Emotional Vocalizations Alter Behaviors and Neurochemical Release into the Amygdala

Abstract

The basolateral amygdala (BLA), a brain center of emotional expression, contributes to acoustic communication by first interpreting the meaning of social sounds in the context of the listener s internal state, then organizing the appropriate behavioral responses. We propose that modulatory neurochemicals such as acetylcholine (ACh) and dopamine (DA) provide internal-state signals to the BLA while an animal listens to social vocalizations. We tested this in a vocal playback experiment wherein we sampled fluids within the BLA and observed behavioral responses of male and female mice while presenting highly affective vocal sequences associated with either mating or restraint behaviors. In male mice, playback of restraint vocalizations increased ACh release and decreased DA release, while playback of mating sequences evoked the opposite neurochemical release patterns. In non-estrus female mice, the ACh and DA release patterns to mating playback were similar to males. Estrous females, however, showed increased ACh, associated with vigilance, as well as increased DA, associated with reward-seeking. Across these groups, increased ACh concentration was correlated with an increase in defensive behavior. These neurochemical release patterns and several behavioral responses depended on prior experience with the mating and restraint behaviors. Our results support a model in which ACh and DA provide contextual information to sound-analyzing BLA neurons that modulates their output to downstream brain regions responsible for appropriate behavioral outcomes.

Hearing, touching, and multisensory integration during mate choice

“…Microdialysis in the basolateral amygdala (a projection target of the VTA) while presenting male and female mice with USVs from the opposite sex showed an increase in DA levels in both males and females (Ghasemahmad, 2020 ), indicating the overall incentive rewarding nature of USVs. There are also a few studies investigating the rewarding neural correlate of social touch (Sun et al, 2018 ; Elias and Abdus-Saboor, 2022 ).…”

Emotional Vocalizations Alter Behaviors and Neurochemical Release into the Amygdala

“…To study how vocalizations affect behaviors and release of neurochemicals within BLA, we first developed highly salient vocal stimuli associated with appetitive (mating) and aversive (restraint) behaviors of CBA/CaJ mice. From more intense, mating-related interactions between adult male and female mice that included female head-sniffing and attempted or actual mounting (Gaub et al, 2016 ;Ghasemahmad, 2020 , see Materials and Methods), we selected several sequences of vocalizations to form a 20-minute mating vocal stimulus. These sequences included ultrasonic vocalizations (USVs) with harmonics, steps, and complex structure, mostly emitted by males, and low frequency harmonic calls (LFHs) emitted by females (Fig.…”

“…These sequences included ultrasonic vocalizations (USVs) with harmonics, steps, and complex structure, mostly emitted by males, and low frequency harmonic calls (LFHs) emitted by females (Fig. 1A,C ) (Finton et al, 2017 ;Gaub et al, 2016 ;Ghasemahmad, 2020 ;Hanson & Hurley, 2012 ). During short periods of restraint, mice produce distinctive mid-frequency vocalizations (MFVs) that are associated with anxiety-related behaviors and increased release of the stress hormone corticosterone (Dornellas et al, 2021 ;.…”

“…Each block was composed of a set of vocal sequence exemplars that alternated with an equal duration of background sound ("Silence") associated with the preceding exemplar. The exemplars were recorded during mating interactions and restraint, and selected based on high SNR, correspondence with behavioral category by video analysis, and representation of the spectrotemporal features of vocalizations emitted during mating and restraint (Ghasemahmad, 2020 ;. Mating stimulus blocks contained five exemplars of vocal sequences emitted during mating interactions.…”

Early-life stress affects Mongolian gerbil interactions with conspecific vocalizations in a sex-specific manner

“…Ultrasonic vocalizations emitted during friendly greetings and sexual encounters cause an increase in risk-assessment behaviors in female, but not male mice, suggesting that the sexes perceive the valence (i.e., pleasantness or unpleasantness) of this type of vocalization differently. However, playback of a distress call caused both male and female mice to increase risk-assessment behaviors ( Ghasemahmad et al, 2022 ). Thus, the sexes perceive the emotional content of some vocalizations differently.…”