R. S., eds. Mammalian parenting.
New York: Oxford University Press; 1990:305-323.
105. Mogenson, G. J.; Jones, D. L.; Yim, C. Y. From motivation to
action: functional interface between the limbic system and the motor system. Prog. Neurobiol. 14:69-97; 1980.
106. Moltz, H. E-series prostaglandins and arginine vasopressin in the
modulation of male sexual behavior. Neurosci. Biobehav. Rev.
14:109-115; 1990.
107. Moody, K.; Donohue, C.; Steinman, J.; Komisaruk, B.; Adler, N.
Behavioral effects of exogenous oxytocin in moderately receptive
female rats. Conf. Reprod. Behav., Atlanta, GA; 1990:99.
108. Moore, F. L. Behavioral actions of neurohypophysial peptides. In:
Crews, D., ed. Psychobiology of reproductive behavior: an evolutionary perspective. Englewood Cliffs, NJ: Prentice Hall; 1987:6287.
109. Moos, F.; Richard, P. Excitatory effect of dopamine on oxytocin
and vasopressin reflex releases in the rat. Brain Res. 241:249-260;
1982.
110. Moos, F.; Freund-Mercier, M. J.; Guerue, Y.; Guerne. J. M.;
Stoeckel, M. E.; Richard, P. Release of oxytocin and vasopressin
by magnocellular nuclei in vitro: specific facititatory effect of oxytocin on its own release..I. Endocrinol. 102:63-72; 1984.
111. Monaghan, E. P.; Breedlove, S. M. Evidence for oxytocin innervation of perineal motor neurons in rats. Soc. Neurosci. Abstr. 13:
55; 1987.
112. Montagnese, C.; Poulain, D. A.; Theodosis, D. T. Influence of
ovarian steroids on the ultrastructural plasticity of adult rat supraoptic nucleus induced by central administration of oxytocin. J.
Neuroendocrinol. 2:225-230; 1990.
113. Montagnese, C. M.; Poulain, D. A.; Vincent, J.-D.; Theodosis,
D. T. Structural plasticity in the rat supraoptic nucleus during gestation, post-partum lactation and suckling-induced pseudogestation
and lactation. J. Endocrinol. 115:97-105; 1987.
114. Montagnese, C. M.; Poulain, D. A.; Vincent, J.-D.; Theodosis,
D. T. Synaptic and neuronal-glial plasticity in the adult oxytocinergic system in response to physiological stimuli. Brain Res. Bull.
20:681-692; 1988.
115. Mosovich, A.; Tallaferro, A. Studies on EEG and sex function orgasm. Dis. Nerv. Syst. 15:218-220; 1954.
116. Murphy, M. R.: Checkley, S. A.; Seckl. J. R.; Lightman. S. L.
Naloxone inhibits oxytocin release at orgasm in man. J. Clin. Endocrinol. Metab. 71:1056-1058; 1990.
117. Murphy, M. R.; Seckl, J. R.; Burton, S.; Checkley, S. A.; Lightman, S. L. Changes in oxytocin and vasopressin secretion during
sexual activity in men. J. Clin. Endocrinol. Metab. 65:738-741;
1987.
118. Newton, N. Interrelationships between sexual responsiveness, birth,
and breast feeding. In: Zubin, J.; Money, J., eds. Contemporary
sexual behavior: critical issues in the 1970s. Baltimore: Johns
Hopkins University Press; 1973:77-98.
119. Newton, N. The role of the oxytocin reflexes in three interpersonal
reproductive acts: coitus, birth and breastfeeding. In: Carenza, L.;
Pancheri, P.; Zichella, L., eds. Clinical psychoneuroendocrinology
in reproduction. New York: Academic Press; 1978:411-418.
120. Nicolson, H. D.; Swann, R. W.; Burford, G. D.; Wathes, D. C.;
Porter, D. C.; Pickering, B. T. Identification of oxytocin and vasopressin in the testes and adrenal tissue. Regul. Pept. 8:141-146:

CARTER

1984.
121. Niemo, M.; Kormano, B. Contractility of the seminiferous tubules
of the rat testis and its response to oxytocin. Ann. Med. Exp. Biol.
Fenn. 43:40-42; 1965.
122. Numan, M. Maternal behavior. In: Knobil, E.; Neill, J. et al., eds.
The physiology of reproduction. New York: Raven Press; 1988:
1569-1645.
123. Ogawa, S.; Kudo, S.; Kitsunai, Y.; Fukuchi, S. Increase in oxytocin secretion at ejaculation in male. Clin. Endocrinol. 13:95-97;
1980.
124. Panksepp, J.; Siviy, S. M.; Normansell, L. A. Brain opioids and
social emotions. In: Reite, M.; Field, T. M., eds. The psychobiology of attachment and separation. New York: Academic Press;
1985:3-49.
125. Pedersen, C. A.; Prange, A. J., Jr. Induction of maternal behavior
in virgin rats after intracerebroventricular administration of oxytocin. Proc. Natl. Acad. Sci. USA 76:6661-6665; 1979.
126. Pedersen, C. A.; Prange, A. J., Jr. Evidence that central oxytocin
plays a role in the activation of maternal behavior. In: Krasnegor,
N. A.; Blass, E. M.; Hofer, M. A.; Smotherman, W. P., eds.
Perinatal development: A psychobiological perspective. New York:
Academic Press; 1987:299-320.
127. Pedersen, C. A.; Caldwell, J. D.; Jirkowski, G. R. Oxytocin and
reproductive behaviors. In: Yoshida, S.; Share, L., eds. Recent
progress in posterior pituitary hormones 1988. Amsterdam: Excerpta Medica; 1988:127-132.
128. Persky, H. Psychoendocrinology of human sexual behavior. New
York: Praeger; 1987.
129. Pfaff, D. W. Multiplicative responses to hormones by hypothalamic neurons. In: Yoshida, S.; Share, L., eds. Recent progress in
posterior pituitary hormones 1988. Amsterdam: Excerpta Medica;
1988:257-267.
130. Pfaff, D. W.; Schwartz-Giblin, S. Cellular mechanisms of female
reproductive behaviors. In: Knobil, E.; Neill, J. et al., eds. The
physiology of reproduction. New York: Raven Press; 1988:14871568.
131. Pfaus, J. G.; Gorzalka, B. B. Opioids and sexual behavior. Neurosci. Biobehav. Rev. 11:1-34; 1987.
132. Poulain. D. A.; Theodosis. D. T. Coupling of electrical activity
and hormone release in mammalian neurosecretory neurons. In:
Ganten, D.; Pfaff, D., eds. Current topics in neuroendocrinology,
vol. 9. Berlin: Springer-Verlag; 1988:73-104.
133. Raggenbass, M.; Charpak, S.; Dubois-Dauphin, M.; Dreifuss, J.
J. Electrophysiological evidence for oxytocin receptors on neurones
located in the dorsal motor nucleus of the vagus nerve in the rat
brainstem. J. Recep. Res. 8:273-282; 1988.
134. Reamy, K. J.; White, S. E. Sexuality in the puerperium: A review. Arch. Sex. Behav. 16:165-186.
135. Rhodes, C. H.; Morrell, J. I.; Pfaff, D. W. Immunohistochemical
analysis of magnocellular elements in rat hypothalamus: distribution and numbers of cells containing neurophysin, oxytocin, and
vasopressin. J. Comp. Neurol. 198:45-64; 1981.
136. Rhodes, C. H.; Morrell, J. I.; Pfaff, D. W. Distribution of estrogen concentrating, neurophysin-containing magnocellular neurons
in the rat hypothalamus as demonstrated by a techniques combining steroid autoradiography and immunohistology in the same tissue. Neuroendocrinology 33:18-23; 1981.
137. Rhodes, C. H.; Morrell, J. I.; Pfaff, D. W. Estrogen-concentrating, neurophysin-containing hypothalamic magnocellular neurons
in the vasopressin-deficient (Brattleboro) rat: a study combining
steroid autoradiography and immunocytochemistry. J. Neurosci.
2:1718-1724; 1981.
138. Rosen, R. C.; Goldstein, L.; Scoles, V., lII; Lazarus, C. Psychophysiologic correlates of nocturnal penile tumescence in normal
males. Psychosom. Med. 48:423--429; 1986.
139. Sachs, B. D.; Meisel, R. L. The physiology of male sexual behavior. In: Knobil, E.; Neill, J. et al., eds. The physiology of reproduction. New York: Raven Press; 1988:1393-1485.
140. Salm, A. K.; Modney, B. K.; Hatton, G. I. Alternations in supraoptic nucleus ultrastructure of maternally behaving virgin rats.
Brain Res. Bull. 21:685-691; 1988.
141. Sanders, D.; Bancroft, J. Hormones and the sexuality of women-the menstrual cycle. Clin. Endocrinol. Metab. 11:639-659; 1982.

OXYTOCIN

AND SEXUAL

BEHAVIOR

142. Sanders, G.; Freilicher, J.; Lightman, S. L. Psychological stress

of exposure to uncontrollable noise increases plasma oxytocin in
high emotionality women. Psychoneuroendocrinology 15:47-58;
1990.
143. Sawchenko, P. E.; Swanson, L. W. The organization and biochemical specificity of afferent projections to the paraventricular
and supraoptic nuclei. In: Cross, B. A.; Leng, G., eds. The neurohypophysis: structure, function and control. Prog. Brain Res.
vol, 60. Amersterdam: Elsevier; 1983:19-29.
144. Schreiner, L.; Kling, A. Rhinencephalon and behavior. Am. J.
Physiol. 184:486--490; 1956.
145. Schumacher, M.; Coirini, H.; Frankfurt, M.; McEwen, B. S. Localized actions of progesterone in hypothalamus involve oxytocin.
Proc. Natl. Acad. Sci. USA 86:6798-6801; 1989.
146. Schumacher, M.; Coirini, H.; Pfaff, D. W.; McEwen, B. S. Behavioral effects of progesterone associated with rapid modulation
of oxytocin receptors. Science 250:691-694; 1990.
147. Seckl, J.; Lightman, S. L. Opioid peptides, oxytocin, and human
reproduction. In: Dyer, R. G.; Bicknell, R. J., eds. Brain opioid
systems in reproduction. Oxford: Oxford University Press; 1989:
309-324.
148. Segraves, R. T.; Madsen, R.; Carter, C. S.; Davis, J. M. Erectile
dysfunction associated with pharmacological agents. In: Segraves,
R. T.; Schoenberg, H. W., eds. Diagnosis and treatment of erectile disturbances. New York: Plenum Medical Book Company;
1985:23-63.
149. Shapiro, L. E.; Insel, T. R. Infant's response to social separation
reflects adult differences in affiliative behavior: a comparative developmental study in prairie and montane voles. Dev. Psychobiol.
23:375-394; 1990.
150. Sharma, O. P.; Hays, R. L. Release of an oxytocic substance following genital stimulation in bulls. J. Reprod. Fertil. 35:359-362;
1973.
151. Sharma, O. P.; Hays, R. L. A possible role for oxytocin in the
male rabbit. J. Endocrinol. 68:43-47, 1976.
152. Sharma, O. P.; Fitzpatrick, R. J.; Ward, W. R. Coital-induced release of oxytocin in the ram. J. Reprod. Fertil. 31:488-489. 1972.
153. Sheldrick, E. L.; Flint, A. P. F. Endocrine control of uterine oxytocin receptors in the ewe. J. Endocrinol. 106:249-258; 1985.
154. Sherfey, M. J. The nature and evolution of female sexuality. New
York: Random House; 1972.
155. Sherwin, B. B. A comparative analysis of the role of androgen in
human male and female sexual behavior: behavioral specificity,
critical thresholds, and sensitivity. Psychobiology 16:416-425; 1988.
156. Sherwin, B. B.; Gelfand, M. M.; Brender, W. Androgen enhances
sexual motivation in females: a prospective, crossover study of sex
steroid administration in the surgical menopause. Psychosom. Med.
47:339-351 ; 1985.
157. Smithson, K. G.; Weiss, M. L.; Hatton, G. I. Supraoptic nucleus
afferents from the main olfactory bulb--I, anatomical evidence
from anterograde and retrograde tracers in rat. Neuroscience 31:
277-287; 1989.
158. Sodersten. P.; Forsberg, G.; Bednar, I.; Eneroth, P.; WiesenfeldHallin, Z. Opioid peptide inhibition of sexual behaviour in female
rats. In: Dyer, R. G.; Bicknell, R. J., eds. Brain opioid systems
in reproduction. Oxford: Oxford University Press; 1989:201-215.
159. Sofroniew, M. V. Vasopressin, oxytocin and their related neurophysins. In: Bjorklund, A.; Hokfelt, T., eds. Handbook of chemical neuroanatomy. Amsterdam: Elsevier Science Publ.; 1985:93165.
160. Soloff, M. S. Oxytocin receptors and mechanisms of oxytocin action. In: Amico, J. A.; Robinson, A. G., eds. Oxytocin: clinical
and laboratory studies. Amsterdam: Else~,ier Science Publ.; 1985:
259-276.
161. Stock, S.; Uvnas-Moberg. K. Increased plasma levels of oxytocin
in response to afferent electrical stimulation of the sciatic and vagal nerves and in response to touch and pinch in anaesthetized rats.
Acta Physiol. Scand. 132:29-34; 1988.
162. Stoneham, M. D.; Everitt, B. J.; Hansen, S.; Lightman, S. L.;
Todd, K. Oxytocin and sexual behavior in the male rat and rabbit.
J. Endocrinol. 107:97-106; 1985.
163. Summerlee, A. J. S.; Parry, L. J. Stimulus secretion coupling in
the oxytocin system. In: Ganten, D.; Pfaff, D., eds. Current topics

143

164.
165.
166.
167.

168.
169.

170.
171.

172.
173.
174.
175.
176.

177.
178.

179.
180.

181.

182.
183.
184.
185.

in neuroendocrinology, vol. 9. Berlin: Springer-Verlag; 1,9.88:

29-72.
Swanson, L. W.; Sawchenko, P. E. Hypothalamic integration: organization of the paraventricular and supraoptic nuclei. Annu. Rev.
Neurosci. 6:269-324; 1983.
Theodosis, D. T. Oxytocin-immunoreactive terminals synapse on
oxytocin neurones in the supraoptic nucleus. Nature 313:682-684;
1985.
Theodosis, D. T.; Poulain, D. A. Oxytocin-secreting neurones: a
physiological model for structural plasticity in the adult mammalian brain. Trends Neurosci. 10:476--450; 1987.
Theodosis, D. T.; Pant, L.; Tappaz, M. L. Immunocytochemical
analysis of the GABAergic innervation of oxytocin- and vasopressin-secreting neurons in the rat supraoptic nucleus. Neuroscience 19:207-222; 1986.
Theodosis, D. T.; Poulain, D. A.; Vincent, J.-D. Possible morphological bases for synchronization of neuronal firing in the rat
supraoptic nucleus during lactation. Neuroscience 6:919-929; 1981.
Theodosis, D. T.; Montagnese, C.; Rodriguez, F.; Vincent, J.-D.;
Poulaln, D. A. Oxytocin induces morphological plasticity in the
adult hypothalamo-neurohypophysial system. Nature 322:738-740;
1986.
Todd, K.; Lightman, S. L. Oxytocin release during coitus in male
and female rabbits: Effect of opiate receptor blockade with naloxone. Psychoneuroendocrinology 11:367-371; 1986.
Tribollet, E.; Barberis, C.; Jard, S.; Dubois-Dauphin, M.; Dreiffus, J. J. Localization and pharmacological characterization of high
affinity binding sites for vasopressin and oxytocin in the rat brain
by light microscopic autoradiography. Brain Res. 442:105-118;
1988.
Tweedle, C. D.; Hatton, G. I. Magnocellular neuropeptidergic terminals in neurohypophysis: rapid glial release of enclosed axons
during parturition. Brain Res. Bull. 8:205-209; 1982.
Tweedle, C. D.; Modney, B. K.; Hatton, G. I. Ultrastructural
changes in the rat neurohypophysis following castration and testosterone replacement. Brain Res. Bull. 20:33-38; 1988.
Vance, E. B.; Wagner, N. N. Written descriptions of orgasms: a
study of sex differences. Arch. Sex. Behav. 5:87-98; 1976.
Wakerley, J. B.; Clarke, G.; Summerlee, A. J. S. Milk ejection
and its control. In: Knobil, E.; Neill, J. et al., eds. The physiology of reproduction. New York: Raven Press; 1988:2283-2321.
Wakerley, J. B.; Foreman, C. T.; Ingram, C. D. Effect of centrally administered oxytocin on the association between cortical
electroencephalogram and milk ejection in the rat. J. Neuroendocrinol. 1:173-178; 1989.
Wallen, K. Desire and ability: Hormones and the regulation of female sexual behavior. Neurosci. Biobehav. Rev. 14:233-241; 1990.
Warner, R. K.; Bazzett, T. J.; Markowski, V. P.; Lumley, L.;
Hull, E. M. Apomorphine in the basolateral amygdala affects copulation of male rats. Conf. Reprod. Behav. Abstr., Atlanta, GA;
1990:115.
Wathes, D. C.; Swann, R. W.; Porter, D. G.; Picketing, B. T.
Oxytocin as an ovarian hormone. In: Ganten, D.; Pfaff, D., eds.
Neurobiology of oxytocin. Berlin: Springer-Verlag; 1986:129-152.
Wiesner, J. B.; Moss, R. L. A psychopharmacological characterization of the opioid suppression of sexual behaviour in the female
rat. In: Dyer, R. G.; Bicknell, R. J., eds. Brain opioid systems in
reproduction. Oxford: Oxford University Press; 1989:187-202.
Wilhelmi, A. E.; Pickford, G. E.; Sawyer, W. H. Initiation of the
spawning reflex response in Fundulus by the administration of fish
and mammalian neurohypophyseal preparations and synthetic oxytocin. Endocrinology 57:243-254; 1955.
Williams, J. R.; Carter, C. S. Pair bond formation in prairie voles:
Behavioral hormonal and neural contributions. Conf. Reprod. Behav.
Abstr., Monterey, CA; 1991:14.
Winslow, J.; lnsel, T. R. Social status in pairs of male squirrel
monkeys determines the behavioral response to central oxytocin
administration. J. Neurosci. 11:2032-2038; 1991.
Witt, D. M.; Insel, T. R. Interactions of gonadal steroids and oxytocin: effects on sexual and social behavior in rats. Conf. Reprod.
Behav. Abstr., Atlanta, GA; 1990:120.
Witt, D. M.; Insel, T. R. A selective oxytocin antagonist attenuates progesterone facilitation of female sexual behavior. Endocri-

1~

nology 128:3269-3276, 1991.

186. Witt, D. M.; Carter, C. S.; Insel, T. R. Oxytocin receptor binding
in female prairie voles: effects of endogenous and exogenous estradiol stimulation. J. Neuroendocrinol. 3:155-161; 1991.
187. Witt, D. M.; Carter, C. S.; Walton, D. M. Central and peripheral
effects of oxytocin administration in prairie voles (Microtus ochrogaster). Pharmacol. Biochem. Behav. 37:63-69; 1990.
188. Witt, D. M.; Carter, C. S.; Carlstead, L.; Read, L. D. Sexual and
social interactions preceding and during male-induced oestrus in
prairie voles (Microtus ochrogaster). Anita. Behav. 36:1465-1471;
1988.
189. Yang, Q. Z.; Hatton, G. I. Dye coupling among supraoptic nu-

CARTER

cleus neurons without dendritic damage: differential incidence in

nursing mother and virgin rats. Brain Res. Bull. 19:559-565; 1987.
190. Yang, Q. Z.; Hatton, G. I. Dye coupling incidence among supraoptic nucleus (SON) is increased by lateral olfactory tract (LOT)
stimulation in slices from lactating but not virgin or male rats. Soc.
Neurosci. Abstr. 13:1593; 1987.
191. Yang, Q. Z.; Hatton, G. I. Direct evidence for electrical coupling
among rat supraoptic nucleus neurons. Brain Res. 463:47-56;
1988.
192. Yashpal, K.; Gauthier, S.; Henry, J. L. Oxytocin administered intrathecally preferentially increases heart rate rather than arterial
pressure in the rat. J. Autonom. Nerv. S~,,st. 20:167-178; 1987.