The role of conditioning on heterosexual and homosexual partner preferences in rats (2012)

Genaro A. Coria-Avila, DVM, MSc, PhD^*

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Partner preferences are expressed by many social species, including humans. They are commonly observed as selective contacts with an individual, more time spent together, and directed courtship behavior that leads to selective copulation. This review discusses the effect of conditioning on the development of heterosexual and homosexual partner preferences in rodents. Learned preferences may develop when a conditioned stimulus (CS) is associated in contingency with an unconditioned stimulus (UCS) that functions as a reinforcer. Consequently, an individual may display preference for a partner that bears a CS. Some UCS may be more or less reinforcing, depending on when they are experienced, and may be different for males and females. For example, it could be that, only during periods of early development, that stimuli associated with nurture and juvenile play become conditioned. In adulthood, other stimuli such as sexual reward, cohabitation, mild stress, or even pharmacological manipulations may function as reinforcers to condition partner preferences. Evolutionary biologists and psychologists must take into consideration the idea that an individual’s experience with reward (i.e. sexual and pharmacological) can override presumably ‘innate’ mate choices (e.g. assortativeness and orientation) or mate strategies (e.g. monogamy or polygamy) by means of Pavlovian and operant contingencies. In fact, it is likely as innate to learn about the environment in ways that maximize reward and minimize aversive outcomes, making so-called ‘proximate’ causes (e.g. pleasure) ultimately more powerful predictors of social behavior and choice than so-called ‘ultimate’ causes (e.g. genetic or reproductive fitness).

Early postnatal period

Certain stimuli that are sensed during early critical periods of life become associated through Pavlovian conditioning with innate rewards (e.g. maternal care, nutrient intake, etc.). This type of conditioning is termed ‘imprinting’ and can strongly affect sexual preferences in adulthood (Batenson, 1978). This conditioning occurs at young age when the brain is especially sensitive to make new associations. Imprinting usually occurs to the features of parents and species and is considered the first step in the phenomenon of assortative mating, in which animals choose to mate selectively with members of their own strain relative to members of a different strain or species that are genetically less similar. Assortative mating is believed to maintain homozygosity in a strain and, thereby, keep strains from outbreeding positive characteristics. In humans, assortative mating might occur when people display partner preference for phenotypic (e.g. racial, facial, etc.), social (e.g. cultural/religious beliefs), and personality characteristics (e.g. introversion/extroversion) that are somewhat similar to one’s own (Luo & Klohnen, 2005; Malina, Selby, Buschang, Aronson, & Little, 1983; Salces, Rebato, & Susanne, 2004), which would naturally result from the fact that people are more likely to interact harmoniously with others with similar attitudes/manerisms.

There is evidence indicating that males of different species can develop sexual imprinting for mates that bear cues associated with the female that nursed them or cues associated with the nursing period. In one study, for example, neonatal rats were nursed by their biological mother, which had a neutral odor (lemon) applied on her abdomen. At the appropriate time, the males were weaned and never exposed to the scent again, until about 100 days of age, when they were paired with scented or unscented unfamiliar females for copulation. The results indicated that males exposed in the early postnatal period to a lemon scent, displayed shorter ejaculation latency with lemon-scented females when they grew up, relative to the ejaculation latency observed when they were exposed to non-scented females (Fillion & Blass, 1986). That experiment was one of the first to demonstrate that neutral odors that are sensed during early periods can increase sexual excitement during future sexual encounters. In that case, a stronger sexual excitement was observed as shorter ejaculation latency with a receptive female bearing the odor.

Other experiments with imprinting in male rats have been more focused on partner preference and have demonstrated that this type of learned preference may depend on rewarding stimuli that the mother provides to the offspring during critical periods of life. For example, the positive effects of licking during the first 10 days of life can be conditioned to olfactory stimuli as well. In one study by Menard, Gelez, Coria-Avila, Jacubovich, and Pfaus (2006), newborn male pups were taken away from their mothers for 15 min every day. During this time away, males in a paired group were exposed to a lemon scent sprayed on the woodchip bedding of a different cage. At the same time, they received tactile stimulation performed artificially with a small paintbrush on their back and head, so that the strokes would mimic the dam’s licking at the time that they smelled the lemon scent. Males in a control group were exposed to woodchip bedding sprayed with water alone during tactile stimulation. Both groups were weaned at 21 days of age and never exposed to the odor again. After 2 months, males were placed in a large open field (123×123×46 cm chamber) and allowed to copulate freely with two females at the same time, one scented and one unscented. The results of that preference test indicated that a significant proportion of the paired males displayed a preference to ejaculate first with the scented female, whereas the control group showed no preference for scented females (Menard et al., 2006).

Other experiments have demonstrated that imprinting is so powerful that it can actually induce sexual preferences toward a different species. In one study, for example, male sheep and goats that were cross fostered developed a sexual partner preference toward females of the species of the foster mother (Kendrick, Hinton, Atkins, Haupt, & Skinner, 1998). Taken together, these studies indicate that stimuli sensed during early development can be learned and consequently direct partner preference during future sexual encounters.

Juvenile period

Although the period of maternal care is very critical for development, the postweaning period is also important because animals will experience their first non-fraternal social interactions through play behavior. In rats, this behavior involves repeated bouts of rough and tumble play and dorsal contacts directed to the nape of the opponent (Panksepp, Jalowiec, DeEskinazi, & Bishop, 1985). Social play has positive effects on the normal development of animals and is also believed to be rewarding. For example, one study showed that socially isolated juvenile rats allowed to engage in intense bouts of rough and tumble play during short, daily periods, did not turn timid and aggressive, compared to isolated animals not allowed to play (Einon, Humphreys, Chivers, Field, & Naylor, 1981). Furthermore, young animals develop place preference only for sides associated with the possibility to engage in play behavior (Calcagnetti & Schechter, 1992). The rewarding properties of social play (as well as other social experiences) are modulated by opioids, since treatment with opioid agonists such as morphine increases the intensity and frequency of the behavior (Panksepp et al., 1985), whereas an opioid antagonist like naloxone readily reduces its frequency.

Very recently, a study from our laboratory showed that female rats develop conditioned partner preference toward males that bear olfactory cues previously associated with juvenile play (Paredes-Ramos, Miquel, Manzo, & Coria-Avila, 2011). In that study, prepubescent female rats were socially isolated at 31 days old and were allowed to play daily for 30 min, during 10 trials, with another young female that bore an odor (either almond or lemon scent) as a CS. One day after the last conditioning trial, all the females were tested for conditioned play partner preference with two young and prepubescent male rats, one scented with almond and the other with lemon. The results indicated that females in the almond-paired group preferred the almond male as play partner, ignoring the lemon-scented male. However, in the lemon-paired group, females preferred the lemon-scented male. Some days later, when females were approximately 55 days old, they were ovariectomized, and hormone-primed with estradiol and progesterone to induce sexual receptivity. Then, they were tested for their first sexual partner preference with two unfamiliar stud males, one almond-scented and one lemon-scented. The results indicated that females displayed a very selective sexual partner preference toward males bearing an odor (either almond or lemon) previously paired with juvenile play. This was observed with more solicitations, hops and darts, visits, and olfactory investigations, directed toward the preferred male. Sexual solicitations (including hops and darts) indicate females sexual desire and function as an invitation for males to engage in sexual behavior with them (Pfaus, Shadiack, Van Soest, Tse, & Molinoff, 2004). Indeed, the females solicited more toward males bearing the conditioned stimulus, which resulted in more intromissions and ejaculations from them, including the very first ejaculation. This might have very important implications in gonadally intact females. For instance, we have previously demonstrated that the first ejaculation may result in 100% of fatherhood if the female does not receive any other intromission for at least 10 min after (Coria-Avila, Pfaus, Hernandez, Manzo, & Pacheco, 2004). Accordingly, conditioning of partner preference during the juvenile period may bias assortative mating.

Postpubertal period

The postpubertal period is more flexible in time than the early postnatal weeks and juvenile phase. It is a critical period because animals commonly experience their first sexually rewarding encounters. For example, in one study of male rats, the levels of luteinizing hormone and testosterone were increased following exposure to a conditioned odor (i.e. wintergreen) previously paired with copulation (Graham & Desjardins, 1980). The increases were similar to those following exposure to estrous odors in naïve males, suggesting that association with the copulatory reward state makes a neutral odor to become a CS capable of triggering a conditioned neuroendocrine response that prepares the animal for a sexual behavior.

Conditioned odors associated with copulation can also facilitate motivation for a partner. For example, Kippin, Talinakis, Chattmann, Bartholomew, and Pfaus (1998) trained one group of males (the paired group) to associate an almond or lemon odor painted on the back of a female’s neck and anogenital region with copulation to ejaculation. Another group (the unpaired group) received copulatory trials with unscented females (Kippin et al., 1998). On a final test in a laboratory open field, the males received access to two sexually receptive females, one scented with the odor and the other unscented. Males in the paired group displayed a conditioned partner preference in which the scented females were chosen to receive the males’ first ejaculation. Subsequent studies revealed that the learning of this conditioned ejaculatory preference took place during the postejaculatory refractory period (Kippin & Pfaus, 2001). Thus, polygamous male rats acquired a preferred partner by exposure to a simple Pavlovian conditioning procedure that linked a neutral olfactory stimulus to sexual reward induced by ejaculation.

Based on the fact that the postejaculatory period is sufficiently rewarding to support the development of heterosexual partner preference in male rats, we tested its effects on conditioned homosexual partner preference. In a study from our laboratory (Cibrian-Llanderal, Triana-Del Rio, Tecamachaltzi-Silvaran, & Coria-Avila, 2011), we allowed male rats to copulate to one ejaculation with sexually receptive female rats. Immediately after ejaculation, males were gently removed from the female’s arena and were placed into a different arena to cohabitate for 1 h with another male that bore almond scent as a CS. This occurred during 10 conditioning trials, just as in the study of Kippin and Pfaus (2001). In a control group, males were placed for cohabitation 12 h after copulating with the female. One day after the last conditioning trial, males were tested for homosexual partner preference in a chamber with two stud males as potential partners, one almond scented and one unscented. Contrary to our hypothesis, both groups failed to develop a conditioned homosexual preference for the CS+ male, indicating that the ‘critical period’ induced by ejaculation is sufficient to support heterosexual, but not homosexual conditioning of partner preference in putatively heterosexual males. Nevertheless, there were some interesting statistical trends (non-significant). For example, about 40% of the males in the experimental group displayed mount attempts toward scented males, compared to 20% of males in the control group. In addition, experimental males displayed higher frequency of play behaviors (dorsal contacts and rough-and-tumble events) toward scented males. This might indicate that exposure to a male during the postejaculatory period resulted in conditioned play partner preference but not in homosexual preference.

First sexual experiences

As discussed before, the sexual reward state induced by ejaculation is a critical UCS that facilitates a subsequent preference for stimuli that predict it. It has been hypothesized that conditioned ejaculatory preference in rats may be a rudiment of the monogamous behavior observed in other species of rodents (Pfaus et al., 2001). For example, mating facilitates pair-bonding in monogamous prairie voles (Williams, Catania, & Carter, 1992), suggesting that mating-induced pair bonds are mediated by sexual reward (Young & Wang, 2004). Pair bonds are observed when a vole has the choice of two partners, one familiar, with whom copulation occurred previously, and one novel. A bonded vole usually selects the familiar one to spend more time, copulate, and reproduce with. Some reports indicate that this behavior may last for life, since bonded individuals rarely mate with other partners even following permanent separation from the original partner (Getz, McGuire, Pizzuto, Hofmann, & Frase, 1993). It is possible that a bonded vole remains monogamous because of the constant positive reinforcement from the partner during social contact and recurrent mating. As a result, the specific features of the partner (e.g. olfactory signature) may become conditionally preferred and reinforced by social stimulation and mating.

Other stimuli that affect partner preference conditioning

Stress

There are arousing stimuli other than those experienced during copulation that can also facilitate the formation of partner preference. For example, in male prairie voles, long periods of swimming are believed to be stressful. If voles are forced to swim and then allowed to cohabit for a period of 6 h (which is normally not enough time to induce bonding), pair bonds are more likely to occur (Carter, 1998; DeVries, DeVries, Taymans, & Carter, 1996). This behavior is believed to be facilitated via the hormones that are released during the stress response (i.e. corticosteroids), because injections of corticosterone in males facilitate the formation of pair bonds (DeVries et al., 1996). The exact process is not completely understood; however, one possible explanation is based on the fact that corticosteroids induce an increase of activity in mesolimbic dopamine (DA) (Der-Avakian et al., 2006; Rouge-Pont, Marinelli, Le Moal, Simon, & Piazza, 1995), and DA mediates the development of partner preferences and pair bonds (Aragona, Liu, Curtis, Stephan, & Wang, 2003; Aragona et al., 2006; Wang, et al., 1999). There is evidence in humans about the effects of stress on the formation of new pair bonds. Some cases have been documented in the so-called Stockholm syndrome (Julich, 2005; Namnyak et al., 2008), in which a hostage develops empathy or a bond toward the captor. Thus, it is possible that, depending on its intensity and duration, a stress response may facilitate or disrupt the formation of partner preferences. However, the exact mechanisms that result in preference or aversion are not well understood (Fig. 1).

 

Fig. 1

Periods in which development of partner preference may occur. During the prenatal period, there is organization of brain circuitries (e.g. brain dimorphism) that facilitates motivation and preference for partners that bear strong UCS. This innate preference …

Pharmacological manipulations

Other peptides

In the monogamous voles, females express more OT receptors in areas related to recognition and sex, compared to polygamous females (e.g. in prelimbic cortex, bed nucleus of the stria terminalis, dorsomedial thalamus, lateral amygdala, and NAc; Insel, 1992). However, polygamous females express more OT receptors in other areas such as the lateral septum, ventromedial hypothalamus, and corticomedial amygdala (Young et al., 1997). Only a few of these differences appear to be relevant in the formation of partner preferences. For instance, OT antagonist in the prelimbic cortex or NAc can block the formation of new partner preferences in voles induced by sex or D2 agonists (Liu & Wang, 2003). With regard to AVP, monogamous male voles express higher density in the ventral pallidum, compared to polygamous males (Lim & Young, 2004). Infusions of AVP antagonist into the ventral pallidum disrupts the development of pair bonds induced by sex (Young & Wang, 2004). There is a study indicating that the increase of AVP receptors via viral vectors from a monogamous to a polygamous male vole can readily increase the capacity of the latter to form pair bonds (Lim et al., 2004).

Given the systematic interrelationship between DA and some peptides like OT and AVP, we tested the effect of a D2-type receptor agonist + OT on the development of homosexual partner preference in female rats. As discussed above, the effect of a D2 agonist alone (quinpirole) during cohabitation, facilitated conditioned homosexual preference between male rats but not between female rats. However, as we found later, treatment with quinpirole, followed 10 min later by OT, facilitated the development of homosexual preferences between females in just three trials (Cibrian-Llanderal et al., submitted). The preference was observed with more proceptive behaviors (i.e. solicitations and hops and darts) and more time spent together with the familiar female. The effect of quinpirole + OT indicates that female rats not only require D2-type receptor activity but also the effects of the peptide to crystallize a preference for a partner. In fact, that combination may be required to experience sexual reward during mating and may reflect the combination of these two neurochemicals during rewarding copulation in which female receive intromissions (Becker, Rudick, & Jenkins, 2001; Coria-Avila et al., 2005, 2006) (Table 1).

 

Table 1

Some unconditioned stimuli (UCS) that function as reinforcers and help condition partner preference in rodents. Some UCSs are explicitly sexual, but others are not. A partner that bears conditioned stimuli (CS) that predict the UCS will be preferred.? …

Other implications of learned partner preferences

The author would like to thank Dr. Jim Pfaus, and Dr. Larry J. Young for useful discussions and to his graduate students Tamara Cibrian-Llanderal, Pedro Paredes-Ramos, Rodrigo Triana-Del Rio, and Felix Montero-Dominguez for their hard work and commitment to their research projects.

1. Agmo A, Berenfeld R. Reinforcing properties of ejaculation in the male rat: role of opioids and dopamine. Behavioral Neuroscience. 1990;104(1):177–182. [PubMed]
2. Aragona B.J, Liu Y, Curtis J.T, Stephan F.K, Wang Z. A critical role for nucleus accumbens dopamine in partner-preference formation in male prairie voles. Journal of Neuroscience. 2003;23(8):3483–3490. [PubMed]
3. Aragona B.J, Liu Y, Yu Y.J, Curtis J.T, Detwiler J.M, Insel T.R, et al. Nucleus accumbens dopamine differentially mediates the formation and maintenance of monogamous pair bonds. Nature Neuroscience. 2006;9(1):133–139. [PubMed]
4. Bales K.L, van Westerhuyzen J.A, Lewis-Reese A.D, Grotte N.D, Lanter J.A, Carter C.S. Oxytocin has dose-dependent developmental effects on pair-bonding and alloparental care in female prairie voles. Hormones and Behavior. 2007;52(2):274–279. [PMC free article] [PubMed]
5. Balfour M.E, Yu L, Coolen L.M. Sexual behavior and sex-associated environmental cues activate the mesolimbic system in male rats. Neuropsychopharmacology. 2004;29(4):718–730. [PubMed]
6. Batenson P. Early experience and sexual preference. In: Hutchinson J.B, editor. Biological determinants of sexual behavior. Chichester: John Wiley & Sons; 1978. pp. 29–53.
7. Becker J.B, Rudick C.N, Jenkins W.J. The role of dopamine in the nucleus accumbens and striatum during sexual behavior in the female rat. Journal of Neuroscience. 2001;21(9):3236–3241. [PubMed]
8. Beery A.K, Zucker I. Oxytocin and same-sex social behavior in female meadow voles. Neuroscience. 2010;169(2):665–673. [PubMed]
9. Berridge K.C, Robinson T.E. What is the role of dopamine in reward: Hedonic impact, reward learning, or incentive salience? Brain Research. Brain Research Reviews. 1998;28(3):309–369. [PubMed]
10. Bielsky I.F, Young L.J. Oxytocin, vasopressin, and social recognition in mammals. Peptides. 2004;25(9):1565–1574. [PubMed]
11. Calcagnetti D.J, Schechter M.D. Place conditioning reveals the rewarding aspect of social interaction in juvenile rats. Physiology and Behavior. 1992;51(4):667–672. [PubMed]
12. Carmichael M.S, Humbert R, Dixen J, Palmisano G, Greenleaf W, Davidson J.M. Plasma oxytocin increases in the human sexual response. Journal of Clinical Endocrinology and Metabolism. 1987;64(1):27–31. [PubMed]
13. Carter C.S. Neuroendocrine perspectives on social attachment and love. Psychoneuroendocrinology. 1998;23(8):779–818. [PubMed]
14. Carter C.S, DeVries A.C, Getz L.L. Physiological substrates of mammalian monogamy: the prairie vole model. Neuroscience and Biobehavioral Reviews. 1995;19(2):303–314. [PubMed]
15. Carter C.S, Williams J.R, Witt D.M, Insel T.R. Oxytocin and social bonding. Annals of the New York of Academic Sciences. 1992;652:204–211. [PubMed]
16. Cibrian-Llanderal I.L, Rosas-Aguilar V, Triana-Del Rio R, Perez-Estudillo C.A, Manzo J, Garcia L.I, Coria-Avila GA. Development of same-sex partner preference in adult rats: Cohabitation during enhanced D2-type receptor and oxytocin activity; 2012. Submitted to: Pharmacology, Biochemistry & Behavior.
17. Cibrian-Llanderal I.T, Triana-Del Rio R, Tecamachaltzi-Silvaran M, Coria-Avila G.A. Conditioning homosexual behavior in male rats; 2011. Poster session presented at the Annual Meeting of the Society for Behavioral Neuroendocrinology, Queretaro, Mexico.
18. Coria-Avila G.A. Behavioral and neural mechanisms of conditioned partner preference in the female rat. Montreal, Quebec, Canada: Unpublished doctoral dissertation. Psychology Department, Concordia University; 2007.
19. Coria-Avila G.A, Pfaus J.G, Cibrian-Llanderal I.T, Tecamachaltzi-Silvaran M, Triana-Del Rio R, Montero-Domínguez F, et al. Cómo aprender a comportarse sexualmente. e-Neurobiologia. 2010;1(1)
20. Coria-Avila G.A, Gavrila A.M, Boulard B, Charron N, Stanley G, Pfaus J.G. Neurochemical basis of conditioned partner preference in the female rat: II. Disruption by flupenthixol. Behavioral Neuroscience. 2008a;122(2):396–406. [PubMed]
21. Coria-Avila G.A, Jones S.L, Solomon C.E, Gavrila A.M, Jordan G.J, Pfaus J.G. Conditioned partner preference in female rats for strain of male. Physiology and Behavior. 2006;88(4–5):529–537. [PubMed]
22. Coria-Avila G.A, Ouimet A.J, Pacheco P, Manzo J, Pfaus J.G. Olfactory conditioned partner preference in the female rat. Behavioral Neuroscience. 2005;119(3):716–725. [PubMed]
23. Coria-Avila G.A, Pfaus J.G, Hernandez M.E, Manzo J, Pacheco P. Timing between ejaculations changes paternity success. Physiology and Behavior. 2004;80(5):733–737. [PubMed]
24. Coria-Avila G.A, Solomon C.E, Vargas E.B, Lemme I, Ryan R, Menard S, et al. Neurochemical basis of conditioned partner preference in the female rat: I. Disruption by naloxone. Behavioral Neuroscience. 2008b;122(2):385–395. [PubMed]
25. Cushing B.S, Carter C.S. Peripheral pulses of oxytocin increase partner preferences in female, but not male, prairie voles. Hormones and Behavior. 2000;37(1):49–56. [PubMed]
26. Der-Avakian A, Bland S.T, Schmid M.J, Watkins L.R, Spencer R.L, Maier S.F. The role of glucocorticoids in the uncontrollable stress-induced potentiation of nucleus accumbens shell dopamine and conditioned place preference responses to morphine. Psychoneuroendocrinology. 2006;31(5):653–663. [PubMed]
27. DeVries A.C, DeVries M.B, Taymans S.E, Carter C.S. The effects of stress on social preferences are sexually dimorphic in prairie voles. Proceedings of the National Academy of Sciences of the United States of America. 1996;93(21):11980–11984. [PMC free article] [PubMed]
28. Einon D.F, Humphreys A.P, Chivers S.M, Field S, Naylor V. Isolation has permanent effects upon the behavior of the rat, but not the mouse, gerbil, or guinea pig. Developmental Psychobiology. 1981;14(4):343–355. [PubMed]
29. Fillion T.J, Blass E.M. Infantile experience with suckling odors determines adult sexual behavior in male rats. Science. 1986;231(4739):729–731. [PubMed]
30. Garcia-Horsman S.P, Agmo A, Paredes R.G. Infusions of naloxone into the medial preoptic area, ventromedial nucleus of the hypothalamus, and amygdala block conditioned place preference induced by paced mating behavior. Hormones and Behavior. 2008;54(5):709–716. [PubMed]
31. Getz L.L, McGuire B, Pizzuto T, Hofmann J, Frase B. Social organization of the prairie vole, Microtus ochrogaster . Journal of Mammal. 1993;74:44–58.
32. Gingrich B, Liu Y, Cascio C, Wang Z, Insel T.R. Dopamine D2 receptors in the nucleus accumbens are important for social attachment in female prairie voles (Microtus ochrogaster) Behavioral Neuroscience. 2000;114(1):173–183. [PubMed]
33. Graham J.M, Desjardins C. Classical conditioning: induction of luteinizing hormone and testosterone secretion in anticipation of sexual activity. Science. 1980;210(4473):1039–1041. [PubMed]
34. Insel T.R. Oxytocin – a neuropeptide for affiliation: evidence from behavioral, receptor autoradiographic, and comparative studies. Psychoneuroendocrinology. 1992;17(1):3–35. [PubMed]
35. Insel T.R, Shapiro L.E. Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles. Proceedings of the National Academy of Sciences of the United States of America. 1992;89(13):5981–5985. [PMC free article] [PubMed]
36. Insel T.R, Young L.J. The neurobiology of attachment. Nature Reviews. Neuroscience. 2001;2(2):129–136. [PubMed]
37. Ismail N, Gelez H, Lachapelle I, Pfaus J.G. Pacing conditions contribute to the conditioned ejaculatory preference for a familiar female in the male rat. Physiology and Behavior. 2009;96(2):201–208. [PubMed]
38. Jones S.L, Bozzini P, Pfaus J.G. Morphine potentiates the development of a conditioned ejaculatory preference in rats; Neuroscience Meeting Planner; Society for Neuroscience; 2009. Online.
39. Julich S. Stockholm syndrome and child sexual abuse. Journal of Child Sex Abuse. 2005;14(3):107–129. [PubMed]
40. Kendrick K.M, Hinton M.R, Atkins K, Haupt M.A, Skinner J.D. Mothers determine sexual preferences. Nature. 1998;395(6699):229–230. [PubMed]
41. Kippin T.E, Cain S.W, Pfaus J.G. Estrous odors and sexually conditioned neutral odors activate separate neural pathways in the male rat. Neuroscience. 2003;117(4):971–979. [PubMed]
42. Kippin T.E, Pfaus J.G. The development of olfactory conditioned ejaculatory preferences in the male rat. I. Nature of the unconditioned stimulus. Physiology and Behavior. 2001;73(4):457–469. [PubMed]
43. Kippin T.E, Talinakis E, Chattmann L, Bartholomew S, Pfaus J.G. Olfactory conditioning of sexual behavior in the male rat (Rattus norvegicus) Journal of Comparative Psychology. 1998;112(4):389–399.
44. Lim M.M, Wang Z, Olazabal D.E, Ren X, Terwilliger E.F, Young L.J. Enhanced partner preference in a promiscuous species by manipulating the expression of a single gene. Nature. 2004;429(6993):754–757. [PubMed]
45. Lim M.M, Young L.J. Vasopressin-dependent neural circuits underlying pair bond formation in the monogamous prairie vole. Neuroscience. 2004;125(1):35–45. [PubMed]
46. Liu Y, Aragona B.J, Young K.A, Dietz D.M, Kabbaj M, Mazei-Robison M, et al. Nucleus accumbens dopamine mediates amphetamine-induced impairment of social bonding in a monogamous rodent species. Proceedings of the National Academy of Sciences of the United States of America. 2010;107(3):1217–1222. [PMC free article] [PubMed]
47. Liu Y, Wang Z.X. Nucleus accumbens oxytocin and dopamine interact to regulate pair bond formation in female prairie voles. Neuroscience. 2003;121(3):537–544. [PubMed]
48. Luo S, Klohnen E.C. Assortative mating and marital quality in newlyweds: a couple-centered approach. Journal of Personality and Social Psychology. 2005;88(2):304–326. [PubMed]
49. Malina R.M, Selby H.A, Buschang P.H, Aronson W.L, Little B.B. Assortative mating for phenotypic characteristics in a Zapotec community in Oaxaca, Mexico. Journal of Biosocial Science. 1983;15(3):273–280. [PubMed]
50. Menard S, Gelez H, Coria-Avila G.A, Jacubovich M, Pfaus J.G. Impact of neonatal olfactory condit ioning on later sexual partner preference in the male rat; 2006. Poster session presented at the Annual Meeting of the Society for Behavioral Neuroendocrinology, Pittsburgh, PE.
51. Namnyak M, Tufton N, Szekely R, Toal M, Worboys S, Sampson E.L. Stockholm syndrome’: psychiatric diagnosis or urban myth? Acta Psychiatrica Scandinavica. 2008;117(1):4–11. [PubMed]
52. Panksepp J, Jalowiec J, DeEskinazi F.G, Bishop P. Opiates and play dominance in juvenile rats. Behavioral Neuroscience. 1985;99(3):441–453. [PubMed]
53. Parada M, Abdul-Ahad F, Censi S, Sparks L, Pfaus J.G. Context alters the ability of clitoral stimulation to induce a sexually-conditioned partner preference in the rat. Hormones and Behavior. 2011;59:520–527. [PubMed]
54. Paredes R.G, Alonso A. Sexual behavior regulated (paced) by the female induces conditioned place preference. Behavioral Neuroscience. 1997;111(1):123–128. [PubMed]
55. Paredes R.G, Martinez I. Naloxone blocks place preference conditioning after paced mating in female rats. Behavioral Neuroscience. 2001;115(6):1363–1367. [PubMed]
56. Paredes R.G, Vazquez B. What do female rats like about sex? Paced mating. Behavioural Brain Research. 1999;105(1):117–127. [PubMed]
57. Paredes-Ramos P, Miquel M, Manzo J, Coria-Avila G.A. Juvenile play conditions sexual partner preference in adult female rats. Physiology and Behavior. 2011;104:1016–1023. [PubMed]
58. Paredes-Ramos P, Miquel M, Manzo J, Pfaus J.G, López-Meraz M.L, Coria-Avila G.A. Tickling in Juvenile but not Adult Female Rats Conditions Sexual Partner Preference. 2012 Submitted to: Physiology & Behavior. [PubMed]
59. Pavlov I. Conditioned reflexes. Oxford: University Press; 1927.
60. Penn D, Potts W. MHC-disassortative mating preferences reversed by cross-fostering. Proceedings of Biological Science. 1998;265(1403):1299–1306. [PMC free article] [PubMed]
61. Pfaus J.G, Damsma G, Nomikos G.G, Wenkstern D.G, Blaha C.D, Phillips A.G, et al. Sexual behavior enhances central dopamine transmission in the male rat. Brain Research. 1990;530(2):345–348. [PubMed]
62. Pfaus J.G, Damsma G, Wenkstern D, Fibiger H.C. Sexual activity increases dopamine transmission in the nucleus accumbens and striatum of female rats. Brain Research. 1995;693(1–2):21–30. [PubMed]
63. Pfaus J.G, Kippin T.E, Centeno S. Conditioning and sexual behavior: A review. Hormones and Behavior. 2001;40(2):291–321. [PubMed]
64. Pfaus J.G, Shadiack A, Van Soest T, Tse M, Molinoff P. Selective facilitation of sexual solicitation in the female rat by a melanocortin receptor agonist. Proceedings of the National Academy of Sciences of the United States of America. 2004;101(27):10201–10204. [PMC free article] [PubMed]
65. Rouge-Pont F, Marinelli M, Le Moal M, Simon H, Piazza P.V. Stress-induced sensitization and glucocorticoids. II. Sensitization of the increase in extracellular dopamine induced by cocaine depends on stress-induced corticosterone secretion. Journal of Neuroscience. 1995;15(11):7189–7195. [PubMed]
66. Salces I, Rebato E, Susanne C. Evidence of phenotypic and social assortative mating for anthropometric and physiological traits in couples from the Basque country (Spain) Journal of Biosocial Science. 2004;36(2):235–250. [PubMed]
67. Schultz W. Getting formal with dopamine and reward. Neuron. 2002;36(2):241–263. [PubMed]
68. Schultz W, Apicella P, Scarnati E, Ljungberg T. Neuronal activity in monkey ventral striatum related to the expectation of reward. Journal of Neuroscience. 1992;12(12):4595–4610. [PubMed]
69. Skinner B.F. Some contributions of an experimental analysis of behavior to psychology as a whole. American Psychologists. 1953;8:69–78.
70. Skinner B.F. What is the experimental analysis of behavior? Journal of the Experimental Analysis of Behavior. 1966;9(3):213–218. [PMC free article] [PubMed]
71. Tauber M, Mantoulan C, Copet P, Jauregui J, Demeer G, Diene G, et al. Oxytocin may be useful to increase trust in others and decrease disruptive behaviours in patients with Prader-Willi syndrome: a randomised placebo-controlled trial in 24 patients. Orphanet Journal of Rare Diseases. 2011;6(1):47. [PMC free article] [PubMed]
72. Triana-Del Rio R, Montero-Dominguez F, Cibrian-Llanderal T, Tecamachaltzi-Silvaran M.B, Garcia L.I, Manzo J, et al. Same-sex cohabitation under the effects of quinpirole induces a conditioned socio-sexual partner preference in males, but not in female rats. Pharmacology Biochemistry and Behavior. 2011;99(4):604–613. [PubMed]
73. van Furth W.R, Wolterink G, van Ree J.M. Regulation of masculine sexual behavior: involvement of brain opioids and dopamine. Brain Research. Brain Research Reviews. 1995;21(2):162–184. [PubMed]
74. Wang Z, Hulihan T.J, Insel T.R. Sexual and social experience is associated with different patterns of behavior and neural activation in male prairie voles. Brain Research. 1997;767(2):321–332. [PubMed]
75. Wang Z, Yu G, Cascio C, Liu Y, Gingrich B, Insel T.R. Dopamine D2 receptor-mediated regulation of partner preferences in female prairie voles (Microtus ochrogaster): A mechanism for pair bonding? Behavioral Neuroscience. 1999;113(3):602–611. [PubMed]
76. Williams J.R, Catania K.C, Carter C.S. Development of partner preferences in female prairie voles (Microtus ochrogaster): The role of social and sexual experience. Hormones and Behavior. 1992;26(3):339–349. [PubMed]
77. Winslow J.T, Hastings N, Carter C.S, Harbaugh C.R, Insel T.R. A role for central vasopressin in pair bonding in monogamous prairie voles. Nature. 1993;365(6446):545–548. [PubMed]
78. Yamazaki K, Beauchamp G.K, Kupniewski D, Bard J, Thomas L, Boyse E.A. Familial imprinting determines H-2 selective mating preferences. Science. 1988;240(4857):1331–1332. [PubMed]
79. Young L.J, Wang Z. The neurobiology of pair bonding. Nature Neuroscience. 2004;7(10):1048–1054. [PubMed]
80. Young L.J, Winslow J.T, Wang Z, Gingrich B, Guo Q, Matzuk M.M, et al. Gene targeting approaches to neuroendocrinology: Oxytocin, maternal behavior, and affiliation. Hormones and Behavior. 1997;31(3):221–231. [PubMed]