Differences in affiliative behavior, pair bonding, and vaginal cytology in two species of vole (Microtus ochrogaster and M. montanus).

Prairie voles (Microtus ochrogaster) and montane voles (M. montanus) display marked differences in social organization in the field. Trios of 1 male and 2 females were studied in a large enclosure for a 10-day period. Prairie voles spent 59% of the observation time in side-by-side contact, whereas montane voles spent only 7% of the time in contact. Vaginal smears indicated female–female suppression of estrus in prairie voles; female montane voles appeared to cycle in the presence of males. Male prairie voles preferentially paired and nested with 1 of the females, and vaginal estrus generally followed pair formation by 2 days. Male montane voles did not spend time preferentially with either female, even after mating. These results suggest that the contrasting mating systems of these species result from differences in the propensity for affiliative behavior and social bonding rather than from mate availability or female receptivity. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Male preferences for unmated versus mated females in two species of voles (Micotus ochrogaster and M. montanus).

Examined male preference for unmated vs mated females in 2 species of voles, using 73 prairie voles and 78 montane voles in 2 testing situations each. In Exp I, conducted in a tether test situation, prairie voles spent significantly more time and copulated more with unmated than with mated females. In Exp II, male prairie voles spent significantly more time visiting and investigating anesthetized unmated females than anesthetized mated females. In Exp III, male montane voles showed no significant visitation or copulatory preference for unmated vs mated females in the tether situation. In Exp IV, male montane voles spent more time with unmated, anesthetized females than mated females but displayed no other significant differences. In general, male prairie voles appeared more discriminating in their mate choice than male montane voles. These differences are consistent with differences in male parental effort in the field. (29 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Estrus induction in four species of voles (Microtus).

Male-induced estrus was examined in montane (Microtus montanus), meadow (M. pennsylvanicus), prairie (M. ochrogaster), and pine (M. pinetorum) voles. Duration of male contact needed for receptivity, effects of parity, and vaginal cytology were assessed. Among nulliparous females, montane voles attained receptivity with less male contact than prairie voles. Meadow and pine voles showed very low receptivity rates. Among parous females, montane and meadow voles did not differ in duration of male contact needed for receptivity and required less than prairie voles. Overall, parous females had higher receptivity rates than nulliparous females. When isolated from males, prairie and pine voles had more leukocytes and fewer cornified cells in vaginal smears than montane or meadow voles. Species differences in estrus induction are discussed in relation to species differences in social organization. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Copulatory behavior of voles (Microtus montanus and M. ochrogaster) in multiple-female test situations.

12 male prairie voles and 12 male mountain voles were given test of copulatory behavior with 1, 2, or 4 mating partners. Changes in the number of available partners produced minimal changes in the parameters of copulatory behavior in males of the 2 species. Male montane voles generally copulated with more of the females, showed a lesser tendency to concentrate copulations on a single female, and changed females more often than did prairie voles. These differences are consistent with differences in social structure reported in field studies and may reflect processes underlying species differences in social organization. (33 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Species differences in vasopressin receptor binding are evident early in development: comparative anatomic studies in prairie and montane voles

Monogamous prairie voles (Microtus ochrogaster) and promiscuous montane voles (Microtus montanus) exhibit remarkable differences in the distribution of vasopressin (AVP) receptors in the adult brain. This difference in receptor distribution is associated with species differences in the behaviors, including pair bond formation and paternal care, found selectively in the monogamous vole. To investigate a potential mechanism for this species difference in AVP receptors, the present study examined the ontogeny of receptor binding in the two species to determine whether the adult maps arose from a shared pattern in development. By using 125I-linear-AVP, which is a selective high-affinity ligand for the V1a receptor, we found early appearance and transient expression of AVP receptor binding during postnatal development in both species. However, the ontogenetic patterns of regional AVP receptor binding were species specific. In the diagonal band, the bed nucleus of the stria terminalis, and the central nucleus of the amygdala, prairie voles had higher AVP receptor binding at birth than montane voles, and this difference persisted with little variation into adulthood. In these areas, therefore, species differences in AVP receptor binding appeared to be determined primarily by genetic or prenatal factors. In the lateral septum, both species had low levels of AVP receptor binding at birth. Thereafter, the binding increased rapidly in montane voles, but it remained unchanged in prairie voles. In the cingulate cortex, AVP receptor binding in prairie voles showed a peak in early development with a subsequent decline and reached the adult level at weaning, whereas the binding in montane voles remained unchanged into adulthood. A similar but opposite pattern was found in the frontoparietal cortex, in which AVP receptor binding showed an early peak in montane voles but did not change significantly in prairie voles. These results demonstrate that 1) species differences in regional AVP receptor binding are evident in the early postnatal period and, in several areas, may be determined by genetic or prenatal factors, and 2) AVP may target brain areas differently in infant and adult prairie and montane voles and, thus, could exert differential effects on the organization of the central nervous system in the two species of voles.     

Facilitative and inhibitory influences of reproductive behavior on sperm transport in rats.

Six experiments investigated the effects of the rat's copulatory behavior on sperm transport in the female's reproductive tract. Data from 236 female and 87 male rats show that (a) transcervical sperm transport in rats required 6–20 min after ejaculation for completion; (b) transcervical transport of large numbers of sperm required that the vaginal plug remain lodged tightly in the vaginal-cervical junction; (c) maintenance of an immobile posture by the male, and possibly by the female, at ejaculation facilitated the deposition of a tightly lodged vaginal plug and the transport of large numbers of sperm through the cervix; (d) a single intromission occurring within 2 min after ejaculation disrupted sperm transport, but more copulatory stimulation was required to disrupt sperm transport when delivered between 4 and 10 min after ejaculation; and (e) the average postejaculatory interval was long enough to prevent a male from disrupting the transport of most of his own sperm from the preceding ejaculation. (21 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Three experiments on mate choice in meadow voles (Microtus pennsylvanicus).

Species differences in selectivity with respect to mate choice have been hypothesized to be related to mating systems. Procedures used in 3 previous experiments on monogamous prairie voles (Microtus ochrogaster) and polygamous montane voles (M. montanus) were used with polygamous meadow voles (M. pennsylvanicus). The expectation was that meadow voles would show few preferences. Female meadow voles preferred mating with familiar versus unfamiliar males but displayed no preference for unmated versus mated males. Male meadow voles displayed no preference for unmated versus mated females. The results are partially consistent with the hypothesis that relates mate choice to social and mating system, as this polygamous species resembles polygamous montane voles species in 2 situations but is similar to monogamous prairie voles in the 3rd. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Postpartum sexual behavior of the corn mouse (Calomys musculinus): Repertoire, measurements, and effects of removal of pups.

The patterns of sexual behavior of the South American cricetid Calomys musculinus, the corn mouse, were observed in 36 pairs of laboratory-reared mice during the postpartum estrus. Copulatory behavior was displayed by 26 of these pairs, 15 of which were observed with their litter in the arena. The other 11 pairs had their litters removed immediately after parturition. The behavioral elements were classified in 21 mutually exclusive categories. Seven categories were noninteractive (the animals performed them by themselves). Agonistic behaviors were predominant in male–female encounters in this species, accounting for 6 of the interactive categories. A kind of fighting, probably a ritualized one, usually precedes copulation. Removal of the litter decreases the incidence of aggression by females and increases the incidence of other interactive behaviors by males (e.g., grooming or sniffing the female, especially the genitals). The incidence of precopulatory fighting is not modified by the presence or absence of the litter, however. The copulatory behavior of this species has a general pattern of no lock, intravaginal thrusting, a single intromission per ejaculation, and multiple ejaculations. Copulation started after a short latency. Most pairs performed only two ejaculatory series. The ejaculation latency was shorter than those of other South American species. When compared with other cricetids displaying intravaginal thrusting, the corn mouse performs a high number of thrusts in the intromission with ejaculation. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Postejaculatory quiescence in female and male rats: Consequences for sperm transport during group mating.

Studied the pattern of postejaculatory mating in the social context of a multimale–multifemale group of Sprague-Dawley rats (N?=?21), analyzing its timing and sequence from the females' as well as the males' perspective. During mating, females had a quiescent period following each ejaculation, which was comparable with the males' (a postejaculatory interval, PEI). The PEIs of both sexes were characterized by 3 behaviorally distinguishable phases: a stationary, an interactive, and a sexual phase. There was no significant sex difference in the total length of the PEI. Nonetheless, females began active sexual behavior and entered the sexual phase more quickly than males. The time course of each phase of the PEI is compared with the time course of sperm transport in the female, and the similarities and differences between the two sexes' reproductive strategies following an ejaculation are emphasized. (45 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Female regulation and choice in the copulatory behavior of montane voles (Microtus montanus).

To study female choice of mating partners in montane voles, a male was tethered at each end of an elongate chamber, and an estrous female was allowed to move betweeen the 2 males and a neutral area. In Exp I, using 16 females and 32 males, females with a choice of 2 gonadally intact males copulated preferentially with 1 of them. Preferred males were more effective than nonpreferred males at gaining intromission and had more thrusts per intromission. In Exp II, with 10 females, 10 castrated males, and 10 sham-operated males, females spent more time with and mated preferentially with intact rather than castrated males. It is therefore suggested that the opportunity to copulate is reinforcing for female voles and that they display distinct preferences, correlated with copulatory stimulation, for some partners. (35 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Relation of Fos-IR expression in the pelvic ganglion to sexual behavior in laboratory rats.

The pelvic ganglion (PG) provides both sympathetic and parasympathetic innervation to the genitalia and other pelvic structures. To determine whether neuronal activity of the PG, as detected by Fos-like immunoreactivity (Fos-IR), is related to sexual stimulation, male and female rats were tested under a variety of conditions. In males, Fos-IR expression in the PG was positively correlated with the amount of both genital and noncontact stimulation. In females, only ejaculation preceded by multiple intromissions induced a significant increase in Fos-IR; multiple intromissions or ejaculation preceded by only 0–1 intromission did not affect Fos-IR. Additional experiments comparing Fos-IR expression, in which some females were allowed to pace their sexual contact and others were not, revealed that ejaculation duration was the key factor in the induction of Fos-IR in female rats. Because the conditions under which Fos-IR expression occurred in females are identical to those required for sperm transport, we suggest that, in the female, sperm transport is regulated in part by autonomic outflow from the PG after copulation. These relations between sexual behavior and measures of PG activity are consistent with the idea that the sexually dimorphic organization of the peripheral nervous system plays a major role in mediating the gender-specific outcome of copulation: ejaculation in the male and sperm transport in the female. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

A gender-specific mechanism for pair bonding: Oxytocin and partner preference formation in monogamous voles.

Previous studies have demonstrated that central administration of vasopressin but not oxytocin facilitates pair bonding in the monogamous male prairie vole. This study tested vasopressin and oxytocin in the formation of the female vole's preference for a particular male partner. Initial studies showed that in monogamous female prairie voles (but not in nonmonogamous congeners), mating was followed by a partner preference that endured for at least 2 weeks. Nonmating prairie vole females developed a partner preference following oxytocin infusions, but not after vasopressin or cerebrospinal fluid infusions. Females given a selective oxytocin antagonist showed normal mating behavior, yet failed to develop a partner preference. The vasopressin antagonist failed to block partner preference formation in mated females. These results suggest that oxytocin, released with mating, may be critical to formation of a partner preference in the female prairie vole; this contrasts to vasopressin, which appears to be more important for pair bonding in the male of this species. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Activation of the immune–endocrine system with lipopolysaccharide reduces affiliative behaviors in voles.

In Experiment 1, individually housed male meadow voles (Microtus pennsylvanicus) and prairie voles (Microtus ochrogaster) were injected with lipopolysaccharide (LPS) and exhibited the expected decrease in testosterone and increase in corticosterone and interleukin- 1β concentrations 3 hr later, indicating activation of the endocrine and immune systems. In Experiment 2, LPS- and saline-injected males were tethered in a 3-chamber partner preference apparatus. The time females spent in each chamber with a male, as well as the amount of time spent in social contact, was monitored. Female prairie voles, but not meadow voles, spent more time in the chamber with saline- than with LPS-injected males. LPS-injected male prairie and meadow voles engaged in less social contact with female conspecifics than did saline-injected males. These data suggest that LPS modifies physiology and behavior in male voles and that females may use these changes to discriminate healthy from potentially infected males. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Species differences in the vasopressin-immunoreactive pathways in the bed nucleus of the stria terminalis and medial amygdaloid nucleus in prairie voles (Microtus ochrogaster) and meadow voles (Microtus pennsylvanicus).

Vasopressin-immunoreactive (AVP-ir) cells in the bed nucleus of the stria terminalis (BST) and medial amygdaloid nucleus (MAN) and their AVP-ir projections to the lateral septum were studied in monogamous prairie voles (Microtus ochrogaster) and promiscuous meadow voles (M. pennsylvanicus). A sexually dimorphic AVP-ir pathway was found in both species; males had more AVP-ir cells in the BST and MAN, as well as denser AVP-ir fibers in the lateral septum, than did females. A significant species difference was also found. Overall, meadow voles had more AVP-ir cells in the BST and MAN than did prairie voles. Male prairie voles, however, had a higher density of AVP-ir fibers in the lateral septum than male meadow voles. The species difference in the sexually dimorphic AVP-ir projections in the BST and MAN is implicated in the rodents' different life strategy and behavior. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Developmental exposure to oxytocin facilitates partner preferences in male prairie voles (Microtus ochrogaster).

The authors investigated the effects of postnatal manipulations of oxytocin (OT) on the subsequent tendency to form a partner preference in male prairie voles (Microtus ochrogaster). Neonatally, males received either an injection of OT, an oxytocin antagonist (OTA), 0.9% saline vehicle, or handling without injection. As adults, males were tested for partner preference following 1 hr of cohabitation with a nonestrous female. In a 3-hr preference test, males neonatally exposed to exogenous OT exhibited a significant partner preference, not seen in males receiving OTA or saline. Both OT and OTA voles had significantly higher levels of social contact than saline controls. A single neonatal injection of OT increased both total and selective social behaviors in male prairie voles. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Central vasopressin V1a receptor activation is independently necessary for both partner preference formation and expression in socially monogamous male prairie voles.

The neuropeptide arginine vasopressin (AVP) modulates a variety of species-specific social behaviors. In socially monogamous male prairie voles, AVP acts centrally via vasopressin V1a receptor (V1aR) to facilitate mating induced partner preferences. The display of a partner preference requires at least 2 temporally distinct processes: social bond formation as well as its recall, or expression. Studies to date have not determined in which of these processes V1aR acts to promote partner preferences. Here, male prairie voles were administered intracerebroventricularly a V1aR antagonist (AVPA) at different time points to investigate the role of V1aR in social bond formation and expression. Animals receiving AVPA prior to cohabitation with mating or immediately prior to partner preference testing failed to display a partner preference, while animals receiving AVPA immediately after cohabitation with mating and control animals receiving vehicle at all 3 time points displayed partner preferences. These results suggest that V1aR signaling is necessary for both the formation and expression of partner preferences and that these processes are dissociable. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Vasopressin in the lateral septum regulates pair bond formation in male prairie voles (Microtus ochrogaster).

Male prairie voles (Microtus ochrogaster) form a pair bond with a female partner after mating, and this behavior is regulated by the neuropeptide vasopressin (AVP). The authors report that AVP in the lateral septum is important for pair bond formation. Administration of an AVP receptor antagonist in the lateral septum blocked mating-induced pair bonding, whereas administration of AVP induced this behavior in the absence of mating. In addition, administration of an oxytocin (OT) receptor antagonist in the lateral septum also blocked pair bond formation induced by either mating or AVP administration, suggesting that the OT receptor blockade may have interfered with the AVP regulation of behavior. Together, these data provide evidence suggesting that AVP in the lateral septum regulates pair bond formation in male prairie voles and that this process requires access to both AVP and OT receptors. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Sexual Dimorphism and the NMDA Receptor in Alloparental Behavior in Juvenile Prairie Voles (Microtus ochrogaster).

The prairie vole (Microtus ochrogaster) exhibits parental behavior in both males and females and extensive alloparenting in juveniles. The authors studied the effects on juvenile alloparenting of antagonists for the PCP, glycine, and glutamate sites on the N-methyl-D-aspartate (NMDA) receptor. In male voles, all 3 drugs had an inverted-U dose-response curve. This change could not be attributed to fear of the pup or a nonspecific impairment of cognition, level of locomotor activity, or motor coordination. The PCP site antagonist had a U-shaped dose-response curve in females, the opposite of that in males, but neither of the other drugs changed female alloparental behavior. Both male and female voles exhibit alloparental behavior, but its neurobiological underpinnings are sexually dimorphic in juveniles. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Role of prolonged copulatory behavior in facilitating reproductive success in a competitive mating situation in laboratory rats.

Results of 3 experiments (with 50 female F344/MA, 19 male F344, 12 male Long-Evans, 9 male BN/MA, and 9 male MAXX/MA rats) lend support to the hypothesis that the multiple ejaculatory pattern of male rats is of functional significance in that it increases the proportion of offspring sired by a given male when his female partner subsequently mates with a 2nd male, thus establishing conditions for sperm competition. When each male attained just 1 ejaculatory series, there was little effect of mating order (Exp I). Exp II revealed that when the 1st male completed 5 ejaculatory series, he sired a significantly higher porportion of the offspring relative to a 2nd male than when the 1st male attained just 1 ejaculation. The mechanism underlying the advantage of multiple ejaculations appears to lie in the proportion of sperm from each male in the female's tract rather than in either the mere passage of time or the effects of stimulation per se (Exp III). The multiple ejaculation pattern with a single female can be seen not as "wasted activity" but rather as functional in maximizing the reproductive success of individual males. (44 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Sexual activity and satiety over an extended observation period in prairie voles (Microtus ochrogaster).

This study was designed to delineate the course of sexual satiation in prairie voles (Microtus ochrogaster). Fourteen male–female pairs were allowed to copulate freely for 24 hr under continuous observation. Copulations occurred predominantly during the first few hours and decreased in frequency thereafter. The mean number of ejaculations per pair was 5.6 (range, 2–9). Two thirds of the ejaculations occurred during the first 3 hr, and over 90% took place within the first 7 hr after the first intromission. No ejaculations were observed during the last 8 hr. These results suggest that male capacity to deliver ejaculations to a female is limited and that direct observations reveal a more limited capacity than observations made with time-lapse videotape. (PsycINFO Database Record (c) 2010 APA, all rights reserved)