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      Editorial: Acoustic communication analysis for understanding animal behavior

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          Abstract

          Animals of most species emit vocalizations to communicate each other and to convey their emotional states. Intraspecific communication consists of the transfer of information from one or more animals [sender(s)] to one or more conspecifics [receiver(s)] in order to affect the current or future behaviors of the receiver(s). Vocal communication may occur both in the audible and ultrasonic frequency ranges and it is subjected by a complex brain modulation involving multiple areas and neural circuits. Communication is also impaired in a variety of pathological conditions, such as neurodevelopmental disorders (autism spectrum disorders, ASD, in particular), and these alterations can be tackled by pharmacological therapeutic strategies that have been proposed in several preclinical studies. One of the most ambitious challenges of animal vocal communication concerns the study of ultrasonic vocalizations (USVs) in rodents and it consists of fully automatizing the procedures for spectrographic USV analysis. This would allow bypassing the operator-dependent and time-consuming analyses that are necessary for the quantitative and qualitative studies of USVs. This challenge was successfully faced by de Chaumont et al. in this special issue, as they developed one open-access software to automatically study mouse USVs. Their system also allowed coupling the spectrographic analysis of USVs with the automatic labeling of several behaviors scored over a long time-period (i.e., 3 days), thus providing an additional evaluation of the behavioral value of USVs in laboratory mice. The method was validated in C57BL/6J mice and also in mutants lacking the Shank3 gene, i.e., a mouse model of autism, in both sexes and at multiple ages. Also Goussha et al. developed a new software, the HybridMouse, that is an audio analysis tool for automatically identifying, labeling, and extracting recorded USVs. The methodological challenges of automatic processing a large amount of data from audio files does not concern only mouse ultrasonic communication. Here Marck et al. developed an automatic system based on audio signal processing algorithms and deep learning and applied to the vocal repertoire of the White Spectacled Bulbul (Pycnonotus xanthopygos), a bird species with a complex vocal communication system. Other modern computational methods for bioacoustics have been developed for the analysis of vocal communication in several animal species (including fish, amphibians, and insects), as described in detail in the review by Sainburg and Gentner. Beside the analysis of the vocalizations emitted by the sender, the response of the receiving animal to vocalizations deserves to be studied. In rats, two main types of vocalizations are typically distinguished (Brudzynski, 2013; Wöhr and Schwarting, 2013): vocalizations with frequencies around 22 kHz, that are referred to as aversive or distress calls, presumably representing a negative affective state (Blanchard et al., 1991; Fendt et al., 2018), and vocalizations with frequencies around 50 kHz, that are thought to represent a positive affective state usually emitted during appetitive situations like play or mating (Knutson et al., 1998; Panksepp, 2005). In this context, Berz et al. investigated the emission of USVs in response to the playback of natural 50 kHz USVs in male juvenile rats of different strains. Their data demonstrated that most rats emitted response calls specifically linked to 50-kHz USV playback and these response calls were mostly characterized by a frequency range of 20–32 kHz and a mean duration of approximately 300 ms in all rat strains. The possible function of these type of calls has yet to be clarified, although it was unaffected by the pharmacological blockade of dopamine D2 receptors by haloperidol administration. In rats, the emission of USVs can be also promoted by operant conditioning during multiple weeks: this approach was employed in the study by Johnson et al. where a semi-automated method for training rats to increase their rate of USV production was introduced. The impact of social context on animal communication is an issue of critical relevance that is far from being fully elucidated. Here, Warren et al. studied the ontogeny of prairie vole pup ultrasonic vocalizations when isolated or when the mother was present, but physically unattainable. They demonstrated a developmental maturation in all features of pup vocalizations and the impact of the different social contexts in modifying vocal emission. Capas-Peneda et al. reviewed instead the role of mouse USVs in the reproductive context; indeed, they summarized the most recent evidence demonstrating that USVs have an important role in parental cooperation, inducing both maternal and paternal behaviors. Bouguiyoud et al. investigated the effects of visual deprivation in acoustic communication and social behaviors using a mouse model of congenital blindness. They demonstrated here that congenital visual deprivation had no effect on the number of USVs emitted in pups and juveniles, but affected the USV emission in adult males and the social behaviors in juvenile and adult mice. The role of social isolation on adult USVs and social behaviors was instead assessed in both male and female mice by Premoli et al. Their study contributed to provide new guidelines for assessing ultrasonic communication in inbred mice, demonstrating also several sex differences in ultrasonic communication and social behaviors that were mostly unaffected by pre-testing social isolation. Finally, another interesting aspect that has been investigated in a study included in this special issue concerns the molecular mechanisms underlying vocal communication. In particular, Aamodt and White examined whether microRNA-128 is behaviorally regulated in Area X (the striatopallidal song control nucleus) in juvenile zebra finches and found that its levels decline with singing. Furthermore, they demonstrated that inhibition of miR-128 in young birds enhanced the organization of learned vocal sequences, thus suggesting an important role for miR-128 in vocal communication and as a potential therapeutic target for autism spectrum disorders. Author contributions All authors listed have made a substantial, direct, and intellectual contribution to the work and approved it for publication. Funding SP received funding from Bordeaux University, CNRS, Association Autour de Williams and Fondation pour l'Audition (FPA-RD-2020-8). SAB received funding from the University of Brescia. Conflict of interest The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Publisher's note All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

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          Ethotransmission: communication of emotional states through ultrasonic vocalization in rats.

          Adult rats emit two categories of ultrasonic vocalizations, 22 kHz calls and 50 kHz calls. These vocalizations communicate animal's emotional state to other members of the social group. Production of social vocalizations is an evolutionary old activity in vertebrates, and is regulated by well-preserved brain circuitries. The 22 kHz calls express negative, aversive state and are initiated by activity of the mesolimbic cholinergic system originating from laterodorsal tegmental nucleus. The 50 kHz calls express positive, appetitive state and are initiated by activity of the mesolimbic dopaminergic system originating from the ventral tegmental area. The 22 kHz calls serve as warning and alarm calls, while the 50 kHz calls serve as affiliative and social-cooperating calls. These specie-specific vocalizations play role of ethological transmitters, termed ethotransmitters, that is, they are species-specific signals that are selectively recognized by receivers and have capability of changing emotional state of the receivers. Copyright © 2013 Elsevier Ltd. All rights reserved.
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            Affective communication in rodents: ultrasonic vocalizations as a tool for research on emotion and motivation.

            Mice and rats emit and perceive calls in the ultrasonic range, i.e., above the human hearing threshold of about 20 kHz: so-called ultrasonic vocalizations (USV). Juvenile and adult rats emit 22-kHz USV in aversive situations, such as predator exposure and fighting or during drug withdrawal, whereas 50-kHz USV occur in appetitive situations, such as rough-and-tumble play and mating or in response to drugs of abuse, e.g., amphetamine. Aversive 22-kHz USV and appetitive 50-kHz USV serve distinct communicative functions. Whereas 22-kHz USV induce freezing behavior in the receiver, 50-kHz USV lead to social approach behavior. These opposite behavioral responses are paralleled by distinct patterns of brain activation. Freezing behavior in response to 22-kHz USV is paralleled by increased neuronal activity in brain areas regulating fear and anxiety, such as the amygdala and periaqueductal gray, whereas social approach behavior elicited by 50-kHz USV is accompanied by reduced activity levels in the amygdala but enhanced activity in the nucleus accumbens, a brain area implicated in reward processing. These opposing behavioral responses, together with distinct patterns of brain activation, particularly the bidirectional tonic activation or deactivation of the amygdala elicited by 22-kHz and 50-kHz USV, respectively, concur with a wealth of behavioral and neuroimaging studies in humans involving emotionally salient stimuli, such as fearful and happy facial expressions. Affective ultrasonic communication therefore offers a translational tool for studying the neurobiology underlying socio-affective communication. This is particularly relevant for rodent models of neurodevelopmental disorders characterized by social and communication deficits, such as autism and schizophrenia.
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              Twenty-two kHz alarm cries to presentation of a predator, by laboratory rats living in visible burrow systems.

              When a cat was presented to groups of 3 male and 2 female laboratory rats in the open area of a visible burrow system, the rats retreated to the burrow system and showed high levels of 18-24 kHz ultrasonic cries during the cat presentation and for 30 min following removal of the cat. Latency to make ultrasonic vocalizations, durations of these vocalizations, and duration in the burrow systems were all strikingly and reliably different during and after cat exposure in comparison to similar periods with a control (stuffed cat toy) stimulus. However, when individual rats were exposed to a cat in an open area of similar size, ultrasonic cry production was minimal. Also rats exposed individually to a cat in an apparatus providing an escape chamber similarly showed no ultrasonic cries, indicating that concealment per se is not a sufficient condition for their appearance. These results suggest that the production of ultrasonic vocalizations during and after exposure to a predator is greatly facilitated by the presence of familiar conspecifics, and may serve as alarm cries. While the alarm cry hypothesis also suggests a possible function for 18-24 kHz ultrasounds in the context of copulation and intraspecies aggression, the sonographic and functional relationships among the cries emitted in these different situations remain to be analyzed.
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                Author and article information

                Contributors
                Journal
                Front Behav Neurosci
                Front Behav Neurosci
                Front. Behav. Neurosci.
                Frontiers in Behavioral Neuroscience
                Frontiers Media S.A.
                1662-5153
                03 August 2022
                2022
                : 16
                : 991573
                Affiliations
                [1] 1Department of Molecular and Translational Medicine, University of Brescia , Brescia, Italy
                [2] 2Institut de Neurosciences Cognitives et Intégratives d'Aquitaine (INCIA), University of Bordeaux, CNRS, UMR 5287 , Bordeaux, France
                Author notes

                Edited and reviewed by: Walter Adriani, National Institute of Health (ISS), Italy

                *Correspondence: Sara Anna Bonini sara.bonini@ 123456unibs.it

                This article was submitted to Individual and Social Behaviors, a section of the journal Frontiers in Behavioral Neuroscience

                Article
                10.3389/fnbeh.2022.991573
                9382230
                3f64340b-ec45-441a-8e9c-2e5b9ebcdbe8
                Copyright © 2022 Bonini and Pietropaolo.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 11 July 2022
                : 21 July 2022
                Page count
                Figures: 0, Tables: 0, Equations: 0, References: 6, Pages: 03, Words: 1490
                Categories
                Behavioral Neuroscience
                Editorial

                Neurosciences
                acoustic communication,ultrasonic vocalizations,animal behavior,social context,communication analysis,automatic usvs analysis

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