Oxytocin has dose-dependent developmental effects on pair-bonding and alloparental care in female prairie voles

Abstract

The present study examines the developmental consequences of neonatal exposure to oxytocin on adult social behaviors in female prairie voles (Microtus ochrogaster). Female neonates were injected within 24 hours of birth with isotonic saline or one of four dosages of oxytocin (OT). As adults, females were tested in an elevated plus-maze paradigm (a measure of anxiety and exploratory behavior), and for alloparental behavior and partner preferences. At 2 mg/kg OT, females took longer to approach pups, but were the only group to form a statistically significant within-group partner preference. At 4 mg/kg OT, females retrieved pups significantly more frequently but no longer displayed a partner preference; while females treated developmentally with 8 mg/kg spent significantly more time in side-to-side contact with a male stranger than any other treatment group. OT may have broad developmental consequences, but these effects are not linear and may both increase and decrease the propensity to display behaviors such as pair-bonding.The neuropeptide oxytocin (OT) has been implicated in social behavior in both male and female mammals. OT's peripheral effects include the induction of parturition and milk let-down, while central OT has been associated with the onset of maternal behavior (Pedersen and Prange Jr., 1979;Pedersen et al., 1982;Pedersen and Boccia, 2002), and other positive social behaviors such as pair-bonding (Insel and Hulihan, 1995;Carter and Altemus, 1997;Cho et al., 1999) and male parental care (Bales et al., 2004b). It is also becoming evident that manipulations of OT and a related peptide, arginine vasopressin (AVP) during the perinatal period of life can have life-long implications for social behavior and neuroendocrine function (Stribley and Carter, 1999;Diaz-Cabiale et al., 2000;Carter, 2003;Lipschitz et al., 2003). These exposures can be either endogenous, through responses to touch, warmth (Uvnas-Moberg, 1998) or perhaps through OT in breast milk (Leake et al., 1981); they could also be pharmacological, for example through use of pitocin or an oxytocin antagonist to manipulate labor (Husslein, 2002).In this context, we have begun to examine the consequences of OT manipulations in early life for subsequent social behaviors and neuroendocrine variables. Because we were particularly interested in the developmental control of social behaviors such as pair-bond formation and biparental behaviors, we chose to study the socially monogamous prairie vole (Microtus ochrogaster). In this species both males and females display parental care and form selective partner preferences indicative of pair-bonding, although the mechanisms for these behaviors Please direct correspondence to: Karen L. Bales, Dept. of Psychology, One Shields Ave., University of California, Davis, CA 95616. Ph: (530) 754−5890, Fax: (530) 752−2087, email: klbales@ucdavis.edu Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this e...

Oxytocin is associated with infant-care behavior and motivation in cooperatively breeding marmoset monkeys

“…Rather, OT may be involved in the motivational regulation of infant-care, which is also consistent with stimulating effects of exogenous OT-administration on maternal (Kendrick et al, 1987;Pedersen et al, 1994) and non-maternal (Bales et al, 2007;Madden and Clutton-Brock, 2011;Saito and Nakamura, 2011) care-taking in mammals.…”

“…Accordingly, experienced marmoset fathers could express normal paternal care even if prolactin was suppressed (Almond et al, 2006). In contrast, OT has been shown to stimulate alloparental infant-care motivation in different mammal species: In rodents, peripheral OT administration facilitated alloparental pup-retrieval, -licking, andgrooming in females (Bales et al, 2007), and OT-antagonist inhibited such behaviors in males (Bales et al, 2004). Peripheral OT administration also enhanced guarding, feeding, and association with pups in meerkats (Madden and Clutton-Brock, 2011), and intracerebroventricular OT administration facilitated paternal food sharing in marmosets (Saito and Nakamura, 2011).…”

“…We also compared the effects in early and late infancy, because frequencies and importance of the different infant-directed behaviors change over time. The facilitating effects of exogenous OT on paternal food transfer in marmosets (Saito and Nakamura, 2011) and alloparental behaviors in other mammals (Bales et al, 2007;Madden and Clutton-Brock, 2011) suggest that OT may be positively associated with intrinsic care-taking motivation. We therefor expected urinary OT A C C E P T E D M A N U S C R I P T ACCEPTED MANUSCRIPT 9 levels to be positively linked in particular to those care-taking behaviors that can be freely expressed by all individuals motivated to do so.…”

Developmental Perspectives on Oxytocin and Vasopressin

“…A single postnatal injection of oxytocin in male prairie voles increased the probability of partner preference and reduced anxiety-like behavior in adulthood (Bales and Carter, 2003), and a neonatal dose of OXTR antagonist reduced alloparental behavior in adult male prairie voles, without affecting partner preference behavior (Bales et al, 2004). The same perinatal dose in females did not affect partner preference behavior in adulthood, although higher doses did affect partner preference behavior, but in a non-linear manner (Bales et al, 2007b;Carter et al, 2009). …”

Hormonal imprinting in the central nervous system: causes and consequences

“…A fenti megfi gyelések alapján valószínűnek látszik, hogy az újszülöttkori oxitocinimprinting nem marad hatás nélkül a későbbi agyi folyamatokra [59]. A vizsgálatok azt mutatják, hogy patkányokban az egyetlen újszülöttkori kezelés hatására négy hónapos állatokban az agyi biogénamin-szint jelentősen eltér a kontrollokétól.…”