Distinct classes of low frequency ultrasonic vocalizations in rats during sexual interactions relate to different emotional states

Abstract

This study examined low-frequency ultrasonic vocalizations (lUSVs) in rats during two types of sexual interactions: postejaculatory interval (PEI) and barrier-noncontact (NC) test. We report distinct classes of lUSVs that can be assigned to different emotional states; relaxation vs. frustration. Totally flat, 22-kHz calls (Class A), were observed during the relaxation state following ejaculation; characterized by immobilization or grooming during the PEI. On the other hand, two-three component lUSVs (Class B) that start at a higher frequency (45-kHz: flat, upward or short signal) and then shift to 35-23-kHz (mostly to 28-23-kHz), correspond as we assume, to arousal and frustration-active states associated with sniffing a hole or exploration during the NC test. We suggest that momentary, abrupt decreases of arousal during the frustration state correspond to Class B lUSVs. The detailed spectral analysis of the high-frequency component of two-component lUSVs is crucial for establishing the relationship between such lUSVs and the corresponding behavior and emotional states. Our studies indicate that while the two-component Class B 22-kHz lUSVs may relate to the frustration state, a single component, flat, Class A lUSV relates to the relaxation state. The results of these studies support a notion that rats emit distinct vocalization patterns, reflecting their emotional states.

Biological Functions of Rat Ultrasonic Vocalizations, Arousal Mechanisms, and Call Initiation

“…Acoustic analysis of the postejaculatory of 22 kHz vocalizations emitted by males during sexual contacts, or intended contacts, revealed that the calls are heterogenous and consist of long flat 22 kHz calls (20–35 kHz range) during the postejaculatory period, and anther class of 22 kHz calls. The other class of calls has higher sound frequency (23–45 kHz range) and some modulated frequency components that were observed during encounters of males with a female in a cage with a physical, perforated barrier, where animals could not have physical contact [ 157 ]. This last precopulatory category of calls would be compatible with a negative state of frustration caused by the presence of an inaccessible female, and not as a social detachment function [ 157 ] (for more details, see Section 2.8 and Section 3.5 ).…”

“…Male rats emitted long 22 kHz vocalizations but with altered frequency structures (for acoustic details, see Section 2.5.2 , above) as compared to postejaculatory 22 kHz calls. These calls were associated with the exploration of holes in the barriers and were compatible with irritation and frustration [ 157 ]. These frustration calls were also observed in rat sexual encounters during unsuccessful mounting attempts or failed intromissions [ 148 ].…”

“…The emission of 22 kHz calls during withdrawal when the drug of abuse is not available, or during frustration caused by lack of availability and access to a receptive female, being separated from the male by a partition [ 157 ], may be interpreted as signals sent to other conspecifics, even if they might not be available or cannot help. These aversive situations and the resulting behavior have been explained as frustration-induced anxiety [ 337 ], and the anxiety is signaled to conspecifics.…”

The Sexual Motivation of Male Rats as a Tool in Animal Models of Human Health Disorders

“…An enhanced level of general arousal and sexual arousal before the termination of postejaculatory vocalizations can be distinguished by spectral analysis of postejaculatory calls. Before the termination of vocalizations, at the time as exploration or noncontact erection take place, some frequency modulations or a shift from about the 45-kHz to the 28-23-kHz band are more often detected, and these differ from the very flat 22-kHz frequency ultrasonic vocalizations at the beginning and middle of the postejaculatory period (Bialy et al, 2019).…”

“…Furthermore, such vocalizations are present only in a familiar environment, and cues that increase anxiety level (odor cues from unfamiliar males) significantly reduce such postejaculatory vocalization (Bialy et al, 2016). Moreover, the postejaculatory vocalizations are distinct from shorter low-frequency vocalizations that are produced by a male rat expressing a sexually related frustration state (Bialy et al, 2019). Table 1 summarizes the key components of rat sexual behavior with relevant parameters that describe specific aspects of the behavior (first column).…”