Chronic cold exposure causes left ventricular hypertrophy that appears to be physiological.

Exposure to winter cold causes an increase in energy demands to meet the challenge of thermoregulation. In small rodents, this increase in cardiac output leads to a profound cardiac hypertrophy, 2-3x that typically seen with exercise training. The nature of this hypertrophy and its relevance to winter mortality remains unclear. Our goal was to characterize cold-induced cardiac hypertrophy and to assess its similarity to either exercise-induced (physiological) hypertrophy or the pathological hypertrophy of hypertension. We hypothesized that cold-induced hypertrophy will most closely resemble exercise-induced hypertrophy, but be another unique pathway for physiological cardiac growth. We found that cold-induced hypertrophy was largely reversed after return to warm temperatures. Further, metabolic rates were elevated while gene expression and mitochondrial enzyme activities indicative of pathology were absent. A gene expression panel comparing hearts of exercised and cold exposed mice further suggests that these activities are similar, although not identical. In conclusion, we found that chronic cold led to a phenotype that most closely resembled physiological hypertrophy, with enhanced metabolic rate, without induction of fetal genes , but with decreased expression of genes associated with fatty acid oxidation, suggesting that heart failure is not a cause of winter mortality in small rodents and identifying a novel approach for the study of cardiac growth.

Sexual differences in responses of meadow voles to environmental cues in the presence of mink odor.

In rodents, defensive behaviors increase the chances of survival during a predator encounter. Observable rodent defensive behaviors have been shown to be influenced by the presence of predator odors and nearby environmental cues such as cover, odors from conspecifics and food availability. Our experiment tested whether a predator scent cue influenced refuge preference in meadow voles within a laboratory setting. We placed voles in an experimental apparatus with bedding soaked in mink scent versus olive oil as a control across from four tubes that either contained (a) a dark plastic covering, (b) opposite-sex conspecific odor, (c) a food pellet, or (d) an empty, unscented space. A three-way interaction of tube contents, subject sex, and the presence of mink or olive oil on the preference of meadow voles to spend time in each area of the experimental apparatus and their latency to enter each area of the apparatus revealed sex differences in the environmental preference of meadow voles facing the risk of predation. The environmental preference of female, but not male, meadow voles was altered by the presence of mink urine or olive oil. A similar trend was found in the latency of males and females to enter each area of the experimental apparatus. These differences suggest that each sex utilizes different methods to increase their fitness when experiencing a predation risk. The observed sex differences may be explained by the natural history of voles owing to the differences in territorial range and the dynamics of evasion of terrestrial predators.

Examining Empathy Through Consolation Behavior in Prairie Voles.

Empathy is an affective and cognitive event in which an organism experiences an approximation of the physical or psychological state of another organism. The phenomenon has been well-studied in humans but is not as widely researched in other animals. Burkett and colleagues in a 2016 article published in Science measured empathy in prairie voles (Microtus ochrogaster) and meadow voles (Microtus pennsylvanicus) by observing consolation behavior between non-stressed and stressed individuals. Their data from behavioral analyses and histochemistry support their hypothesis that consolation behavior in prairie voles shares similar behavioral characteristics and conserved biological mechanisms with human empathy. Prairie voles match anxiety and fear states as well as groom stressed familiar conspecifics to lessen their stress. An oxytocin receptor antagonist abolished this empathetic response. This research impacted the field of neuroscience by demonstrating human-like empathy in rodents, and thereby supporting the value of animal models to investigations of higher order human experiences. The paper is also a valuable and accessible resource to undergraduate neuroscience students-from introductory courses to advanced seminars. In the classroom, this research provides a foundational look at the expanding field of social neuroscience. Empathy in prairie voles raises thought-provoking discussion concerning emotions, social behavior, and human nature.

Stress impairs new but not established relationships in seasonally social voles.

Affiliative social relationships are impacted by stressors and can shape responses to stress. However, the effects of stress on social relationships in different contexts are not well understood. Meadow voles provide an opportunity to study these effects on peer relationships outside of a reproductive context. In winter months, female meadow voles cohabit with peers of both sexes, and social huddling is facilitated by exposure to short, winter-like day lengths in the lab. We investigated the role of stress and corticosterone (cort) levels in social behavior in short day-housed female meadow voles. A brief forced swim elevated cort levels, and we assessed the effects of this stressor on new and established relationships between females. In pairs formed following exposure to swim stress, the stressor significantly reduced the fraction of huddling time subjects spent with a familiar partner. Swim stress did not affect partner preferences in pairs established prior to the stressor. Finally, we examined fecal glucocorticoid metabolite levels via immunoassay in voles housed under short day (10h light) versus long day (14 h light) conditions and detected higher glucocorticoid levels in long day-housed voles. These findings support a role for stress regulation in the formation of social relationships in female meadow voles, and are consistent with a potential role for seasonal variation in cort in the behavioral transition from solitary to social. Together they highlight the importance of stress and possibly glucocorticoid signaling for social behavior.

Behavioral comparisons of male and female pups of prairie voles (Microtus ochrogaster) and meadow voles (M. pennsylvanicus).

Sexual dimorphism in mammals typically is reduced in monogamous species relative to polygynous species, with promiscuous species being intermediate. This pattern of dimorphism characterizes adult behavior and body mass of prairie voles, a monogamous species, when compared with meadow voles, a closely related polygynous or promiscuous species. We examined whether the pattern also applies to young of the two species by observing individual pups living in family groups in seminatural environments. Observations during the second week of life revealed no sex differences in pup behavior or body mass. However, we detected species differences in suckling behavior, jockeying for position within the huddle (especially among males), and body mass that replicate and extend our previous observations. These data indicate that patterns of sexual dimorphism associated with different mating systems may not be evident in juvenile mammals, but that species differences in behavior and body mass can be obvious at this stage.

Selectivity and Sociality: Aggression and Affiliation Shape Vole Social Relationships.

The formation of selective social relationships is not a requirement of group living; sociality can be supported by motivation for social interaction in the absence of preferences for specific individuals, and by tolerance in place of social motivation. For species that form selective social relationships, these can be maintained by preference for familiar partners, as well as by avoidance of or aggression toward individuals outside of the social bond. In this review, we explore the roles that aggression, motivation, and tolerance play in the maintenance of selective affiliation. We focus on prairie voles (Microtus ochrogaster) and meadow voles (Microtus pennsylvanicus) as rodent species that both exhibit the unusual tendency to form selective social relationships, but differ with regard to mating system. These species provide an opportunity to investigate the mechanisms that underlie social relationships, and to compare mechanisms supporting pair bonds with mates and same-sex peer relationships. We then relate this to the role of aggression in group composition in a comparative context.

Social selectivity and social motivation in voles.

Selective relationships are fundamental to humans and many other animals, but relationships between mates, family members, or peers may be mediated differently. We examined connections between social reward and social selectivity, aggression, and oxytocin receptor signaling pathways in rodents that naturally form enduring, selective relationships with mates and peers (monogamous prairie voles) or peers (group-living meadow voles). Female prairie and meadow voles worked harder to access familiar versus unfamiliar individuals, regardless of sex, and huddled extensively with familiar subjects. Male prairie voles displayed strongly selective huddling preferences for familiar animals, but only worked harder to repeatedly access females versus males, with no difference in effort by familiarity. This reveals a striking sex difference in pathways underlying social monogamy and demonstrates a fundamental disconnect between motivation and social selectivity in males-a distinction not detected by the partner preference test. Meadow voles exhibited social preferences but low social motivation, consistent with tolerance rather than reward supporting social groups in this species. Natural variation in oxytocin receptor binding predicted individual variation in prosocial and aggressive behaviors. These results provide a basis for understanding species, sex, and individual differences in the mechanisms underlying the role of social reward in social preference.

What factors drive the formation of social relationships can vary greatly in animals. While some individuals may be motivated to find social partners, others may just tolerate being around others. A desire to avoid strangers may also lead an individual to seek out acquaintances or friends. Sometimes a mix of these factors shape social behavior. Studying motivation for social relationships in the laboratory is tricky. Traditional laboratory animals like mice and rats do not bond with specific peers or mates. But small burrowing rodents called voles are a more relationship-oriented alternative to mice and rats. Prairie voles form selective and enduring preferences for both their mates and familiar same-sex peers. Meadow voles on the other hand, live alone much of the year but move in with other animals over the winter. Beery et al. show that social motivation in voles varies by relationship type, species and sex. In the experiments, voles were first trained to press a lever to get a food reward. Then, the food reward was swapped with access to familiar or unfamiliar voles. Female prairie voles strived to be with animals they knew rather than to be with strangers, while male prairie voles tried hard to access any female. In contrast, meadow voles did not overly exert themselves to access other animals. Beery et al. then measured oxytocin receptor levels in the brains of prairie voles. Prairie voles that had more receptors for oxytocin in part of their brain known as the nucleus accumbens worked harder to access their familiar partner. But individuals with more oxytocin receptors in the bed nucleus of the stria terminalis were more likely to attack an unfamiliar animal. The meadow voles' behavior suggests that they are more motivated by tolerance of familiar animals, while the female prairie voles may find it rewarding to be with animals they have bonded with. These differences may help explain why these two species of vole have evolved different social behaviors. The experiments also suggest that oxytocin ­ which is linked with maternal behavior ­ plays an important role in social motivation. Learning more about the biological mechanisms that underlie vole social behaviors may help scientists identify fundamental aspects of social behavior that may apply to other species including humans.

Use of space and habitats by meadow voles at the home range, patch and landscape scales.

Using capture/recapture methods, we examined the spatial usage patterns of Microtus pennsylvanicus within and between experimentally created habitat patches of three sizes (1.0, 0.25 and 0.0625 ha) and between a 20-ha fragmented and a 20-ha continuous habitat landscape. We tested the prediction that home ranges near patch edges would be qualitatively different from those in patch interiors, and that the edge:interior habitat ratio could be used to make predictions concerning the dispersion and spatial use of individuals occupying different sized patches and between landscapes with different habitat structure. We found adult females on patch edges to have larger and more exclusive home ranges, larger body sizes, longer residence times, and to reproduce at a higher frequency than those in patch interiors. These "edge effects" also appeared to be largely responsible for the greater proportion of larger, reproductive females we found in small than larger patches and in the fragmented than in the continuous habitat (control) landscape. The selection of higher quality edge habitats by dominant females and the relegation of sub-dominants to patch interiors provides an explanation for the observed differences in the distribution and performance of females over patches and between landscapes.

HETEROZYGOSITY, AGGRESSION, AND POPULATION FLUCTUATIONS IN MEADOW VOLES (MICROTUS PENNSYLVANICUS).

We tested whether variation in heterozygosity could produce cyclic changes in population size in meadow voles (Microtus pennsylvanicus). For this to occur, three conditions must be met: (1) populations are more outbred (heterozygotic) at high than low population density, (2) heterozygotic voles are more aggressive than relatively inbred individuals, and (3) heterozygotic voles have lower reproductive fitness, though being superior at defending resources. We found no evidence that heterozygosity varied with population size or that reproductive success varied with heterozygosity. However, the former test was indirect and relatively weak. We directly measured aggression and heterozygosity of individual voles. Aggression was significantly related to heterozygosity: higher heterozygosity correlated with more aggression in males and less aggression in females. The proportion of variance in aggression that could be explained by heterozygosity was small. These results suggest that changes in population size of meadow voles could not be driven by systematic changes in heterozygosity with population size.