Maturation of Social-Vocal Communication in Prairie Vole (Microtus ochrogaster) Pups

Impairments in social communication are common among neurodevelopmental disorders. While traditional animal models have advanced our understanding of the physiological and pathological development of social behavior, they do not recapitulate some aspects where social communication is essential, such as biparental care and the ability to form long-lasting social bonds. Prairie voles (Microtus ochrogaster) have emerged as a valuable rodent model in social neuroscience because they naturally display these behaviors. Nonetheless, the role of vocalizations in prairie vole social communication remains unclear. Here, we studied the ontogeny [from postnatal days (P) 8–16] of prairie vole pup ultrasonic vocalizations (USVs), both when isolated and when the mother was present but physically unattainable. In contrast to other similarly sized rodents such as mice, prairie vole pups of all ages produced isolation USVs with a relatively low fundamental frequency between 22 and 50 kHz, often with strong harmonic structure. Males consistently emitted vocalizations with a lower frequency than females. With age, pups vocalized less, and the acoustic features of vocalizations (e.g., duration and bandwidth) became more stereotyped. Manipulating an isolated pup's social environment by introducing its mother significantly increased vocal production at older (P12–16) but not younger ages, when pups were likely unable to hear or see her. Our data provide the first indication of a maturation in social context-dependent vocal emission, which may facilitate more active acoustic communication. These results help lay a foundation for the use of prairie voles as a model organism to probe the role of early life experience in the development of social-vocal communication.

Hearing Ability of Prairie Voles (Microtus ochrogaster)

Hearing ability of mammals can be impacted by many factors including social cues, environment, and physical properties of animal morphology. Despite being used commonly to study social behaviors, the hearing ability of the monogamous prairie vole (Microtus ochrogaster) has never been fully characterized. In this study, we measure morphological head and pinna features and use auditory brainstem responses to measure hearing ability of prairie voles characterizing monaural and binaural hearing and hearing range. Additionally, we measured unbonded male and female voles to characterize differences due to sex. We found that prairie voles have intermediate hearing ability with an optimal hearing range of 8 to 32 kHz, robust binaural hearing ability, and characteristic monaural ABRs. We show no differences between the sexes for binaural hearing or hearing range, however female voles have increased amplitude of peripheral ABR waves I and II and increased latency of wave IV. Our results confirm that prairie voles have both low and high frequency hearing, binaural hearing capability, and despite biparental care and monogamy, differences in processing of sound information between the sexes. These data further highlight the necessity to understand sex-specific differences in neural processing that may underly variability in behavioral responses between sexes.

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

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.

Do prairie voles (Microtus ochrogaster) change their activity and space use in response to domestic cat (Felis catus) excreta?

Behavioral changes that reduce the risk of predation in response to predator-derived odor cues are widespread among mammalian taxa and have received a great deal of attention. Although voles of the genus Microtus are staples in the diet of many mammalian predators, including domestic cats (Felis catus), there are no previous studies on vole space utilization and activity levels in response to odor cues from domestic cats. Therefore, the objective of our study was to investigate responses of adult prairie voles (Microtus ochrogaster) living in semi-natural habitats to odor cues from domestic cat excreta. Contrary to expectations, neither adult males or females showed significant changes in space use or willingness to enter traps in response to cat odors. One hypothesis to explain our results are that prairie voles have not co-evolved with domestic cats long enough to respond to their odors. Other possible explanations include whether levels of odors in the environment were sufficient to trigger a response or that the perceived risk of predation from odor cues alone did not outweigh relative costs of changing space use and activity levels. Future studies should consider multiple factors when determining what cues are sufficient to elicit antipredatory behavior.