Elsevier

Psychoneuroendocrinology

Volume 39, January 2014, Pages 152-157
Psychoneuroendocrinology

Short Communication
Social partners prevent alcohol relapse behavior in prairie voles

https://doi.org/10.1016/j.psyneuen.2013.10.006Get rights and content

Summary

There is robust evidence for a protective role of interpersonal factors such as social support on alcohol relapse, but research on the mechanisms that social factors may be acting on to effectively protect individuals against relapse is lacking. Prairie voles are highly social, monogamous rodents that freely self-administer ethanol in high amounts, and are a useful model for understanding social influences on alcohol drinking. Here we investigated whether prairie voles can be used to model social influences on relapse using the alcohol deprivation effect, in which animals show a transient increase in ethanol drinking following deprivation. In Experiment I, subjects were housed alone during four weeks of 24-h access to 10% ethanol in a two-bottle choice test. Ethanol was then removed from the cage for 72 h. Animals remained in isolation or were then housed with a familiar same-sex social partner, and ethanol access was resumed. Animals that remained isolated showed an increase in ethanol intake relative to pre-deprivation baseline, indicative of relapse-like behavior. However, animals that were socially housed did not show an increase in ethanol intake, and this was independent of whether the social partner also had access to ethanol. Experiment II replicated the alcohol deprivation effect in a separate cohort of isolated animals. These findings demonstrate that prairie voles display an alcohol deprivation effect and suggest a ‘social buffering’ effect of relapse-like behavior in the prairie vole. This behavioral paradigm provides a novel approach for investigating the behavioral and neurobiological underpinnings of social influences on alcohol relapse.

Introduction

Rates of relapse from alcohol use disorders are estimated as high as 80% (Dawson et al., 2007). It is critical to understand the biological mechanisms underlying relapse-related behaviors and to identify target treatments for improving rates of remission in alcoholics. There is robust evidence for a protective role of interpersonal factors such as social support, marital status, and marital quality against alcohol relapse (Garmendia et al., 2008, Walter et al., 2006). However, research on the mechanisms that social factors may be acting on to effectively protect individuals against relapse is lacking (Hunter-Reel et al., 2009).

Prairie voles (Microtus ochrogaster) are highly social and, unlike other traditional rodent models, show specific social attachments for both same-sex (DeVries et al., 1997) and opposite-sex partners (Carter and Getz, 1993). These animals freely self-administer ethanol in high amounts, and will do so without training on a sucrose-fading procedure (Anacker et al., 2011a). Prairie voles also display drinking patterns under social conditions that contrast with what is typically seen in other animal models. Specifically, voles that are housed in same-sex pairs show higher basal levels of both alcohol consumption and preference compared to animals housed in isolation (Anacker et al., 2011a, Hostetler et al., 2012). This is in contrast to the isolation-induced increases in drinking observed in many other rodents (as reviewed in Anacker and Ryabinin, 2010), and is more similar to social facilitation of drinking that is observed in humans (de Castro, 1990). On the other hand, under certain social conditions, the drinking behavior of one animal can exert a direct and persistent effect to reduce drinking in a social partner (Anacker et al., 2011b). Thus, it is becoming increasingly clear that the details of social context are important factors in the ethanol drinking behavior of voles. This is relevant for modeling human behavior, in which the influence of a social partner can be highly specific to the social relationship and context.

Relapse has been modeled in mice and rats by the alcohol deprivation effect (ADE), in which alcohol-exposed subjects show elevated intake of alcohol following abstinence (Sinclair and Senter, 1968, Spanagel and Holter, 1999). Specifically, animals show a transient (<48 h) increase in alcohol drinking following deprivation. However, mice and rats do not show specific social attachments, and the effects of social influences on the ADE have not been studied in rodents. The aims of this study were two-fold: (1) determine whether prairie voles demonstrate an ADE, and (2) investigate whether the ADE is influenced by the social environment. Specifically, we hypothesized that the presence of a familiar social partner would ‘buffer’ against expression of the ADE. We also investigated whether the drinking behavior of a social partner would affect the ADE, and expected that a non-drinking (“abstinent”) partner would be more effective at social buffering of relapse-like behavior than a drinking partner.

Section snippets

Methods

The subjects used in this study were from a breeding colony housed at the Portland Veterans Affairs Medical Center Veterinary Medical Unit. Animals were weaned at 21 days and housed in same-sex sibling groups in cages (27 cm × 27 cm × 13 cm) under controlled temperature, humidity, and 14L:10D light conditions. Food (LabDiet Hi-Fiber Rabbit chow, cracked corn, and oats) and water were available ad libitum throughout the experiments. All subjects had access to cotton nestlets throughout the experiments.

Experiment I

Daily ethanol intake and preference during Experiment I are presented in Fig. 1. The baseline daily g/kg intake (average of Days 23–28) for each group was: isolated: 8.67 ± 1.3; with dinking partner: 9.34 ± 1.3; with abstinent partner: 8.5 ± 1.3. There was a significant interaction between time and housing on ethanol intake (F4,112 = 3.91, p = 0.005; Fig. 1a), but not preference (F4,112 = 0.85, p = 0.49; Fig. 1b). Post hoc comparisons indicated a significant increase in ethanol intake relative to baseline on

Discussion

We demonstrated for the first time that prairie voles display an ADE, indicative of relapse-like behavior. In two experiments we found that four weeks of self-administration followed by a brief (72 h) forced abstinence period is sufficient to induce relapse-like alcohol drinking in the prairie vole. Isolated voles increased both ethanol intake (26% and 40% in Experiment I and II, respectively; Figure 1, Figure 2) and preference (35%, but this increase was significant only in Experiment II; Fig. 2

Role of funding source

This research was funded by NIH grant AA019793. The funding agency had no role in the design of the present study or in the analysis, interpretation, or writing of the data.

Conflict of interest

The authors declare no conflict of interest.

Acknowledgements

We gratefully acknowledge Allison Anacker, Jennifer Loftis and the Portland VA animal care staff for assistance on this project.

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