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      Playback of Alarm and Appetitive Calls Differentially Impacts Vocal, Heart-Rate, and Motor Response in Rats

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          Summary

          Our rudimentary knowledge about rat intraspecific vocal system of information exchange is limited by experimental models of communication. Rats emit 50-kHz ultrasonic vocalizations in appetitive states and 22-kHz ones in aversive states. Both affective states influence heart rate. We propose a behavioral model employing exposure to pre-recorded playbacks in home-cage-like conditions. Fifty-kHz playbacks elicited the most vocalizations (>60 calls per minute, mostly of 50-kHz type), increased heart rate, and locomotor activity. In contrast, 22-kHz playback led to abrupt decrease in heart rate and locomotor activity. Observed effects were more pronounced in singly housed rats compared with the paired housed group; they were stronger when evoked by natural playback than by corresponding artificial tones. Finally, we also observed correlations between the number of vocalizations, heart rate levels, and locomotor activity. The correlations were especially strong in response to 50-kHz playback.

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          Highlights

          • Rats vocalized abundantly when exposed to recorded ultrasonic playback

          • Playback of appetitive calls caused an increase in heart rate

          • Playback of alarm/aversive calls caused a decrease in heart rate

          • Singly housed rats exhibited more vocalizations and higher heart rate

          Abstract

          Biological Sciences; Animals; Ethology

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          Most cited references64

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          The polyvagal perspective.

          The polyvagal theory introduced a new perspective relating autonomic function to behavior, that included an appreciation of the autonomic nervous system as a "system," the identification of neural circuits involved in the regulation of autonomic state, and an interpretation of autonomic reactivity as adaptive within the context of the phylogeny of the vertebrate autonomic nervous system. The paper has two objectives: first, to provide an explicit statement of the theory; and second, to introduce the features of a polyvagal perspective. The polyvagal perspective emphasizes how an understanding of neurophysiological mechanisms and phylogenetic shifts in neural regulation leads to different questions, paradigms, explanations, and conclusions regarding autonomic function in biobehavioral processes than peripheral models. Foremost, the polyvagal perspective emphasizes the importance of phylogenetic changes in the neural structures regulating the autonomic nervous system and how these phylogenetic shifts provide insights into the adaptive function and the neural regulation of the two vagal systems.
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            Natural selective attention: orienting and emotion.

            The foundations of orienting and attention are hypothesized to stem from activation of defensive and appetitive motivational systems that evolved to protect and sustain the life of the individual. Motivational activation initiates a cascade of perceptual and motor processes that facilitate the selection of appropriate behavior. Among these are detection of significance, indexed by a late centro-parietal positivity in the event-related potential, enhanced perceptual processing, indexed by a initial cardiac deceleration, and preparation for action, indexed by electrodermal changes. Data exploring the role of stimulus novelty and significance in orienting are presented that indicate different components of the orienting response habituate at different rates. Taken together, it is suggested that orienting is mediated by activation of fundamental motivational systems that have evolved to support survival.
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              Orienting in a defensive world: mammalian modifications of our evolutionary heritage. A Polyvagal Theory.

              The vagus, the 10th cranial nerve, contains pathways that contribute to the regulation of the internal viscera, including the heart. Vagal efferent fibers do not originate in a common brainstem structure. The Polyvagal Theory is introduced to explain the different functions of the two primary medullary source nuclei of the vagus: the nucleus ambiguus (NA) and the dorsal motor nucleus (DMNX). Although vagal pathways from both nuclei terminate on the sinoatrial node, it is argued that the fibers originating in NA are uniquely responsible for respiratory sinus arrhythmia (RSA). Divergent shifts in RSA and heart rate are explained by independent actions of DMNX and NA. The theory emphasizes a phylogenetic perspective and speculates that mammalian, but not reptilian, brainstem organization is characterized by a ventral vagal complex (including NA) related to processes associated with attention, motion, emotion, and communication. Various clinical disorders, such as sudden infant death syndrome and asthma, may be related to the competition between DMNX and NA.
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                Author and article information

                Contributors
                Journal
                iScience
                iScience
                iScience
                Elsevier
                2589-0042
                19 September 2020
                23 October 2020
                19 September 2020
                : 23
                : 10
                : 101577
                Affiliations
                [1 ]Behavior and Metabolism Research Laboratory, Mossakowski Medical Research Centre, Polish Academy of Sciences, 5 Pawinskiego St, 02-106 Warsaw, Poland
                [2 ]Laboratory of Animal Models, Nencki Institute of Experimental Biology, Polish Academy of Sciences, 3 Pasteur St, 02-093 Warsaw, Poland
                Author notes
                []Corresponding author rfilipkowski@ 123456imdik.pan.pl
                [3]

                Lead Contact

                Article
                S2589-0042(20)30769-0 101577
                10.1016/j.isci.2020.101577
                7553343
                33083743
                67a95b9b-6e88-4181-9099-5af9319921d4
                © 2020 The Author(s)

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                : 19 May 2020
                : 7 August 2020
                : 15 September 2020
                Categories
                Article

                biological sciences,animals,ethology
                biological sciences, animals, ethology

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