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1. Postweaning Isolation Alters the Responses of Auditory Neurons to Serotonergic Modulation

   https://doi.org/10.1093/icb/icab051  

   Davis, Sarah E ; Sansone, Jack M ; Hurley, Laura M ( May 2021 , Integrative and Comparative Biology)

   null (Ed.)

   Abstract Juvenile social experience, such as social isolation, has profound effects on communicative behavior, including signal production and reception. In the current study, we explored responsiveness to the neuromodulator serotonin as a potential mechanistic link between early life social isolation and auditory processing. The serotonergic system is sensitive to social isolation in many brain regions including the inferior colliculus (IC), an auditory midbrain nucleus. We investigated the effects of social experience on serotonergic responsiveness by measuring cFos, an immediate early gene product, in the IC of female mice. Serotonin was manipulated pharmacologically by administering fenfluramine, pCPA, or saline to mice that had undergone an extreme dichotomy in social experience after weaning: being housed in social groups versus individually. These mice were exposed to a 60-min recording of vocalizations from an opposite-sex interaction and perfused. Using immunohistochemistry, we measured the density of cFos-positive (cFos+) nuclei in the major subdivisions of the IC. Housing condition, drug treatment, and IC subregion all had a significant effect on cFos+ density. The central IC showed the highest density of cFos+ cells and also the most pronounced effects of housing condition and drug treatment. In the central IC, cFos+ density was higher following fenfluramine treatment than saline, and lower following pCPA treatment than fenfluramine. Individually housed mice showed a higher cFos+ density than socially housed mice in both of the pharmacological treatment groups, but not in the saline group. Drug treatment but not housing condition had strong effects on the behaviors of grooming, digging, rearing, and movement. Once the effects of drug condition were controlled, there were no across-individual correlations between cFos+ densities and behaviors. These findings suggest that the responses of auditory neurons to neuromodulation by serotonin are influenced by early life experience. 

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2. Sound‐induced monoaminergic turnover in the auditory forebrain depends on endocrine state in a seasonally‐breeding songbird

   https://doi.org/10.1111/jne.12606  

   Rodríguez‐Saltos, C. A. ; Lyons, S. M. ; Sockman, K. W. ; Maney, D. L. ( June 2018 , Journal of Neuroendocrinology)

   Sensory responses to courtship signals can be altered by reproductive hormones. In seasonally‐breeding female songbirds, for example, sound‐induced immediate early gene expression in the auditory pathway is selective for male song over behaviourally irrelevant sounds only when plasma oestradiol reaches breeding‐like levels. This selectivity has been hypothesised to be mediated by the release of monoaminergic neuromodulators in the auditory pathway. We previously showed that in oestrogen‐primed female white‐throated sparrows, exposure to male song induced dopamine and serotonin release in auditory regions. To mediate hormone‐dependent selectivity, this release must be (i) selective for song and (ii) modulated by endocrine state. Therefore, in the present study, we addressed both questions by conducting playbacks of song or a control sound to females in a breeding‐like or a nonbreeding endocrine state. We then used high‐performance liquid chromatography to measure turnover of dopamine, norepinephrine and serotonin in the auditory midbrain and forebrain. We found that sound‐induced turnover of dopamine and serotonin depended on endocrine state; hearing sound increased turnover in the auditory forebrain only in the birds in a breeding‐like endocrine state. Contrary to our expectations, these increases occurred in response to either song or artificial tones; in other words, they were not selective for song. The selectivity of sound‐induced monoamine release was thus strikingly different from that of immediate early gene responses described in previous studies. We did, however, find that constitutive monoamine release was altered by endocrine state; irrespective of whether the birds heard sound or not, turnover of serotonin in the auditory forebrain was higher in a breeding‐like state than in a nonbreeding endocrine state. The results of the present study suggest that dopaminergic and serotonergic responses to song and other sounds, as well as serotonergic tone in auditory areas, could be seasonally modulated.

    

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3. Playback of broadband vocalizations of female mice suppresses male ultrasonic calls

   https://doi.org/10.1371/journal.pone.0273742  

   Hood, Kayleigh E. ; Long, Eden ; Navarro, Eric ; Hurley, Laura M. ( January 2023 , PLOS ONE)

   Coleman, Melissa J. (Ed.)

   Although male vocalizations during opposite- sex interaction have been heavily studied as sexually selected signals, the understanding of the roles of female vocal signals produced in this context is more limited. During intersexual interactions between mice, males produce a majority of ultrasonic vocalizations (USVs), while females produce a majority of human-audible squeaks, also called broadband vocalizations (BBVs). BBVs may be produced in conjunction with defensive aggression, making it difficult to assess whether males respond to BBVs themselves. To assess the direct effect of BBVs on male behavior, we used a split-cage paradigm in which high rates of male USVs were elicited by female presence on the other side of a barrier, but which precluded extensive male-female contact and the spontaneous production of BBVs. In this paradigm, playback of female BBVs decreased USV production, which recovered after the playback period. Trials in which female vocalizations were prevented by the use of female bedding alone or of anesthetized females as stimuli also showed a decrease in response to BBV playback. No non-vocal behaviors declined during playback, although digging behavior increased. Similar to BBVs, WNs also robustly suppressed USV production, albeit to a significantly larger extent. USVs suppression had two distinct temporal components. When grouped in 5-second bins, USVs interleaved with bursts of stimulus BBVs. USV suppression also adapted to BBV playback on the order of minutes. Adaptation occurred more rapidly in males that were housed individually as opposed to socially for a week prior to testing, suggesting that the adaptation trajectory is sensitive to social experience. These findings suggest the possibility that vocal interaction between male and female mice, with males suppressing USVs in response to BBVs, may influence the dynamics of communicative behavior. 

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4. Social experience and pheromone receptor activity reprogram gene expression in sensory neurons

   https://doi.org/10.1093/g3journal/jkad072  

   Deanhardt, Bryson ; Duan, Qichen ; Du, Chengcheng ; Soeder, Charles ; Morlote, Alec ; Garg, Deeya ; Saha, Aishani ; Jones, Corbin D ; Volkan, Pelin Cayirlioglu ( March 2023 , G3 Genes|Genomes|Genetics)

   Ramaswami, Mani (Ed.)

   Abstract Social experience and pheromone signaling in olfactory neurons affect neuronal responses and male courtship behaviors in Drosophila. We previously showed that social experience and pheromone signaling modulate chromatin around behavioral switch gene fruitless, which encodes a transcription factor necessary and sufficient for male sexual behaviors. Fruitless drives social experience-dependent modulation of courtship behaviors and physiological sensory neuron responses to pheromone; however, the molecular mechanisms underlying this modulation of neural responses remain less clear. To identify the molecular mechanisms driving social experience-dependent changes in neuronal responses, we performed RNA-seq from antennal samples of mutants in pheromone receptors and fruitless, as well as grouped or isolated wild-type males. Genes affecting neuronal physiology and function, such as neurotransmitter receptors, ion channels, ion and membrane transporters, and odorant binding proteins are differentially regulated by social context and pheromone signaling. While we found that loss of pheromone detection only has small effects on differential promoter and exon usage within fruitless gene, many of the differentially regulated genes have Fruitless binding sites or are bound by Fruitless in the nervous system. Recent studies showed that social experience and juvenile hormone signaling co-regulate fruitless chromatin to modify pheromone responses in olfactory neurons. Interestingly, genes involved in juvenile hormone metabolism are also misregulated in different social contexts and mutant backgrounds. Our results suggest that modulation of neuronal activity and behaviors in response to social experience and pheromone signaling likely arise due to large-scale changes in transcriptional programs for neuronal function downstream of behavioral switch gene function. 

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5. Versatility in a loud call: Dual affiliative and agonistic functions in the blue monkey boom

   https://doi.org/10.1111/eth.12955  

   Fuller, James L. ; Cords, Marina ; Koenig, ed., Walter ( October 2019 , Ethology)

   To investigate the selective agents that shape signals, we examined function (adaptive benefit to signaler) in theboomloud call by male blue monkeys. Using natural observation and playbacks in a wild population in Kenya, we characterizedboomfunction from conspecifics' behavioral responses and also variation in call usage relating to context and reproductive season.Boomsoccurred in several contexts and after varied stimuli, including falling branches, yet were strongly associated with intragroup activity and, in particular, affiliative interactions between callers and females. Males produced moreboomsduring the mating season and, congruently, when more females in their groups were sexually active. After hearingbooms, compared to no call, females spent more time near groupmates and the caller and were more likely to approach and have mating interactions with him. Males tended to move away after hearing aboom. In the aggregate, results indicate thatboomsachieve multiple functions relating to facilitating group cohesion, affiliative interactions, and mating opportunities, while also repelling rival males. An observed association with falling branches is puzzlingly distinct from these social functions. We explore the hypothesis thatboomsenable affiliative encounters by acting as signals of benign intent, and discuss the functional versatility of signals perceived by multiple receivers that vary in age, sex, and relationship to signalers.

    

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