Mating and social exposure induces an opioid-dependent conditioned place preference in male but not in female prairie voles (Microtus ochrogaster)

Ulloa, Miguel; Portillo, Wendy; Diaz, NF; Young, Larry J.; Camacho, FJ; Rodrı́guez, V.M.; Paredes, RG

doi:10.1016/j.yhbeh.2017.10.015

Cited by 29 publications

(27 citation statements)

References 77 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Adult female voles were ovariectomized, and sexual receptivity was induced by daily subcutaneous injections of estradiol benzoate (EB, 0.5 μ g/vole, Sigma-Aldrich) for four days before the behavioral test. This procedure consistently induces sexual receptivity [ 24 , 44 , 45 ].…”

Section: Methodsmentioning

confidence: 99%

See 1 more Smart Citation

Effects of Mating and Social Exposure on Cell Proliferation in the Adult Male Prairie Vole (Microtus ochrogaster)

et al. 2020

Self Cite

View full text Add to dashboard Cite

Microtus ochrogaster is a rodent with a monogamous reproductive strategy characterized by strong pair bond formation after 6 h of mating. Here, we determine whether mating-induced pair bonding increases cell proliferation in the subventricular zone (SVZ), rostral migratory stream (RMS), and dentate gyrus (DG) of the hippocampus in male voles. Males were assigned to one of the four groups: (1) control: males were placed alone in a clean cage; (2) social exposure to a female (SE m/f): males that could see, hear, and smell a sexually receptive female but where physical contact was not possible, because the animals were separated by an acrylic screen with small holes; (3) social exposure to a male (SE m/m): same as group 2 but males were exposed to another male without physical contact; and (4) social cohabitation with mating (SCM): males that mated freely with a receptive female for 6 h. This procedure leads to pair bond formation. Groups 2 and 3 were controls for social interaction. Male prairie voles were injected with 5-bromo-2′-deoxyuridine (BrdU) during the behavioral tests and were sacrificed 48 h later. Brains were processed to identify the new cells (BrdU-positive) and neuron precursor cells (neuroblasts). Our principal findings are that in the dorsal region of the SVZ, SCM and SE m/f and m/m increase the percentage of neuron precursor cells. In the anterior region of the RMS, SE m/f decreases the percentage of neuron precursor cells, and in the medial region SE m/f and m/m decrease the number of new cells and neuron precursor cells. In the infrapyramidal blade of the subgranular zone of the DG, SE m/m and SCM increase the number of new neuron precursor cells and SE m/m increases the percentage of these neurons. Our data suggests that social interaction, as well as sexual stimulation, leads to pair bonding in male voles modulating cell proliferation and differentiation to neuronal precursor cells at the SVZ, RMS, and DG.

show abstract

Section: Methodsmentioning

confidence: 99%

“…The activity of both regions modulates odor recognition and olfactory learning and memory [ 17 , 18 ]. The OB and hippocampus are structures that change their activity and functional organization in response to environmental and physiological stimulation (reviews in [ 19 – 24 ]).…”

Section: Introductionmentioning

confidence: 99%

Effects of Mating and Social Exposure on Cell Proliferation in the Adult Male Prairie Vole (Microtus ochrogaster)

et al. 2020

Self Cite

View full text Add to dashboard Cite

show abstract

“…Female rats in natural, semi-natural and laboratory conditions can pace the sexual interaction, controlling the frequency and intensity of the sexual stimulation they receive (McClintock and Adler, 1978;Erskine, 1989). Mating in pacing conditions induces a reward state evaluated by the conditional place preference (CPP) test in male and female rats, mice and voles (Agmo and Berenfeld, 1990;Martinez and Paredes, 2001;Kudwa et al, 2005;Coria-Avila et al, 2006Parada et al, 2012;Pfaus et al, 2012;Ulloa et al, 2018). When females or males mate without pacing the sexual interaction, this behavior does not induces a reward state (Martinez and Paredes, 2001;Ulloa et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Repeated Paced Mating Increases the Survival of New Neurons in the Accessory Olfactory Bulb

2020

View full text Add to dashboard Cite

In female rats, the first sexual experience under paced mating conditions increases the number of newborn cells that migrate into the granular layer of the accessory olfactory bulb (AOB). Repeated paced mating has a potentiating effect on the number of new neurons that migrate to the AOB compared with a single session 15 days after paced mating. On the other hand, one paced mating session does no increases the survival of new cells 45 days after mating. In the present study, we evaluated if four paced mating sessions could increase the survival of new neurons in the AOB and main olfactory bulb (MOB) 45 days after females mated. Sexually naive female rats were ovariectomized, hormonally supplemented and randomly assigned to one of five groups: (1) Control, no sexual contact (C); (2) Four sessions in which females were exposed, without mating, to a sexually experience male rat (SE); (3) One session of paced mating (PM1); (4) Four sessions of paced mating (PM4); and (5) Four sessions of non-paced mating (NPM4). In the first behavioral test, females received the DNA synthesis marker 5-bromo-2 deoxyuridine and were euthanized 45 days later. Our data showed that the number of new cells that survived in the mitral cell layer of the AOB decreased when females were exposed to a sexually active male, in comparison to females that mated once pacing the sexual interaction. Repeated sexual behavior in pacing conditions did not increase the survival of new cells in other layers of the MOB and AOB. However, a significant increase in the percentage of new neurons in the granular and glomerular layers of the AOB and granular layer of the MOB was observed in females that mated in four sessions pacing the sexual interaction. In the group that paced the sexual interaction for one session, a significant increase in the percentage of neurons was observed in the glomerular layer of the AOB. Our data suggest that repeated paced mating increases the percentage of new neurons that survive in the olfactory bulb of female rats.

show abstract

“…the maintenance of the pair bond (Walum & Young, 2018). In this process, an association has to be created between the reinforcing properties of sex (mating) and the olfactory signature from the partner (Ulloa et al, 2018; L. J. Young & Wang, 2004; L. J.…”

Section: Introductionmentioning

confidence: 99%

Brain functional connectivity modulates social bonding in monogamous voles

Camacho

et al. 2019

Preprint

View full text Add to dashboard Cite

Microtus ochrogaster, the prairie vole, has become a valuable rodent model to study complex social behaviors, including enduring social bonding. Previous studies have related pair bonding in the prairie vole with plastic changes in several brain regions. However, the network interaction between these regions and their relevance to such socio-sexual behaviors has yet to be described. In this study, we used resting state functional magnetic resonance imaging (rsfMRI) to explore the longitudinal changes in the functional interactions of a set of brain regions previously associated with pair bonding in prairie voles. Specifically, 32 prairie voles were scanned at baseline, after 24 hours and two weeks of cohabitation and mating with a sexual partner (16 male-female pairs). Between 48 and 72 hours of cohabitation voles showed significant preference for the partner over a stranger, confirming pair bond formation; however, individual variability was observed. Network based statistics showed no sex differences in functional connectivity, but revealed a common network with significant longitudinal changes between sessions, including the anterior cingulate cortex (ACC), anterior olfactory nucleus (AON), dentate gyrus (DG), dorsal hippocampus (dHIP), lateral septum (LS), medial prefrontal cortex (mPFC), retrosplenial cortex (RSC), ventral hippocampus (vHIP), and ventral tegmental area (VTA). Furthermore, baseline functional connectivity in three sub-networks including the ACC, nucleus accumbens (NAcc), basolateral amygdala, and DG (ACC-NAcc-BLA-DG), the medial amygdala (MeA)-ventral pallidum (VP), and RSC-VTA, predicted the onset of affiliative behavior (huddling latency) in the first hours of cohabitation, even before sexual experience. Finally, a relationship was found between the strength of the pair bond (partner preference index) with long-term changes in the functional connectivity between the ventral pallidum and medial amygdala (MeA-VP). Overall, our findings revealed the association between network-level changes and the process of social bonding, and provide a novel approach to further investigate the neurophysiology of complex social behaviors displayed in the prairie vole.

show abstract

Mating and social exposure induces an opioid-dependent conditioned place preference in male but not in female prairie voles (Microtus ochrogaster)

Cited by 29 publications

References 77 publications

Effects of Mating and Social Exposure on Cell Proliferation in the Adult Male Prairie Vole (Microtus ochrogaster)

Effects of Mating and Social Exposure on Cell Proliferation in the Adult Male Prairie Vole (Microtus ochrogaster)

Repeated Paced Mating Increases the Survival of New Neurons in the Accessory Olfactory Bulb

Brain functional connectivity modulates social bonding in monogamous voles

Contact Info

Product

Resources

About