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Methamphetamine Consumption Inhibits Pair Bonding and Hypothalamic Oxytocin in Prairie Voles.

ABSTRACT: Methamphetamine (MA) abuse has been linked to violence, risk-taking behaviors, decreased sexual inhibition, and criminal activity. It is important to understand mechanisms underlying these drug effects for prevention and treatment of MA-associated social problems. Previous studies have demonstrated that experimenter-administered amphetamine inhibits pair bonding and increases aggression in monogamous prairie voles. It is not currently known whether similar effects on social behaviors would be obtained under conditions during which the drug is voluntarily (actively) administered. The current study investigated whether MA drinking affects pair bonding and what neurocircuits are engaged. In Experiment 1, we exposed male and female voles to 4 days each of 20 and 40 mg/L MA under a continuous 2-bottle choice (2BC) procedure. Animals were housed either singly or in mesh-divided cages with a social partner. Voles consumed MA in a drinking solution, but MA drinking was not affected by either sex or housing condition. In Experiment 2, we investigated whether MA drinking disrupts social bonding by measuring aggression and partner preference formation following three consecutive days of 18-hour/day access to 100 mg/L MA in a 2BC procedure. Although aggression toward a novel opposite-sex animal was not affected by MA exposure, partner preference was inhibited in MA drinking animals. Experiment 3 examined whether alterations in hypothalamic neuropeptides provide a potential explanation for the inhibition of partner preference observed in Experiment 2. MA drinking led to significant decreases in oxytocin, but not vasopressin, in the paraventricular nucleus of the hypothalamus. These experiments are the first investigation into how voluntary pre-exposure to MA affects the development of social attachment in a socially monogamous species and identify potential neural circuits involved in these effects.

SUBMITTER: Hostetler CM

PROVIDER: S-EPMC4933333 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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Methamphetamine Consumption Inhibits Pair Bonding and Hypothalamic Oxytocin in Prairie Voles.

Hostetler Caroline M CM Phillips Tamara J TJ Ryabinin Andrey E AE

PloS one 20160705 7

Methamphetamine (MA) abuse has been linked to violence, risk-taking behaviors, decreased sexual inhibition, and criminal activity. It is important to understand mechanisms underlying these drug effects for prevention and treatment of MA-associated social problems. Previous studies have demonstrated that experimenter-administered amphetamine inhibits pair bonding and increases aggression in monogamous prairie voles. It is not currently known whether similar effects on social behaviors would be ob ...[more]

PMID: 27380172

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Project description:There is much interest in targeting the activity in the oxytocin system to regulate social bonding. However, studies with exogenous administration of oxytocin face the caveats of its low stability, poor brain permeability and insufficient receptor specificity. The use of a small-molecule oxytocin receptor-specific agonist could overcome these caveats. Prior to testing the potential effects of a brain-penetrant oxytocin receptor agonist in clinical settings, it is important to assess how such an agonist would affect social bonds in animal models. The facultatively monogamous prairie voles (Microtus ochrogaster), capable of forming long-term social attachments between adult individuals, are an ideal rodent model for such testing. Therefore, in a series of experiments we investigated the effects of the recently developed oxytocin receptor-specific agonist LIT-001 on the acquisition and expression of partner preference, a well-established model of pair bonding, in prairie voles. LIT-001 (10 mg/kg, intraperitoneal), as expected, facilitated the acquisition of partner preference when administered prior to a 4hr cohabitation. In contrast, while animals injected with vehicle after the 4hr cohabitation exhibited significant partner preference, animals that were injected with LIT-001 did not show such partner preference. This result suggests that OXTR activation during expression of pair bonding can inhibit partner preference. The difference in effects of LIT-001 on acquisition versus expression was not due to basal differences in partner preference between the experiments, as LIT-001 had no significant effects on expression of partner preference if administered following a shorter (2hr-long) cohabitation. Instead, this difference agrees with the hypothesis that the activation of oxytocin receptors acts as a signal of presence of a social partner. Our results indicate that the effects of pharmacological activation of oxytocin receptors crucially depend on the phase of social attachments.

Project description:Around 5 % of mammals are socially monogamous and both parents provide care to the pups (biparental, BP). Prairie voles are socially monogamous rodents extensively used to understand the neurobiological basis of pair bond formation and the consequences that the absence of one parent has in the offspring. Pair bonding, characterized by selective affiliation with a sexual partner, is facilitated in prairie voles by mating for 6 h or cohabitation without mating for 24 h. It was previously shown that prairie voles raised by their mother alone (monoparental, MP) show delayed pair bond formation upon reaching adulthood. In this study we evaluated the effects of BP and MP care provided on the offspring's development, ability to detect olfactory cues, preference for sexually relevant odors, display of sexual behavior, as well as the rewarding effects of mating. We also measured dopamine and serotonin concentration in the nucleus accumbens (ventral striatum) and dorsal striatum after cohabitation and mating (CM) to determine if differences in these neurotransmitters could underlie the delay in pair bond formation in MP voles. Our data showed that MP voles received less licking/grooming than BP voles, but no developmental differences between groups were found. No differences were found in the detection and discrimination of olfactory cues or preference for sexually relevant odors, as all groups innately preferred opposite sex odors. No differences were found in the display of sexual behavior. However, CM induced reinforcing properties only in BP males, followed by a preference for their sexual partner in BP but not MP males. BP males showed an increase in dopamine turnover (DOPAC/DA and HVA/DA) in the nucleus accumbens in comparison to MP voles. No differences in dopamine, serotonin or their metabolites were found in the dorsal striatum. Our results indicate that MP voles that received less licking behavior exhibit a delay in pair bond formation possibly because the sexual interaction is not rewarding enough.

Dataset Information

Methamphetamine Consumption Inhibits Pair Bonding and Hypothalamic Oxytocin in Prairie Voles.

Publications

Methamphetamine Consumption Inhibits Pair Bonding and Hypothalamic Oxytocin in Prairie Voles.

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