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Monogamous Behavior in Males 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 HORMONAL, GENETIC, and NEURAL mechanisms

Monogamous Behavior in Males prarie vole pine vole california mouse common marmoset montane vole meadow vole white-footed mouse rhesus monkey Monogamous

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Monogamous Behavior in Males

• prarie vole• pine vole• california mouse• common marmoset

• montane vole• meadow vole• white-footed mouse• rhesus monkey

Monogamous Behaviorsocially monogamousforms partner preferencehighly affiliativebi-parental

Non-Monogamous Behaviorsocially promiscuousforms no partner preferenceasocialnon-paternal

HORMONAL, GENETIC, and NEURAL mechanisms

Affiliative Behavior test

Partner Preference test

StrangerExp. AnimalPartner

StrangerExp. Animal

Partner preference formation in Prarie Voles

StrangerExp. AnimalPartner

Role for Vasopressin (AVP)?

• in males:– communication– sexual behavior– aggression– pair bonding

HORMONES

In voles (and humans) mating stimulates AVP release

prarie vole

montane vole

young et al, nature 1999

StrangerExp. Animal

Affiliative Behavior

prarie vole

montane vole

Lim et al, Nature 2004

V1a receptor expression

Ventral Pallidum has higer V1a expression

Young and Wang, Nature Neuroscience 2004

V1a receptor gene--V1a receptor protein 99% homologous between vole species--binding kinetics (affinity between hormone and receptor) identical--expression level differences?

GENETICS

StrangerExp. AnimalPartner

partner preference behavior

Meadow Vole: role of V1a

• 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

time with partner

time with stranger

Control injectioninto VP

V1a Injectioninto other brain areas

V1a Injectioninto ventral pallidum

Transgenics in non-monogamous mice

• Inject prarie vole V1a gene into mouse embryo

• measure change in affiliative behavior after AVP injection as an adult

StrangerExp. Animal

Monogamous Behavior in Males

• prarie vole• pine vole• california mouse• common marmoset

• montane vole• meadow vole• white-footed mouse• rhesus monkey

Monogamous Behaviorsocially monogamousforms partner preferencebi-parental

Non-Monogamous Behaviorsocially promiscuousforms no partner preferencenon-paternal

HORMONAL, GENETIC, and NEURAL mechanisms

HIGHER V1a expression LOWER V1a expression

Ventral Pallidum• 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

NEURAL

Summary

• 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

• 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

• Ventral Pallidum appears to enhance partner preference because it activates the ‘reward pathway’ during mating

NEURAL

GENETIC

HORMONAL

V1a viral vector insertion into Prarie vole ventral pallidum increases affiliative behaviorwithout the need for mating first.insertion into caudate putamen doesn’t have this effect

# of receptors present associated behavioral response

cerebrospinal fluidAVPoxytocin

prarie vole with V1a receptor antagonist

cerebrospinal fluid (vehicle)V1a receptor antagonistoxytocin receptor antagonist

before mating with female after mating with female

Winslow et al Nature 1993