Abstract
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.
Highlights
Our understanding of the pathological and physiological development of social-vocal communication has improved through the use of traditional animal models such as rats and mice
Similar to other rodent species (Naito and Tonoue, 1987; Campbell et al, 2014; Johnson et al, 2017) and prior reports in prairie voles (Rabon Jr et al, 2001; Terleph, 2011), pup vocal emission decreases with age
We assessed changes in variability in the number of segments per vocalization and found that younger pups showed the greatest variability in the number of segments within individual vocalizations [F(5, 84) = 10.5, p < 10−7; one-way ANOVA; Figure 6D]. Both P6 and P8 pups emitted vocalizations that were significantly more variable than P10– P16 pups. These results indicate that the acoustic features of prairie vole pup vocalizations, including vocal duration, bandwidth, and the number of unique
Summary
Our understanding of the pathological and physiological development of social-vocal communication has improved through the use of traditional animal models such as rats and mice. Traditional rodent models fail to capture the breadth and diversity of human behavior wherein social communication is essential, such as biparental care of offspring and the ability to form long-lasting, selective social bonds (Bales et al, 2021). Prairie voles typically form lifelong, socially monogamous relationships with a single mate, exhibit biparental rearing of pups, and engage in alloparental care (McGraw and Young, 2010; Sadino and Donaldson, 2018; Walum and Young, 2018). Studies using prairie voles and other vole species have been vital in furthering our understanding of the neural basis of affiliative behaviors. Despite the volume of neurobiological and ethological studies on prairie voles, the role of specific sensory modalities in social communication during affiliative behaviors is not well-understood. Vocalizations may play a larger role in prairie vole social communication as compared to other rodents
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