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      Social Transmission of Fear in Rats: The Role of 22-kHz Ultrasonic Distress Vocalization

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          Abstract

          Background

          Social alarm calls alert animals to potential danger and thereby promote group survival. Adult laboratory rats in distress emit 22-kHz ultrasonic vocalization (USV) calls, but the question of whether these USV calls directly elicit defensive behavior in conspecifics is unresolved.

          Methodology/Principal Findings

          The present study investigated, in pair-housed male rats, whether and how the conditioned fear-induced 22-kHz USVs emitted by the ‘sender’ animal affect the behavior of its partner, the ‘receiver’ animal, when both are placed together in a novel chamber. The sender rats’ conditioned fear responses evoked significant freezing (an overt evidence of fear) in receiver rats that had previously experienced an aversive event but not in naïve receiver rats. Permanent lesions and reversible inactivations of the medial geniculate nucleus (MGN) of the thalamus effectively blocked the receivers’ freeezing response to the senders' conditioned fear responses, and this occurred in absence of lesions/inactivations impeding the receiver animals' ability to freeze and emit 22-kHz USVs to the aversive event per se.

          Conclusions/Significance

          These results—that prior experience of fear and intact auditory system are required for receiver rats to respond to their conspecifics' conditioned fear responses—indicate that the 22-kHz USV is the main factor for social transmission of fear and that learning plays a crucial role in the development of social signaling of danger by USVs.

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          Most cited references29

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          Social learning of fear.

          Research across species highlights the critical role of the amygdala in fear conditioning. However, fear conditioning, involving direct aversive experience, is only one means by which fears can be acquired. Exploiting aversive experiences of other individuals through social fear learning is less risky. Behavioral research provides important insights into the workings of social fear learning, and the neural mechanisms are beginning to be understood. We review research suggesting that an amygdala-centered model of fear conditioning can help to explain social learning of fear through observation and instruction. We also describe how observational and instructed fear is distinguished by involvement of additional neural systems implicated in social-emotional behavior, language and explicit memory, and propose a modified conditioning model to account for social fear learning. A better understanding of social fear learning promotes integration of biological principles of learning with cultural evolution.
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            Ultrasonic vocalizations as indices of affective states in rats.

            Adult rats spontaneously vocalize in ultrasonic frequencies. Although these ultrasonic vocalizations (USVs) have been described as by-products of locomotor activity or social signals, accumulating evidence suggests that they may also index anticipatory affective states. Converging ethological, pharmacological, and brain stimulation research indicates that whereas long low-frequency (> 0.3-s, approximately 22-kHz) USVs occur during anticipation of punishment or avoidance behavior, short, high-frequency (< 0.3-s, approximately 50-kHz) USVs typically occur during anticipation of reward or approach behavior. Thus, long 22-kHz USVs may index a state of negative activation, whereas short, 50-kHz USVs may instead index a state of positive activation. This hypothesis has theoretical implications for understanding the brain circuitry underlying mammalian affective states and clinical applicability for modeling hedonic properties of different psychotropic compounds.
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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
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2010
                1 December 2010
                : 5
                : 12
                : e15077
                Affiliations
                [1 ]Department of Psychology, University of Washington, Seattle, Washington, United States of America
                [2 ]Program in Neurobiology and Behavior, University of Washington, Seattle, Washington, United States of America
                Université Pierre et Marie Curie, France
                Author notes

                Conceived and designed the experiments: EJK EK EC JJK. Performed the experiments: EJK EK. Analyzed the data: EJK EK. Contributed reagents/materials/analysis tools: EJK EK. Wrote the paper: EJK EK EC JJK.

                Article
                PONE-D-10-02272
                10.1371/journal.pone.0015077
                2995742
                21152023
                9ae82b55-9dae-4539-bbec-09b649e80d2a
                Kim et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 21 September 2010
                : 18 October 2010
                Page count
                Pages: 8
                Categories
                Research Article
                Biology
                Neuroscience
                Sensory Systems
                Auditory System
                Animal Cognition
                Behavioral Neuroscience
                Learning and Memory
                Systems Biology
                Zoology
                Animal Behavior
                Medicine
                Mental Health
                Psychology
                Psychological Defense Mechanisms
                Social Psychology
                Social and Behavioral Sciences
                Psychology
                Behavior
                Emotions
                Vigilance
                Experimental Psychology

                Uncategorized
                Uncategorized

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