Couples Transforming Neurons. Neurogenesis and Spinogenesis in the Prairie Vole Model

Social relationships are vital in human life. Among them, stable relationships are very strong bonds, associated with benefits for cardiovascular and immune health, reduction of stress and anxiety, and even increasing longevity. For this reason, the death of the partner usually translates into depression and, frequently, the widow or widower has a higher risk of dying than their contemporaries with a partner. Surprisingly, these positive effects also have an impact on their offspring. Studies in developing countries show that children raised by both parents have better physical and mental health.

Despite their relevance, the neurobiological basis of these behaviors remains poorly understood. One obstacle to their study is that only three to five percent of mammals are socially monogamous, that is, they show a preference for a mate (without sexual exclusivity), and even fewer species display paternal care. At this point, the prairie vole (Microtus ochrogaster) stands out, a species that, after living with an specimen of the opposite sex, forms a couple bond that lasts more than one reproductive season. This bond is characterized by selective preference for mates, joint nesting, and the deployment of aggressive behaviors towards other voles. Likewise, the loss of a partner causes depressive and anxious behaviors, cardiovascular deterioration, and exaggerated endocrine responses to stress, factors that, together, can favor premature death.

When voles have offspring, both parents are involved in their upbringing; paternal care is just as important as maternal care. The progeny raised only by the mother present social alterations when they reach adulthood: they take longer to form a couple bond and they have a smaller participation in taking care of their own and others’ offspring.

Our lab researches how couple bonds alter brain plasticity at two key levels: adult neurogenesis and spinogenesis.

NEUROGENESIS
Neurogenesis means that the brain generates new neurons and incorporates them into existing circuits. This process starts with neural stem cells located in two “niches:” the sub-granular zone of the dentate gyrus of the hippocampus and the subventricular zone of the lateral ventricles. There, the cells divide to produce almost identical copies of themselves; they begin to differentiate and migrate to the granular layer of the dentate gyrus of the hippocampus or to the olfactory bulb, where they integrate as highly plastic young neurons, with the ability to modify their structure and function in response to a stimulus, so they are fundamental for learning and sexual memory formation.

Our team has shown that sexually virgin males and females raised only by the mother and who take longer to form a couple bond, have less cell proliferation in both neurogenic niches. When the father participates in the upbringing, the establishment of the couple bond in males increases proliferation in the sub-granular zone of the dentate gyrus of the hippocampus and in the subventricular zone, but this effect is not observed or is reduced if paternal care was lacking. These data suggest that the absence of the paternal figure reduces adult neurogenesis in their offspring and thus produces a delay in the formation of the couple bond. However, the effects of the decrease in adult neurogenesis on other social behaviors in voles are still unknown.

COUPLE RELATIONSHIPS AND TWO-PARENT PARTICIPATION IN RISING THE OFFSPRING HAVE A DECISIVE INFLUENCE ON THE PHYSICAL AND EMOTIONAL HEALTH OF BOTH ADULTS AND THEIR YOUNG
 
ESPINOGENESIS
Another phenomenon we have studied is spinogenesis in mature neurons, i.e. the creation of dendritic spines—small protrusions through which neurons communicate and where much of the plasticity mechanism involved in memory and learning resides. In female voles, we evaluated whether the couple bond modifies spinogenesis in the accumbens nucleus, a brain region that orchestrates motivated and rewarding behaviors (feeding, motherhood, sex, and addiction). In the prairie vole, this region also regulates the formation and maintenance of the couple bond. We found that cohabitation with copulation, as well as sensory cues from the male, elevate the density and maturity of dendritic spines in the accumbens nucleus, likely facilitating the memory of the sexual partner and the reinforcing states it induces.

Together, couple relationships and two-parent participation in rising the offspring have a decisive influence on the physical and emotional health of both adults and their young. Animal models such as the prairie vole allow us to unravel these mechanisms; the challenge now is to find out to what extent analogous processes of neurogenesis and spinogenesis also operate in humans.

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