Monogamous Behavior in Males

1. prarie vole pine vole california mouse common marmoset montane vole meadow vole white-footed mouse rhesus monkey Monogamous Behavior socially monogamous forms partner preference highly affiliative bi-parental Non-Monogamous Behavior socially promiscuous forms no partner preference asocial non-paternal Monogamous Behavior in Males HORMONAL, GENETIC, and NEURAL mechanisms

2. Exp. Animal Stranger Partner Exp. Animal Stranger Affiliative Behavior test Partner Preference test

3. Partner Exp. Animal Stranger Partner preference formation in Prarie Voles HORMONES • in males: • communication • sexual behavior • aggression • pair bonding Role for Vasopressin (AVP)? In voles (and humans) mating stimulates AVP release

4. Exp. Animal Stranger Affiliative Behavior prarie vole montane vole young et al, nature 1999

5. V1a receptor expression prarie vole Ventral Pallidum has higer V1a expression montane vole Lim et al, Nature 2004

6. V1a receptor gene GENETICS --V1a receptor protein 99% homologous between vole species --binding kinetics (affinity between hormone and receptor) identical --expression level differences? Young and Wang, Nature Neuroscience 2004

7. Inject viral vector into specific brain areas vector contains lac Z gene (marker) V1a receptor gene Areas: ventral pallidum other areas mate meadow vole measure partner preference Partner Exp. Animal Stranger Meadow Vole: role of V1a time with partner time with stranger Control injection into VP V1a Injection into ventral pallidum V1a Injection into other brain areas partner preference behavior

8. Inject prarie vole V1a gene into mouse embryo measure change in affiliative behavior after AVP injection as an adult Exp. Animal Stranger Transgenics in non-monogamous mice

9. prarie vole pine vole california mouse common marmoset montane vole meadow vole white-footed mouse rhesus monkey Non-Monogamous Behavior socially promiscuous forms no partner preference non-paternal Monogamous Behavior socially monogamous forms partner preference bi-parental Monogamous Behavior in Males HORMONAL, GENETIC, and NEURAL mechanisms HIGHER V1a expression LOWER V1a expression

10. Ventral Pallidum NEURAL • Part of the reward/reinforcement pathway • in lab rats: • cocaine use activates neurons in ventral pallidum • infuse psychostimulants directly into ventral pallidum • subjects develop ‘conditioned place preference’ for environment where injections occurred • Hypothesis in voles: • V1a in ventral pallidum: activation of this pathway during mating enhances choice of partner later • lack of V1a in non-monogamous voles results in no induction of reward pathway, no preference for partner later

11. Summary HORMONAL • Vasopressin (AVP) is involved in partner preference and affiliative behavior in monogamous voles • Differences in these behaviors between monogamous and non-monogamous species lies in the V1a receptor GENETIC • monogamous voles have a different promoter that increases receptor expression in the ventral pallidum • induction of V1a receptor expression in non-monogamous species induces monogamous-like behaior NEURAL • Ventral Pallidum appears to enhance partner preference because it activates the ‘reward pathway’ during mating

12. V1a viral vector insertion into Prarie vole ventral pallidum increases affiliative behavior without the need for mating first. insertion into caudate putamen doesn’t have this effect # of receptors present associated behavioral response

13. cerebrospinal fluid (vehicle) V1a receptor antagonist oxytocin receptor antagonist cerebrospinal fluid AVP oxytocin prarie vole with V1a receptor antagonist before mating with female after mating with female Winslow et al Nature 1993