The effects of sex, estrous cycle, and social contact on cocaine and heroin self-administration in rats

Lacy, Ryan T.; Strickland, Justin C.; Feinstein, Max; Robinson, Andrea M.; Smith, Mark A.

doi:10.1007/s00213-016-4368-9

Cited by 78 publications

(65 citation statements)

References 74 publications

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“…Importantly, the estrous cycle did not moderate the effects of social contact on cocaine self-administration, meaning that the effects of social contact described above were consistent across all four phases of estrous. We previously reported that social contact did not influence the effects of the estrous cycle on heroin self-administration (Lacy et al, 2016), suggesting that these findings are consistent across different drug classes. Collectively, these results suggest that ovarian hormones do not moderate the effects of social contact on measures of drug-seeking behavior.…”

Section: Discussionsupporting

confidence: 58%

“…Using a multilevel multivariate analysis, responding was greatest during estrus, but the main effect of cycle failed to reach statistical significance ( p = .053). Previous studies have generally reported that cocaine seeking varies across the estrous cycle, with greater levels of responding observed during estrus (Feltenstein and See, 2007; Hecht et al, 1999; Lacy et al, 2016; Lynch et al, 2000; Roberts et al, 1989). Importantly, the estrous cycle did not moderate the effects of social contact on cocaine self-administration, meaning that the effects of social contact described above were consistent across all four phases of estrous.…”

Section: Discussionmentioning

confidence: 99%

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The effects of social contact on cocaine intake in female rats

Robinson

Fronk

Zhang

et al. 2017

Drug and Alcohol Dependence

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Background Studies conducted in male rats report that social contact can either facilitate or inhibit drug intake depending on the behavior of social partners. The purpose of the present study was to: (1) examine the effects of social contact on cocaine intake in female rats, (2) examine the behavioral mechanisms by which social contact influences cocaine intake, and (3) examine whether the estrous cycle moderates the effects of social contact on cocaine intake. Methods Female rats were assigned to either isolated or pair-housed conditions in which a social partner either had access to cocaine (cocaine partner) or did not have access to cocaine (abstinent partner). Pair-housed rats were tested in custom-built operant conditioning chambers that allowed both rats to be tested simultaneously in the same chamber. Results Rats housed with a cocaine partner self-administered more cocaine than isolated rats and rats housed with an abstinent partner. A behavioral economic analysis indicated that these differences were driven by a greater intensity of cocaine demand (i.e., greater intake at lower unit prices) in rats housed with a cocaine partner. Multivariate modeling revealed that the estrous cycle did not moderate the effects of social contact on cocaine intake. Conclusions These findings indicate that: (1) social contact influences cocaine self-administration in females in a manner similar to that reported in males, (2) these effects are due to differences in the effects of social contact on the intensity of cocaine demand, and (3) these effects are consistent across all phases of the estrous cycle.

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Section: Discussionsupporting

confidence: 58%

Section: Discussionmentioning

confidence: 99%

The effects of social contact on cocaine intake in female rats

Robinson

Fronk

Zhang

et al. 2017

Drug and Alcohol Dependence

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“…Moreover, a form of opioid‐mediated long‐term potentiation (LTP) in CA3 pyramidal cells contacted by mossy fibers (i.e., mossy fiber‐CA3 synapses) is present in high‐estrogen state female rats but not male rats (Harte‐Hargrove, Varga‐Wesson, Duffy, Milner, & Scharfman, ), suggesting that opioid‐associative learning processes could be enhanced in females in certain hormonal states. In support, cyclic fluctuations of estrogen levels have been shown to alter morphine sensitivity in women (Ribeiro‐Dasilva et al, ) and patterns of heroin self‐administration in rats (Lacy, Strickland, Feinstein, Robinson, & Smith, ).…”

Section: Introductionmentioning

confidence: 93%

Chronic immobilization stress primes the hippocampal opioid system for oxycodone‐associated learning in female but not male rats

Reich

Zhou

Goldstein

et al. 2019

Synapse

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In adult female, but not male, Sprague Dawley rats, chronic immobilization stress (CIS) increases mossy fiber (MF) Leu-Enkephalin levels and redistributes delta-and mu-opioid receptors (DORs and MORs) in hippocampal CA3 pyramidal cells and GABAergic interneurons to promote excitation and learning processes following subsequent opioid exposure. Here, we demonstrate that CIS females, but not males, acquire conditioned place preference (CPP) to oxycodone and that CIS "primes" the hippocampal opioid system in females for oxycodone-associated learning. In CA3b, oxycodone-injected (Oxy) CIS females relative to saline-injected (Sal) CIS females exhibited an increase in the cytoplasmic and total densities of DORs in pyramidal cell dendrites so that they were similar to Sal-and Oxy-CIS males. Consistent with our earlier studies, Sal-and Oxy-CIS females but not CIS males had elevated DOR densities in MF-CA3 dendritic spines, which we have previously shown are important for opioid-mediated long-term potentiation. In the dentate gyrus, Oxy-CIS females had more DOR-labeled interneurons than Sal-CIS females. Moreover, Sal-and Oxy-CIS females compared to both groups of CIS males had elevated levels of DORs and MORs in GABAergic interneuron dendrites, suggesting capacity for greater synthesis or storage of these receptors in circuits important for opioid-mediated disinhibition.However, more plasmalemmal MORs were on large parvalbumin-containing dendrites of Oxy-CIS males compared to Sal-CIS males, suggesting a limited ability for increased granule cell disinhibition. These results suggest that low levels of DORs in MF-CA3 synapses and hilar GABAergic interneurons may contribute to the attenuation of oxycodone CPP in males exposed to CIS. K E Y W O R D S conditioned place preference, delta-opioid receptor, drug addiction, GABAergic interneurons, Leu-enkephalin, mossy fiber-CA3 synapses, mu-opioid receptor S U PP O RTI N G I N FO R M ATI O N Additional supporting information may be found online in the Supporting Information section at the end of the article. How to cite this article: Reich B, Zhou Y, Goldstein E, et al. Chronic immobilization stress primes the hippocampal opioid system for oxycodone-associated learning in female but not male rats. Synapse. 2019;73:e22088. https://doi.

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“…There are effects of estrous cycle on heroin self-administration, with females reducing intake during proestrus, but exhibiting overall greater heroin intake than males [140]. Female rats also acquire heroin intake more rapidly than males [141,142].…”

Section: Mu-opioid Receptorsmentioning

confidence: 99%

Sex differences in neural mechanisms mediating reward and addiction

Becker

Chartoff

2018

Neuropsychopharmacol

355

251

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There is increasing evidence in humans and laboratory animals for biologically based sex differences in every phase of drug addiction: acute reinforcing effects, transition from occasional to compulsive use, withdrawal-associated negative affective states, craving, and relapse. There is also evidence that many qualitative aspects of the addiction phases do not differ significantly between males and females, but one sex may be more likely to exhibit a trait than the other, resulting in population differences. The conceptual framework of this review is to focus on hormonal, chromosomal, and epigenetic organizational and contingent, sex-dependent mechanisms of four neural systems that are known-primarily in males-to be key players in addiction: dopamine, mu-opioid receptors (MOR), kappa opioid receptors (KOR), and brain-derived neurotrophic factor (BDNF). We highlight data demonstrating sex differences in development, expression, and function of these neural systems as they relate-directly or indirectly-to processes of reward and addictive behavior, with a focus on psychostimulants and opioids. We identify gaps in knowledge about how these neural systems interact with sex to influence addictive behavior, emphasizing throughout that the impact of sex can be highly nuanced and male/female data should be reported regardless of the outcome.

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The effects of sex, estrous cycle, and social contact on cocaine and heroin self-administration in rats

Cited by 78 publications

References 74 publications

The effects of social contact on cocaine intake in female rats

The effects of social contact on cocaine intake in female rats

Chronic immobilization stress primes the hippocampal opioid system for oxycodone‐associated learning in female but not male rats

Sex differences in neural mechanisms mediating reward and addiction

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