Understanding pup affective state through ethologically significant ultrasonic vocalization frequency

Julie Boulanger-Bertolus,Anne-Marie Mouly,Millie Rincón-Cortés,Regina M Sullivan

doi:10.1038/s41598-017-13518-6

Abstract

Throughout life, rats emit ultrasonic vocalizations (USV) when confronted with an aversive situation. However, the conditions classically used to elicit USV vary greatly with the animal’s age (isolation from the dam in infancy, versus nociceptive stimulation in adults). The present study is the first to characterize USV responses to the same aversive event throughout development. Specifically, infant, juvenile and adult rats were presented with mild foot-shocks and their USV frequency, duration, and relationship with respiration and behavior were compared. In juvenile and adult rats, a single class of USV is observed with an age-dependent main frequency and duration (30 kHz/400 ms in juveniles, 22 kHz/900 ms in adults). In contrast, infant rat USV were split into two classes with specific relationships with respiration and behavior: 40 kHz/300 ms and 66 kHz/21 ms. Next, we questioned if these infant USV were also emitted in a more naturalistic context by exposing pups to interactions with the mother treating them roughly. This treatment enhanced 40-kHz USV while leaving 66-kHz USV unchanged suggesting that the use of USV goes far beyond a signal studied in terms of amount of emission, and can inform us about some aspects of the infant’s affective state.

Highlights

Rats and other rodents have developed communication in the ultrasonic range of sound frequencies
The same aversive stimulus across development and compared ultrasonic vocalizations (USV) in response to this stimulus at three different ages: infant, juvenile and adult. This allowed us to describe the existence of two classes of USV in infant rats: one corresponding to the infant USV classically described in the literature and showing similarities with adult and juvenile USV, and a novel class, poorly characterized so far, which appears to be specific to infancy
Juvenile and infant 40-kHz USV, USV duration is correlated with expiration duration (Adult: r = 0.80, n = 3945; Juvenile: r = 0.49, n = 1927; Infant 40-kHz USV: r = 0.55, n = 5479), while this is not the case for infant 66-kHz USV (r = 0.04, n = 3270). (D) Probability of Density Function (PDF) of the respiratory frequency during silent freezing and movement, and during USV emission

Summary

Introduction

Rats and other rodents have developed communication in the ultrasonic range of sound frequencies. Long “22-kHz” vocalizations (18–32 kHz) are observed in aversive situations such as male-male aggression and social defeat[1,2], exposure to predator[3] or inescapable painful stimuli[4]. The same aversive stimulus (foot-shock) across development and compared USV in response to this stimulus at three different ages: infant, juvenile and adult This allowed us to describe the existence of two classes of USV in infant rats: one corresponding to the infant USV classically described in the literature and showing similarities with adult and juvenile USV, and a novel class, poorly characterized so far, which appears to be specific to infancy. We assessed whether the two classes of USV observed in the context of foot-shock delivery were induced by this naturalistic aversive context

Methods

Results

Conclusion