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Cited by 216Animal Vocal Communication and BehaviorMemory and Neural MechanismsPrimate Behavior and Ecology

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

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Kim, Eun Joo, Kim, Earnest S., Covey, Ellen, Kim, Jeansok J.·2010·PLoS ONE
DOI 10.1371/journal.pone.0015077PMC PMC2995742
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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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Figure 1 Social transmission of fear—experimental designs. (A) The sender (S) rats underwent 10 presentations of tone-footshock pairings (fear conditioned, SFC) while receiver (R) rats experienced either no footshock (naïve, RN) or 3 unsignaled footshocks (fear-experienced, RFE). Social transmission of fear was assessed by placing S and R rats together in a novel chamber and presenting the tone CS. (B) 22-kHz USV calls and spectrogram from a SFC rat.
Figure 1 Social transmission of fear—experimental designs. (A) The sender (S) rats underwent 10 presentations of tone-footshock pairings (fear conditioned, SFC) while receiver (R) rats experienced either no footshock (naïve, RN) or 3 unsignaled footshocks (fear-experienced, RFE). Social transmission of fear was assessed by placing S and R rats together in a novel chamber and presenting the tone CS. (B) 22-kHz USV calls and spectrogram from a SFC rat.CC BY · PubMed Central
Figure 2 Results from three groups of sender-receiver pairs (n = 16 rats/pair). fear-conditioned sender and naïve receiver (SFC-RN); fear-conditioned sender and fear-experienced receiver (SFC-RFE); and naïve sender and fear-experienced receiver (SN-RFE). (A–C) Mean (± SEM) percentage time spent emitting USV and displaying freezing by S and R rats during baseline and 8 min tone CS presentation. (D, E) Group differences in USV (F2,23 = 28.583, P<.0001) and freezing (F5,47 = 52.743, P<.0001) during the first 3-min period of the pair-testing (grey sections, A through C). *, ** and *** denote P<.05, P<.001 and P<.0001, respectively, Bonferroni test. (F) A significant correlation between RFE animals' USV onset latencies during 3 unsignaled footshocks on day 1 and the RFE animals' freezing levels during SFC-RFE pair-testing on day 2 (r = −.779, P = .02).
Figure 2 Results from three groups of sender-receiver pairs (n = 16 rats/pair). fear-conditioned sender and naïve receiver (SFC-RN); fear-conditioned sender and fear-experienced receiver (SFC-RFE); and naïve sender and fear-experienced receiver (SN-RFE). (A–C) Mean (± SEM) percentage time spent emitting USV and displaying freezing by S and R rats during baseline and 8 min tone CS presentation. (D, E) Group differences in USV (F2,23 = 28.583, P<.0001) and freezing (F5,47 = 52.743, P<.0001) during the first 3-min period of the pair-testing (grey sections, A through C). *, ** and *** denote P<.05, P<.001 and P<.0001, respectively, Bonferroni test. (F) A significant correlation between RFE animals' USV onset latencies during 3 unsignaled footshocks on day 1 and the RFE animals' freezing levels during SFC-RFE pair-testing on day 2 (r = −.779, P = .02).CC BY · PubMed Central
Figure 3 MGN lesion, MGN inactivation and social transmission of fear. (A) Photomicrograph and histological reconstruction of MGN lesions (solid and gray represent minimum and maximum extent of the lesions, respectively) and cannulae implantation (each dot represents the injection site in the MGN of the SFC (grey) - RMGN(LI)-FE (black) pair). (B, C) Mean percentage USV and freezing from SFC (n = 8) and MGN-lesioned receiver (RMGN(LS)-FE, n = 8) rats during the pair-testing. (D, E) Mean percentage USV and freezing from SFC (n = 7) and MGN-lidocaine receiver (RMGN(LI)-FE, n = 7) rats during the pair-testing. (F, G) Group differences in USV between SFC-RFE, SN-RFE, SFC-RMGN(LS)-FE, and SFC-RMGN(LI)-FE pairs (F 3,30 = 24.681, P<.0001) and freezing between fear-experienced receiver groups (F 3,30 = 5.770, P<.01) during the first 3-min period of the pair-testing (grey sections, B through E). * denotes P<.05 (Bonferroni test); ** denotes P<.001 compared to the other three pairs (Bonferroni test).
Figure 3 MGN lesion, MGN inactivation and social transmission of fear. (A) Photomicrograph and histological reconstruction of MGN lesions (solid and gray represent minimum and maximum extent of the lesions, respectively) and cannulae implantation (each dot represents the injection site in the MGN of the SFC (grey) - RMGN(LI)-FE (black) pair). (B, C) Mean percentage USV and freezing from SFC (n = 8) and MGN-lesioned receiver (RMGN(LS)-FE, n = 8) rats during the pair-testing. (D, E) Mean percentage USV and freezing from SFC (n = 7) and MGN-lidocaine receiver (RMGN(LI)-FE, n = 7) rats during the pair-testing. (F, G) Group differences in USV between SFC-RFE, SN-RFE, SFC-RMGN(LS)-FE, and SFC-RMGN(LI)-FE pairs (F 3,30 = 24.681, P<.0001) and freezing between fear-experienced receiver groups (F 3,30 = 5.770, P<.01) during the first 3-min period of the pair-testing (grey sections, B through E). * denotes P<.05 (Bonferroni test); ** denotes P<.001 compared to the other three pairs (Bonferroni test).CC BY · PubMed Central
Figure 4 A hypothesized model of auto-conditioning. (Left) The ‘receiver’ rat reflexively emits USV response during unsignaled footshock experience. The USV serves as an internally-generated CS that acquires associative strength (Δ) in the amygdala (AMG) by virtue of pairings with succeeding footshock US. (Right) During pair-testing, the USV generated by the ‘sender’ animal will function as an effective CS to the receiver animal, producing a conditioned fear response.
Figure 4 A hypothesized model of auto-conditioning. (Left) The ‘receiver’ rat reflexively emits USV response during unsignaled footshock experience. The USV serves as an internally-generated CS that acquires associative strength (Δ) in the amygdala (AMG) by virtue of pairings with succeeding footshock US. (Right) During pair-testing, the USV generated by the ‘sender’ animal will function as an effective CS to the receiver animal, producing a conditioned fear response.CC BY · PubMed Central

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Metadata

Authors
Kim, E. J., Kim, E. S., Covey, E., & Kim, J. J.
Affiliations
University of Washington (US)
Corresponding author
Kim, Jeansok J.
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2010-12-01
Volume
5
Issue
12
Pages
e15077
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0015077
PMC
PMC2995742
OpenAlex
W1982780621
Cited by
216
References
44
Citations by year
2026: 11 · 2025: 14 · 2024: 13 · 2023: 18 · 2022: 10 · 2021: 14 · 2020: 13 · 2019: 17 · 2018: 27 · 2017: 15 · 2016: 18 · 2015: 10 · 2014: 6 · 2013: 16 · 2012: 9
FWCI
6.59
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Digital Commons - George Fox University (George Fox University) (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
Funders
National Institute of Mental Health (MH64457, R01 MH64457, R01MH064457)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Vocal Communication and Behavior
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Primate Behavior and Ecology
Keywords
distress vocalizations, fear conditioning, freezing behavior, medial geniculate body, thalamus, conspecific communication, rats
MeSH terms
Anesthetics, Local, Animals, Animal Communication, Behavior, Animal, Conditioning, Classical, Fear, Freezing, Geniculate Bodies, Lidocaine, Male, Social Behavior, Thalamus, Ultrasonics, Vocalization, Animal, Rats

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