Studying Socio‐Affective Communication in Rats through Playback of Ultrasonic Vocalizations

Wöhr, Markus; Seffer, Dominik; Schwarting, Rainer K.W.

doi:10.1002/cpns.7

Cited by 31 publications

(29 citation statements)

References 38 publications

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“…In contrast to the wildtype, Ube3a m−/p+ subjects failed to show a strong, sustained response to hearing the cue and only spent significantly more time on the proximal arms during the time period the audio cue was "on". This was an unusual display of social behavior as there should be (1) a clear behavioral preference for the proximal versus distal arms and (2) sustained attempts to locate the source of the emission, as previously reported across genetic models and groups 12,15,18,20,39 . The behavioral alterations displayed by Ube3a m−/p+ rats in response to pro-social 50-kHz USV were clear and substantially more prominent than the social communication deficits seen in other recently developed rat models relevant to autism, including Shank3 15 and Cacna1c 18,19 .…”

Section: Discussionsupporting

confidence: 60%

“…On PND 4,6,8,10,12,14,16, and 18, isolation-induced USV were collected for 3 min as previously described 15 . Each pup, randomly selected from the nest, was placed in a small container with clean bedding and calls were recorded within a sound-attenuating chamber using an ultrasonic microphone and Avisoft-RECORDER software (Avisoft Bioacoustics, Glienicke, Germany).…”

Section: Cohort 1 Behavioral Assays Pup Ultrasonic Vocalizations (Usv)mentioning

confidence: 99%

“…One prominent example is the less complex acoustic communication system in the mouse. Rats emit uniquely detectable ultrasonic vocalizations (USV) that serve as situation-dependent evolved signals and that accomplish important communicative functions as alarm or social contact calls [10][11][12] . Another advantage of a rat model is the ability to utilize advanced cognitive tests for measuring learning and memory.…”

Section: Introductionmentioning

confidence: 99%

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Translational outcomes in a full gene deletion of ubiquitin protein ligase E3A rat model of Angelman syndrome

et al. 2020

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Angelman syndrome (AS) is a rare neurodevelopmental disorder characterized by developmental delay, impaired communication, motor deficits and ataxia, intellectual disabilities, microcephaly, and seizures. The genetic cause of AS is the loss of expression of UBE3A (ubiquitin protein ligase E6-AP) in the brain, typically due to a deletion of the maternal 15q11-q13 region. Previous studies have been performed using a mouse model with a deletion of a single exon of Ube3a. Since three splice variants of Ube3a exist, this has led to a lack of consistent reports and the theory that perhaps not all mouse studies were assessing the effects of an absence of all functional UBE3A. Herein, we report the generation and functional characterization of a novel model of Angelman syndrome by deleting the entire Ube3a gene in the rat. We validated that this resulted in the first comprehensive gene deletion rodent model. Ultrasonic vocalizations from newborn Ube3a m−/p+ were reduced in the maternal inherited deletion group with no observable change in the Ube3a m+/p− paternal transmission cohort. We also discovered Ube3a m−/p+ exhibited delayed reflex development, motor deficits in rearing and fine motor skills, aberrant social communication, and impaired touchscreen learning and memory in young adults. These behavioral deficits were large in effect size and easily apparent in the larger rodent species. Low social communication was detected using a playback task that is unique to rats. Structural imaging illustrated decreased brain volume in Ube3a m−/p+ and a variety of intriguing neuroanatomical phenotypes while Ube3a m+/p− did not exhibit altered neuroanatomy. Our report identifies, for the first time, unique AS relevant functional phenotypes and anatomical markers as preclinical outcomes to test various strategies for gene and molecular therapies in AS.

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Section: Discussionsupporting

confidence: 60%

Section: Cohort 1 Behavioral Assays Pup Ultrasonic Vocalizations (Usv)mentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Translational outcomes in a full gene deletion of ubiquitin protein ligase E3A rat model of Angelman syndrome

et al. 2020

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“…If we then consider the apparently rewarding properties of the 50-kHz USV and the ability of other rewards to reduce cocaine intake, it is not surprising that also the 50-kHz calls were able to do so. It was also well documented that 50-kHz USV serve an important affiliative pro-social function (Wöhr et al 2016; Wöhr & Schwarting 2017). Consequently it could be possible that rats decreased their cocaine intake because they were approaching the loudspeaker and looking for a peer.…”

Section: Discussionmentioning

confidence: 96%

Subthalamic nucleus mediates the modulation on cocaine self-administration induced by ultrasonic 3 vocalizations playback in rats

Montanari

Giorla

Pelloux

et al. 2018

Preprint

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1Drug intake is known to be under the influence of social context. We have recently shown that 2 presence of a peer influences drug intake in both rats and humans. Whether or not social acoustic 3 communications between the peers play a role during cocaine or sucrose self-administration (SA) 4 was investigated here, using playback of ultrasonic vocalizations (USV) at 50-and 22-kHz, 5 conveying respectively positive and negative internal affective states in adult rats. To assess the 6 neurobiological substrate of a potential USV influence on drug and food intake, we tested the 7 effects of subthalamic nucleus (STN) lesions, given its role in emotional and motivational 8 processes. In sham-control rats, playback of USV associated with positive affective states induced 9 long-term decreased cocaine consumption, while USV associated with negative affective states 10 induced short-term increase. Interestingly, no effect of USV playback was observed on sucrose 11 intake, whatever the frequency. STN lesions abolished the influence of USV on cocaine intake, 12 highlighting the influence of STN in emotional processes induced by USV emitted by a peer. These 13 results show how acoustic social communication is important to regulate drug intake in rats and 14 how STN modulation could interfere with addiction processes.15

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“…This could be due to multiple reasons including the CPF-exposed rats not being able to localize the sound source, the CPF-exposed rats having less dopaminergic-mediated motivation for social reward, and/or the CPFexposed rats not being able to understand the communicative function of the pro-social 50-kHz USV. Differentiating between the various possible explanations will require future experiments beyond the scope of this initial generation of the rat model (Seffer et al 2014;Wöhr and Schwarting 2007;Wöhr et al 2016).…”

Section: Discussionmentioning

confidence: 99%

Translational Outcomes Relevant to Neurodevelopmental Disorders Following Early Life Exposure of Rats to Chlorpyrifos

Berg

Ching

Bruun

et al. 2020

Preprint

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Background: Neurodevelopmental disorders (NDDs), including intellectual disability, attention deficit hyperactivity disorder (ADHD) and autism spectrum disorder (ASD), are pervasive, lifelong disorders for which pharmacological interventions are not readily available. Substantial increases in the prevalence of NDDs over a relatively short period cannot be attributed solely to genetic factors and/or improved diagnostic criteria. There is now a consensus that multiple genetic loci combined with exposure(s) to environmental risk factors during critical periods of neurodevelopment influence NDD susceptibility and symptom severity. Organophosphorus (OP) pesticides have been identified as potential environmental risk factors. Epidemiological studies suggest children exposed prenatally to the OP pesticide chlorpyrifos (CPF) have significant mental and motor delays and strong positive associations for the development of a clinical diagnosis of developmental delay, ADHD, or ASD. Methods: We tested the hypothesis that developmental CPF exposure impairs behavior relevant to NDD phenotypes, i.e., deficits in social communication and repetitive, restricted behavior. Male and female rat pups were exposed to CPF at 0.1, 1.0, or 3.0 mg/kg (s.c.) from postnatal days 1-4. Results: These CPF doses did not significantly inhibit acetylcholinesterase activity in the blood or brain but significantly impaired pup ultrasonic vocalizations (USV) in both sexes. Social communication in juveniles via positive affiliative 50-kHz USV playback was absent in females exposed to CPF at 0.3 mg/kg and 1.0 mg/kg. In contrast, this CPF exposure paradigm had no significant effect on gross locomotor abilities or contextual and cued fear memory. Ex vivo magnetic resonance imaging largely found no differences between the CPF rats and the corresponding vehicle controls; however there were some interesting trends in females at a dosage of 0.3 mg/kg. Conclusions: This work characterizes a rat model of developmental CPF exposure that exhibits adverse behavioral phenotypes resulting from perinatal exposures at levels that did not significantly inhibit acetylcholinesterase activity in brain or blood. These data suggest that current regulations regarding safe levels of CPF need to be reconsidered.

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Studying Socio‐Affective Communication in Rats through Playback of Ultrasonic Vocalizations

Cited by 31 publications

References 38 publications

Translational outcomes in a full gene deletion of ubiquitin protein ligase E3A rat model of Angelman syndrome

Translational outcomes in a full gene deletion of ubiquitin protein ligase E3A rat model of Angelman syndrome

Subthalamic nucleus mediates the modulation on cocaine self-administration induced by ultrasonic 3 vocalizations playback in rats

Translational Outcomes Relevant to Neurodevelopmental Disorders Following Early Life Exposure of Rats to Chlorpyrifos

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