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

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.

Hearing ability of prairie voles (Microtus ochrogaster)

“… 8,47 Pup vocalizations are also comparatively “low” with maximal spectra between 22 and 50 kHz, consistent with the broad hearing range. 40 The fact that there are few differences between males and females in ABR-measured hearing range may well be consistent with the presence of strong biparental care given that males and females respond similarly to pup ultrasonic vocalizations. 2,3 It would be interesting to directly compare similar measures and potential sex differences to other species with similar parental care and breeding strategies such as Mongolian gerbils and guinea pigs.…”

“…Prairie voles show a broad hearing range with best hearing between 8 and 32 kHz as for other rodents of similar size 10 and consistent with pup calls that have vocalization fundamental frequencies between 22 and 50 kHz. 40 There were no significant differences in overall click threshold [Fig. 3(B) ; p = 0.35].…”

Vocal recognition of partners by female prairie voles

“…15 Similarly, behavioral studies of pup vocalizations suggest that dams can at least discriminate calls from pups of their own litter 37 or of different sexes, 38 but neither necessarily implies identifying individuals. In fact, while prairie vole pups vocalize at higher rates than pups of similar species, 39,40 their calls become more stereotyped between early infancy and later stages (e.g., P6 to P16), 41 making it unclear whether adult vole vocalizations contain sufficient individuality. Our acoustic analysis and decoding results indicate they do.…”

“…Sounds with fewer than 6 samples (i.e., shorter than 3 ms) were excluded. USVSEG was modified as reported previously 41 to generate frequency contours -traces of the time, sound frequency, and sound amplitude at each sample within all extracted vocalizations. The contours were then further refined using custom-written MATLAB scripts.…”