Rodent ultrasonic vocalizations are bound to active sniffing behavior.

Yevgeniy B Sirotin,Diego A Laplagne,Martã­N Elias Costa

doi:10.3389/fnbeh.2014.00399

Abstract

During rodent active behavior, multiple orofacial sensorimotor behaviors, including sniffing and whisking, display rhythmicity in the theta range (~5–10 Hz). During specific behaviors, these rhythmic patterns interlock, such that execution of individual motor programs becomes dependent on the state of the others. Here we performed simultaneous recordings of the respiratory cycle and ultrasonic vocalization emission by adult rats and mice in social settings. We used automated analysis to examine the relationship between breathing patterns and vocalization over long time periods. Rat ultrasonic vocalizations (USVs, “50 kHz”) were emitted within stretches of active sniffing (5–10 Hz) and were largely absent during periods of passive breathing (1–4 Hz). Because ultrasound was tightly linked to the exhalation phase, the sniffing cycle segmented vocal production into discrete calls and imposed its theta rhythmicity on their timing. In turn, calls briefly prolonged exhalations, causing an immediate drop in sniffing rate. Similar results were obtained in mice. Our results show that ultrasonic vocalizations are an integral part of the rhythmic orofacial behavioral ensemble. This complex behavioral program is thus involved not only in active sensing but also in the temporal structuring of social communication signals. Many other social signals of mammals, including monkey calls and human speech, show structure in the theta range. Our work points to a mechanism for such structuring in rodent ultrasonic vocalizations.

Highlights

Many behaviors are organized into repetitive cycles
Our results show that ultrasonic vocalizations are an integral part of the rhythmic orofacial behavioral ensemble
Our results show that orofacial behaviors with theta rhythmicity are involved in active sampling and temporally structure outgoing communication signals at this rate

Summary

Introduction

Many behaviors are organized into repetitive cycles. In active rodents, orofacial sensorimotor behaviors like sniffing, whisking, and head movements are organized into cycles with a characteristic frequency in the theta range ∼5–10 Hz (Welker, 1964; Macrides, 1975; Deschênes et al, 2012). This yields coordinated patterns of behavior, and coordinated activity in associated neural circuits (Kay, 2005; Grosmaitre et al, 2007; Cury and Uchida, 2010; Shusterman et al, 2011; Deschênes et al, 2012; Miura et al, 2012; Moore et al, 2013) Both hippocampal and cortical theta rhythms can transiently phase lock to motor theta rhythms during specific behaviors (Komisaruk, 1970; Macrides et al, 1982; Ganguly and Kleinfeld, 2004; Kay, 2005; Shusterman et al, 2011). Such structuring suggests that our understanding of each individual behavior can benefit from consideration of the broader behavioral context

Methods

Results

Conclusion