Editorial

3 pages, 160 KiB

Open AccessEditorial

Recent Studies of Rat Ultrasonic Vocalizations—Editorial

by Stefan M. Brudzynski and Jeffrey S. Burgdorf

Brain Sci. 2021, 11(11), 1390; https://doi.org/10.3390/brainsci11111390 - 23 Oct 2021

Cited by 1 | Viewed by 1362

Since the realization that human emotional experiences and behavior evolved from mammalian ancestors and are evolutionary continuations of animal emotional behavior [...] Full article

(This article belongs to the Special Issue Recent Studies of Rodent Ultrasonic Vocalizations and Their Use in Experimental Models)

Research

Jump to: Editorial, Review, Other

19 pages, 2939 KiB

Open AccessArticle

Fear Extinction-Based Inter-Individual and Sex Differences in Pain-Related Vocalizations and Anxiety-like Behaviors but Not Nocifensive Reflexes

by Peyton Presto, Guangchen Ji, Riley Junell, Zach Griffin and Volker Neugebauer

Brain Sci. 2021, 11(10), 1339; https://doi.org/10.3390/brainsci11101339 - 11 Oct 2021

Cited by 11 | Viewed by 2239

Abstract

Inter-individual and sex differences in pain responses are recognized but their mechanisms are not well understood. This study was intended to provide the behavioral framework for analyses of pain mechanisms using fear extinction learning as a predictor of phenotypic and sex differences in [...] Read more.

Inter-individual and sex differences in pain responses are recognized but their mechanisms are not well understood. This study was intended to provide the behavioral framework for analyses of pain mechanisms using fear extinction learning as a predictor of phenotypic and sex differences in sensory (mechanical withdrawal thresholds) and emotional-affective aspects (open field tests for anxiety-like behaviors and audible and ultrasonic components of vocalizations) of acute and chronic pain. In acute arthritis and chronic neuropathic pain models, greater increases in vocalizations were found in females than males and in females with poor fear extinction abilities than females with strong fear extinction, particularly in the neuropathic pain model. Female rats showed higher anxiety-like behavior than males under baseline conditions but no inter-individual or sex differences were seen in the pain models. No inter-individual and sex differences in mechanosensitivity were observed. The data suggest that vocalizations are uniquely suited to detect inter-individual and sex differences in pain models, particularly in chronic neuropathic pain, whereas no such differences were found for mechanosensitivity, and baseline differences in anxiety-like behaviors disappeared in the pain models. Full article

(This article belongs to the Special Issue Recent Studies of Rodent Ultrasonic Vocalizations and Their Use in Experimental Models)

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13 pages, 3828 KiB

Open AccessArticle

Nucleus Accumbens Chemogenetic Inhibition Suppresses Amphetamine-Induced Ultrasonic Vocalizations in Male and Female Rats

by Kate A. Lawson, Abigail Y. Flores, Rachael E. Hokenson, Christina M. Ruiz and Stephen V. Mahler

Brain Sci. 2021, 11(10), 1255; https://doi.org/10.3390/brainsci11101255 - 22 Sep 2021

Cited by 6 | Viewed by 3087

Abstract

Adult rats emit ultrasonic vocalizations (USVs) related to their affective states, potentially providing information about their subjective experiences during behavioral neuroscience experiments. If so, USVs might provide an important link between invasive animal preclinical studies and human studies in which subjective states can [...] Read more.

Adult rats emit ultrasonic vocalizations (USVs) related to their affective states, potentially providing information about their subjective experiences during behavioral neuroscience experiments. If so, USVs might provide an important link between invasive animal preclinical studies and human studies in which subjective states can be readily queried. Here, we induced USVs in male and female Long Evans rats using acute amphetamine (2 mg/kg), and asked how reversibly inhibiting nucleus accumbens neurons using designer receptors exclusively activated by designer drugs (DREADDs) impacts USV production. We analyzed USV characteristics using “Deepsqueak” software, and manually categorized detected calls into four previously defined subtypes. We found that systemic administration of the DREADD agonist clozapine-n-oxide, relative to vehicle in the same rats, suppressed the number of frequency-modulated and trill-containing USVs without impacting high frequency, unmodulated (flat) USVs, nor the small number of low-frequency USVs observed. Using chemogenetics, these results thus confirm that nucleus accumbens neurons are essential for production of amphetamine-induced frequency-modulated USVs. They also support the premise of further investigating the characteristics and subcategories of these calls as a window into the subjective effects of neural manipulations, with potential future clinical applications. Full article

(This article belongs to the Special Issue Recent Studies of Rodent Ultrasonic Vocalizations and Their Use in Experimental Models)

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17 pages, 960 KiB

Open AccessArticle

Effects of Ethanol Exposure during Lactation on Ultrasonic Vocalizations of Rat Pups upon Their Isolation: Increase in Pup Distress Calls

by Mohd. Ashik Shahrier and Hiromi Wada

Brain Sci. 2021, 11(9), 1249; https://doi.org/10.3390/brainsci11091249 - 21 Sep 2021

Cited by 1 | Viewed by 1758

Abstract

Recording ultrasonic vocalizations (USVs) is a highly sensitive tool to study the dam–pup social relationships, and USV recordings have been used to study the effects of ethanol on pups. Gestational effects of ethanol on the emission of USVs in rat pups have been [...] Read more.

Recording ultrasonic vocalizations (USVs) is a highly sensitive tool to study the dam–pup social relationships, and USV recordings have been used to study the effects of ethanol on pups. Gestational effects of ethanol on the emission of USVs in rat pups have been studied in our previous research. In the present study, the effects of ethanol given to dams during lactation on the acoustic parameters of USVs emitted by isolated pups were examined. Ethanol was administered to dams from postnatal days (PNDs) 5–21. From PNDs 11–21, the high- and low-ethanol-treated dams were exposed to ethanol-containing water (v/v) at concentrations of 30% and 15%, respectively. Tap water without ethanol (0%) was provided to the control dams. The pups in all three ethanol-treated groups were separated from the dam and littermates on PNDs 4, 8, 12, and 16, and USVs produced by the pups were recorded for 5 min. It was found that elevated distress USVs with longer duration and higher percentage of frequency modulations were displayed by the pups from the high-ethanol dams. Alterations in USVs were particularly evident in the pups with a reduced body weight at PND 12. This effect might be because high-ethanol dams showed significantly lower intake of higher ethanol-containing water, and consequently, produced lower amount of milk, as well as exhibited poor maternal care. Insufficient maternal care and malnutrition resulted in pup growth retardation and increased mortality rate in the high-ethanol group, which were not observed in the low-ethanol or control pups. Accordingly, the pups in the high-ethanol group experienced elevated negative emotionality during isolation from their dam and increased emission of USVs. Longer duration and increased frequency modulation of pup USVs are expected to be noticed by the dam and to initiate/increase proper maternal care. It is concluded that ethanol given to lactating mothers has more serious consequences on pup development than the gestational ethanol exposure, and has more harmful effects on pups. Full article

(This article belongs to the Special Issue Recent Studies of Rodent Ultrasonic Vocalizations and Their Use in Experimental Models)

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18 pages, 2574 KiB

Open AccessArticle

Rat 50 kHz Trill Calls Are Tied to the Expectation of Social Interaction

by Candace J. Burke, Mariya Markovina, Sergio M. Pellis and David R. Euston

Brain Sci. 2021, 11(9), 1142; https://doi.org/10.3390/brainsci11091142 - 28 Aug 2021

Cited by 11 | Viewed by 2179

Abstract

Rats emit a variety of calls in the 40–80 kHz range (50 kHz calls). While these calls are generally associated with positive affect, it is unclear whether certain calls might be used selectively in certain contexts. To examine this, we looked at ultrasonic [...] Read more.

Rats emit a variety of calls in the 40–80 kHz range (50 kHz calls). While these calls are generally associated with positive affect, it is unclear whether certain calls might be used selectively in certain contexts. To examine this, we looked at ultrasonic calls in 30–40 day old male rats during the expectation of either play or food, both of which are reinforcing. Behavior and vocalizations were recorded while rats were in a test chamber awaiting the arrival of a play partner or food over seven days of testing. Control groups were included for the non-specific effects of food deprivation and social isolation. Play reward led to an increase in 50 kHz vocalizations, generally, with specific increases in trill and “trill with jump” calls not seen in other groups. Expectation of food reward did not lead to a significant increase in vocalizations of any type, perhaps due to the young age of our study group. Further, rats that were food deprived for the food expectation study showed markedly lower calls overall and had a different profile of call types compared to rats that were socially isolated. Taken together, the results suggest that trill-associated calls may be used selectively when rats are socially isolated and/or expecting a social encounter. Full article

(This article belongs to the Special Issue Recent Studies of Rodent Ultrasonic Vocalizations and Their Use in Experimental Models)

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10 pages, 1148 KiB

Open AccessArticle

Chronic Fentanyl Self-Administration Generates a Shift toward Negative Affect in Rats during Drug Use

by Angela N. Dao, Nicholas J. Beacher, Vivian Mayr, Annalisa Montemarano, Sam Hammer and Mark O. West

Brain Sci. 2021, 11(8), 1064; https://doi.org/10.3390/brainsci11081064 - 13 Aug 2021

Cited by 5 | Viewed by 2597

Abstract

Drug addiction is thought to be driven by negative reinforcement, and it is thought that a shift from positive affect upon initial exposure to negative affect after chronic exposure to a drug is responsible for maintaining self-administration (SA) in addicted individuals. This can [...] Read more.

Drug addiction is thought to be driven by negative reinforcement, and it is thought that a shift from positive affect upon initial exposure to negative affect after chronic exposure to a drug is responsible for maintaining self-administration (SA) in addicted individuals. This can be modeled in rats by analyzing ultrasonic vocalizations (USVs), a type of intraspecies communication indicative of affective state based on the frequency of the emission: calls in the 22 kHz range indicate negative affect, whereas calls in the 50 kHz range indicate positive affect. We employed a voluntary chronic, long-access model of fentanyl SA to analyze affective changes in the response to chronic fentanyl exposure. Male Sprague-Dawley rats self-administered either fentanyl (N = 7) or saline (N = 6) for 30 consecutive days and USVs were recorded at four different time points: the day before the first SA session (PRE), the first day of SA (T01), the last day of SA (T30), and the first day of abstinence (ABS). At T01, the ratio of 50 to 22 kHz calls was similar between the fentanyl and saline groups, but at T30, the ratio differed between groups, with the fentanyl group showing significantly fewer 50 kHz calls and more 22 kHz calls relative to saline animals. These results indicate a shift toward a negative affect during drug use after chronic exposure to fentanyl and support negative reinforcement as a main driving factor of opioid addiction. Full article

(This article belongs to the Special Issue Recent Studies of Rodent Ultrasonic Vocalizations and Their Use in Experimental Models)

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17 pages, 2474 KiB

Open AccessArticle

Association between Novel Object Recognition/Spontaneous Alternation Behavior and Emission of Ultrasonic Vocalizations in Rats: Possible Relevance to the Study of Memory

by Giulia Costa, Marcello Serra and Nicola Simola

Brain Sci. 2021, 11(8), 1053; https://doi.org/10.3390/brainsci11081053 - 09 Aug 2021

Cited by 4 | Viewed by 2565

Abstract

Rats emit ultrasonic vocalizations (USVs) in situations with emotional valence, and USVs have also been proposed as a marker for memories conditioned to those situations. This study investigated whether USV emissions can predict and/or be associated with the behavior of rats in tests [...] Read more.

Rats emit ultrasonic vocalizations (USVs) in situations with emotional valence, and USVs have also been proposed as a marker for memories conditioned to those situations. This study investigated whether USV emissions can predict and/or be associated with the behavior of rats in tests that evaluate unconditioned memory. To this end, rats were subjected to “tickling”, a procedure of heterospecific play that has emotional valence and elicits the emission of USVs, and afterwards evaluated in the novel object recognition test (NOR) and in the single trial continuous spontaneous alternation behavior (SAB) test in a Y maze. The number of 22-kHz USVs (aversive) and 50-kHz USVs (appetitive) emitted in response to tickling and during NOR and SAB tests were scored, and the correlations among them and with rats’ behavior evaluated. Rats emitted 50-kHz USVs, but not 22-kHz USVs, during the NOR and SAB tests, and such calling behavior was not linked with the behavioral readouts indicative of memory function in either test. However, rats that prevalently emitted 22-kHz USVs in response to tickling displayed an impaired NOR performance. These findings suggest that measuring the emission of USVs could be of interest in studies of unconditioned memory, at least with regard to 22-kHz USVs. Full article

(This article belongs to the Special Issue Recent Studies of Rodent Ultrasonic Vocalizations and Their Use in Experimental Models)

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18 pages, 2030 KiB

Open AccessArticle

Increased Vocalization of Rats in Response to Ultrasonic Playback as a Sign of Hypervigilance Following Fear Conditioning

by Krzysztof H. Olszyński, Rafał Polowy, Agnieszka D. Wardak, Aneta W. Grymanowska and Robert K. Filipkowski

Brain Sci. 2021, 11(8), 970; https://doi.org/10.3390/brainsci11080970 - 23 Jul 2021

Cited by 9 | Viewed by 2707

Abstract

We investigated the effects of prior stress on rats’ responses to 50-kHz (appetitive) and 22-kHz (aversive) ultrasonic playback. Rats were treated with 0, 1, 6 or 10 shocks (1 s, 1.0 mA each) and were exposed to playbacks the following day. Previous findings [...] Read more.

We investigated the effects of prior stress on rats’ responses to 50-kHz (appetitive) and 22-kHz (aversive) ultrasonic playback. Rats were treated with 0, 1, 6 or 10 shocks (1 s, 1.0 mA each) and were exposed to playbacks the following day. Previous findings were confirmed: (i) rats moved faster during 50-kHz playback and slowed down after 22-kHz playback; (ii) they all approached the speaker, which was more pronounced during and following 50-kHz playback than 22-kHz playback; (iii) 50-kHz playback caused heart rate (HR) increase; 22-kHz playback caused HR decrease; (iv) the rats vocalized more often during and following 50-kHz playback than 22-kHz playback. The previous shock affected the rats such that singly-shocked rats showed lower HR throughout the experiment and a smaller HR response to 50-kHz playback compared to controls and other shocked groups. Interestingly, all pre-shocked rats showed higher locomotor activity during 50-kHz playback and a more significant decrease in activity following 22-kHz playback; they vocalized more often, their ultrasonic vocalizations (USV) were longer and at a higher frequency than those of the control animals. These last two observations could point to hypervigilance, a symptom of post-traumatic stress disorder (PTSD) in human patients. Increased vocalization may be a valuable measure of hypervigilance used for PTSD modeling. Full article

(This article belongs to the Special Issue Recent Studies of Rodent Ultrasonic Vocalizations and Their Use in Experimental Models)

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19 pages, 1143 KiB

Open AccessArticle

Acoustilytix™: A Web-Based Automated Ultrasonic Vocalization Scoring Platform

by Catherine B. Ashley, Ryan D. Snyder, James E. Shepherd, Catalina Cervantes, Nitish Mittal, Sheila Fleming, Jaxon Bailey, Maisie D. Nievera, Sharmin Islam Souleimanova, Bill Nyaoga, Lauren Lichtenfeld, Alicia R. Chen, W. Todd Maddox and Christine L. Duvauchelle

Brain Sci. 2021, 11(7), 864; https://doi.org/10.3390/brainsci11070864 - 29 Jun 2021

Viewed by 2341

Abstract

Ultrasonic vocalizations (USVs) are known to reflect emotional processing, brain neurochemistry, and brain function. Collecting and processing USV data is manual, time-intensive, and costly, creating a significant bottleneck by limiting researchers’ ability to employ fully effective and nuanced experimental designs and serving as [...] Read more.

Ultrasonic vocalizations (USVs) are known to reflect emotional processing, brain neurochemistry, and brain function. Collecting and processing USV data is manual, time-intensive, and costly, creating a significant bottleneck by limiting researchers’ ability to employ fully effective and nuanced experimental designs and serving as a barrier to entry for other researchers. In this report, we provide a snapshot of the current development and testing of Acoustilytix™, a web-based automated USV scoring tool. Acoustilytix implements machine learning methodology in the USV detection and classification process and is recording-environment-agnostic. We summarize the user features identified as desirable by USV researchers and how these were implemented. These include the ability to easily upload USV files, output a list of detected USVs with associated parameters in csv format, and the ability to manually verify or modify an automatically detected call. With no user intervention or tuning, Acoustilytix achieves 93% sensitivity (a measure of how accurately Acoustilytix detects true calls) and 73% precision (a measure of how accurately Acoustilytix avoids false positives) in call detection across four unique recording environments and was superior to the popular DeepSqueak algorithm (sensitivity = 88%; precision = 41%). Future work will include integration and implementation of machine-learning-based call type classification prediction that will recommend a call type to the user for each detected call. Call classification accuracy is currently in the 71–79% accuracy range, which will continue to improve as more USV files are scored by expert scorers, providing more training data for the classification model. We also describe a recently developed feature of Acoustilytix that offers a fast and effective way to train hand-scorers using automated learning principles without the need for an expert hand-scorer to be present and is built upon a foundation of learning science. The key is that trainees are given practice classifying hundreds of calls with immediate corrective feedback based on an expert’s USV classification. We showed that this approach is highly effective with inter-rater reliability (i.e., kappa statistics) between trainees and the expert ranging from 0.30–0.75 (average = 0.55) after only 1000–2000 calls of training. We conclude with a brief discussion of future improvements to the Acoustilytix platform. Full article

(This article belongs to the Special Issue Recent Studies of Rodent Ultrasonic Vocalizations and Their Use in Experimental Models)

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16 pages, 3201 KiB

Open AccessArticle

Relaying Aversive Ultrasonic Alarm Calls Depends on Previous Experience. Empathy, Social Buffering, or Panic?

by Wiktoria Karwicka, Marta Wiatrowska, Kacper Kondrakiewicz, Ewelina Knapska, Miron Bartosz Kursa and Adam Hamed

Brain Sci. 2021, 11(6), 759; https://doi.org/10.3390/brainsci11060759 - 08 Jun 2021

Cited by 6 | Viewed by 2231

Abstract

Ultrasonic vocalizations are among the oldest evolutionarily forms of animal communication. In order to study the communication patterns in an aversive social situation, we used a behavioral model in which one animal, the observer, is witnessing as his cagemate, the demonstrator, is experiencing [...] Read more.

Ultrasonic vocalizations are among the oldest evolutionarily forms of animal communication. In order to study the communication patterns in an aversive social situation, we used a behavioral model in which one animal, the observer, is witnessing as his cagemate, the demonstrator, is experiencing a series of mild electrical foot shocks. We studied the effect of the foot shock experience on the observer and the influence of a warning sound (emitted shortly before the shock) on USV communication. These experiments revealed that such a warning seems to increase the arousal level, which differentiates the responses depending on previous experience. This can be identified by the emission of characteristic, short 22 kHz calls of a duration below 100 ms. Two rats emitted calls that overlapped in time. Analysis of these overlaps revealed that in ‘warned’ pairs with a naive observer, 22 kHz calls were mixed with 50 kHz calls. This fact, combined with a high fraction of very high-pitched 50 kHz calls (over 75 kHz), suggests the presence of the phenomenon of social buffering. Pure 22 kHz overlaps were mostly found in ‘warned’ pairs with an experienced observer, suggesting a possible fear contagion with distress sharing. The results show the importance of dividing 22 kHz calls into long and short categories. Full article

(This article belongs to the Special Issue Recent Studies of Rodent Ultrasonic Vocalizations and Their Use in Experimental Models)

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13 pages, 2369 KiB

Open AccessArticle

The Effect of Vasopressin Antagonists on Maternal-Separation-Induced Ultrasonic Vocalization and Stress-Hormone Level Increase during the Early Postnatal Period

by Bibiána Török, Anna Fodor, Sándor Zsebők, Eszter Sipos and Dóra Zelena

Brain Sci. 2021, 11(4), 444; https://doi.org/10.3390/brainsci11040444 - 30 Mar 2021

Cited by 3 | Viewed by 1667

Abstract

In adults, vasopressin exerts an anxiogenic effect, but less is known about the perinatal period. As a sign of distress, rat pups emit ultrasonic vocalizations when they are separated from their mothers, known as maternal separation-induced ultrasonic vocalization (MS-USV). Previously, reduced MS-USV was [...] Read more.

In adults, vasopressin exerts an anxiogenic effect, but less is known about the perinatal period. As a sign of distress, rat pups emit ultrasonic vocalizations when they are separated from their mothers, known as maternal separation-induced ultrasonic vocalization (MS-USV). Previously, reduced MS-USV was reported in 7–8-day-old genetically vasopressin-deficient Brattleboro rats. Here, we aimed to examine the contributing vasopressin receptor (VR) subtypes using Wistar pups. MS-USV was recorded for 10 min, 30 min after vasopressin (V) 1aR, V1bR or V2R antagonist treatment (SR49059, SSR149415, SR121463B; 3, 10 and 30 mg/kg, intraperitoneal). Sedation was studied by the righting reflex and negative geotaxis, and finally, the stress hormone levels were measured by radioimmunoassay. The vasopressin-deficient pups showed decreased MS-USV and adrenocorticotropin levels even after a saline injection, with unchanged corticosterone levels. Thirty mg/kg of V1aR-antagonist increased the corticosterone levels. All V1bR antagonist doses decreased the MS-USV and adrenocorticotropin, while 10 + 10 mg/kg of V1aR and V1bR antagonists decreased MS-USV without influencing the stress hormones. Three mg/kg of V2R antagonist enhanced MS-USV, while 30 mg/kg increased the stress hormone levels. We confirmed that vasopressin deficiency already caused anxiolytic effects in pups. V1bRs are the most important player in connection with their adrenocorticotropin (ACTH)-regulatory role, but a combination of V1aR and V1bR antagonists might be also beneficial through other mechanisms, reducing the possibility of side effects. In contrast, antagonizing the V2Rs may be stressful due to an induction of imbalance in saltwater homeostasis. Full article

(This article belongs to the Special Issue Recent Studies of Rodent Ultrasonic Vocalizations and Their Use in Experimental Models)

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16 pages, 4507 KiB

Open AccessFeature PaperArticle

Observational Fear Learning in Rats: Role of Trait Anxiety and Ultrasonic Vocalization

by Markus Fendt, Claudia Paulina Gonzalez-Guerrero and Evelyn Kahl

Brain Sci. 2021, 11(4), 423; https://doi.org/10.3390/brainsci11040423 - 26 Mar 2021

Cited by 7 | Viewed by 3840

Abstract

Rats can acquire fear by observing conspecifics that express fear in the presence of conditioned fear stimuli. This process is called observational fear learning and is based on the social transmission of the demonstrator rat’s emotion and the induction of an empathy-like or [...] Read more.

Rats can acquire fear by observing conspecifics that express fear in the presence of conditioned fear stimuli. This process is called observational fear learning and is based on the social transmission of the demonstrator rat’s emotion and the induction of an empathy-like or anxiety state in the observer. The aim of the present study was to investigate the role of trait anxiety and ultrasonic vocalization in observational fear learning. Two experiments with male Wistar rats were performed. In the first experiment, trait anxiety was assessed in a light–dark box test before the rats were submitted to the observational fear learning procedure. In the second experiment, ultrasonic vocalization was recorded throughout the whole observational fear learning procedure, and 22 kHz and 50 kHz calls were analyzed. The results of our study show that trait anxiety differently affects direct fear learning and observational fear learning. Direct fear learning was more pronounced with higher trait anxiety, while observational fear learning was the best with a medium-level of trait anxiety. There were no indications in the present study that ultrasonic vocalization, especially emission of 22 kHz calls, but also 50 kHz calls, are critical for observational fear learning. Full article

(This article belongs to the Special Issue Recent Studies of Rodent Ultrasonic Vocalizations and Their Use in Experimental Models)

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13 pages, 3230 KiB

Open AccessArticle

The Effect of Maternal Immune Activation on Social Play-Induced Ultrasonic Vocalization in Rats

by Kinga Gzielo, Agnieszka Potasiewicz, Ewa Litwa, Diana Piotrowska, Piotr Popik and Agnieszka Nikiforuk

Brain Sci. 2021, 11(3), 344; https://doi.org/10.3390/brainsci11030344 - 09 Mar 2021

Cited by 17 | Viewed by 2509

Abstract

Prenatal maternal infection is associated with an increased risk of various neurodevelopmental disorders, including autism spectrum disorders (ASD). Maternal immune activation (MIA) can be experimentally induced by prenatal administration of polyinosinic:polycytidylic acid (poly I:C), a synthetic viral-like double-stranded RNA. Although this MIA model [...] Read more.

Prenatal maternal infection is associated with an increased risk of various neurodevelopmental disorders, including autism spectrum disorders (ASD). Maternal immune activation (MIA) can be experimentally induced by prenatal administration of polyinosinic:polycytidylic acid (poly I:C), a synthetic viral-like double-stranded RNA. Although this MIA model is adopted in many studies, social and communicative deficits, included in the first diagnostic criterion of ASD, are poorly described in the offspring of poly(I:C)-exposed dams. This study aimed to characterize the impact of prenatal poly(I:C) exposure on socio-communicative behaviors in adolescent rats. For this purpose, social play behavior was assessed in both males and females. We also analyzed quantitative and structural changes in ultrasonic vocalizations (USVs) emitted by rats during the play test. Deficits of social play behaviors were evident only in male rats. Males also emitted a significantly decreased number of USVs during social encounters. Prenatal poly(I:C) exposure also affected acoustic call parameters, as reflected by the increased peak frequencies. Additionally, repetitive behaviors were demonstrated in autistic-like animals regardless of sex. This study demonstrates that prenatal poly(I:C) exposure impairs socio-communicative functioning in adolescent rats. USVs may be a useful tool for identifying early autistic-like abnormalities. Full article

(This article belongs to the Special Issue Recent Studies of Rodent Ultrasonic Vocalizations and Their Use in Experimental Models)

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Review

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21 pages, 1467 KiB

Open AccessReview

Rat Models of Vocal Deficits in Parkinson’s Disease

by Maryann N. Krasko, Jesse D. Hoffmeister, Nicole E. Schaen-Heacock, Jacob M. Welsch, Cynthia A. Kelm-Nelson and Michelle R. Ciucci

Brain Sci. 2021, 11(7), 925; https://doi.org/10.3390/brainsci11070925 - 13 Jul 2021

Cited by 12 | Viewed by 3115

Abstract

Parkinson’s disease (PD) is a progressive, degenerative disorder that affects 10 million people worldwide. More than 90% of individuals with PD develop hypokinetic dysarthria, a motor speech disorder that impairs vocal communication and quality of life. Despite the prevalence of vocal deficits in [...] Read more.

Parkinson’s disease (PD) is a progressive, degenerative disorder that affects 10 million people worldwide. More than 90% of individuals with PD develop hypokinetic dysarthria, a motor speech disorder that impairs vocal communication and quality of life. Despite the prevalence of vocal deficits in this population, very little is known about the pathological mechanisms underlying this aspect of disease. As such, effective treatment options are limited. Rat models have provided unique insights into the disease-specific mechanisms of vocal deficits in PD. This review summarizes recent studies investigating vocal deficits in 6-hydroxydopamine (6-OHDA), alpha-synuclein overexpression, DJ1-/-, and Pink1-/- rat models of PD. Model-specific changes to rat ultrasonic vocalization (USV), and the effects of exercise and pharmacologic interventions on USV production in these models are discussed. Full article

(This article belongs to the Special Issue Recent Studies of Rodent Ultrasonic Vocalizations and Their Use in Experimental Models)

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19 pages, 839 KiB

Open AccessReview

Social Behavior and Ultrasonic Vocalizations in a Genetic Rat Model Haploinsufficient for the Cross-Disorder Risk Gene Cacna1c

by Markus Wöhr, Theresa M. Kisko and Rainer K.W. Schwarting

Brain Sci. 2021, 11(6), 724; https://doi.org/10.3390/brainsci11060724 - 29 May 2021

Cited by 5 | Viewed by 2792

Abstract

The top-ranked cross-disorder risk gene CACNA1C is strongly associated with multiple neuropsychiatric dysfunctions. In a recent series of studies, we applied a genomically informed approach and contributed extensively to the behavioral characterization of a genetic rat model haploinsufficient for the cross-disorder risk gene [...] Read more.

The top-ranked cross-disorder risk gene CACNA1C is strongly associated with multiple neuropsychiatric dysfunctions. In a recent series of studies, we applied a genomically informed approach and contributed extensively to the behavioral characterization of a genetic rat model haploinsufficient for the cross-disorder risk gene Cacna1c. Because deficits in processing social signals are associated with reduced social functioning as commonly seen in neuropsychiatric disorders, we focused on socio-affective communication through 22-kHz and 50-kHz ultrasonic vocalizations (USV). Specifically, we applied a reciprocal approach for studying socio-affective communication in sender and receiver by including rough-and-tumble play and playback of 22-kHz and 50-kHz USV. Here, we review the findings obtained in this recent series of studies and link them to the key features of 50-kHz USV emission during rough-and-tumble play and social approach behavior evoked by playback of 22-kHz and 50-kHz USV. We conclude that Cacna1c haploinsufficiency in rats leads to robust deficits in socio-affective communication through 22-kHz and 50-kHz USV and associated alterations in social behavior, such as rough-and-tumble play behavior. Full article

(This article belongs to the Special Issue Recent Studies of Rodent Ultrasonic Vocalizations and Their Use in Experimental Models)

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17 pages, 1730 KiB

Open AccessReview

Ultrasonic Vocalizations Emission across Development in Rats: Coordination with Respiration and Impact on Brain Neural Dynamics

by Julie Boulanger-Bertolus and Anne-Marie Mouly

Brain Sci. 2021, 11(5), 616; https://doi.org/10.3390/brainsci11050616 - 11 May 2021

Cited by 5 | Viewed by 3358

Abstract

Rats communicate using ultrasonic vocalizations (USV) throughout their life when confronted with emotionally stimulating situations, either negative or positive. The context of USV emission and the psychoacoustic characteristics of the vocalizations change greatly between infancy and adulthood. Importantly, the production of USV is [...] Read more.

Rats communicate using ultrasonic vocalizations (USV) throughout their life when confronted with emotionally stimulating situations, either negative or positive. The context of USV emission and the psychoacoustic characteristics of the vocalizations change greatly between infancy and adulthood. Importantly, the production of USV is tightly coordinated with respiration, and respiratory rhythm is known to influence brain activity and cognitive functions. This review goes through the acoustic characteristics and mechanisms of production of USV both in infant and adult rats and emphasizes the tight relationships that exist between USV emission and respiration throughout the rat’s development. It further describes how USV emission and respiration collectively affect brain oscillatory activities. We discuss the possible association of USV emission with emotional memory processes and point out several avenues of research on USV that are currently overlooked and could fill gaps in our knowledge. Full article

(This article belongs to the Special Issue Recent Studies of Rodent Ultrasonic Vocalizations and Their Use in Experimental Models)

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44 pages, 1222 KiB

Open AccessReview

Biological Functions of Rat Ultrasonic Vocalizations, Arousal Mechanisms, and Call Initiation

by Stefan M. Brudzynski

Brain Sci. 2021, 11(5), 605; https://doi.org/10.3390/brainsci11050605 - 09 May 2021

Cited by 45 | Viewed by 4845

Abstract

This review summarizes all reported and suspected functions of ultrasonic vocalizations in infant and adult rats. The review leads to the conclusion that all types of ultrasonic vocalizations subserving all functions are vocal expressions of emotional arousal initiated by the activity of the [...] Read more.

This review summarizes all reported and suspected functions of ultrasonic vocalizations in infant and adult rats. The review leads to the conclusion that all types of ultrasonic vocalizations subserving all functions are vocal expressions of emotional arousal initiated by the activity of the reticular core of the brainstem. The emotional arousal is dichotomic in nature and is initiated by two opposite-in-function ascending reticular systems that are separate from the cognitive reticular activating system. The mesolimbic cholinergic system initiates the aversive state of anxiety with concomitant emission of 22 kHz calls, while the mesolimbic dopaminergic system initiates the appetitive state of hedonia with concomitant emission of 50 kHz vocalizations. These two mutually exclusive arousal systems prepare the animal for two different behavioral outcomes. The transition from broadband infant isolation calls to the well-structured adult types of vocalizations is explained, and the social importance of adult rat vocal communication is emphasized. The association of 22 kHz and 50 kHz vocalizations with aversive and appetitive states, respectively, was utilized in numerous quantitatively measured preclinical models of physiological, psychological, neurological, neuropsychiatric, and neurodevelopmental investigations. The present review should help in understanding and the interpretation of these models in biomedical research. Full article

(This article belongs to the Special Issue Recent Studies of Rodent Ultrasonic Vocalizations and Their Use in Experimental Models)

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Open AccessReview

Biological and Acoustic Sex Differences in Rat Ultrasonic Vocalization

by Charles Lenell, Courtney K. Broadfoot, Nicole E. Schaen-Heacock and Michelle R. Ciucci

Brain Sci. 2021, 11(4), 459; https://doi.org/10.3390/brainsci11040459 - 04 Apr 2021

Cited by 15 | Viewed by 3598

Abstract

The rat model is a useful tool for understanding peripheral and central mechanisms of laryngeal biology. Rats produce ultrasonic vocalizations (USVs) that have communicative intent and are altered by experimental conditions such as social environment, stress, diet, drugs, age, and neurological diseases, validating [...] Read more.

The rat model is a useful tool for understanding peripheral and central mechanisms of laryngeal biology. Rats produce ultrasonic vocalizations (USVs) that have communicative intent and are altered by experimental conditions such as social environment, stress, diet, drugs, age, and neurological diseases, validating the rat model’s utility for studying communication and related deficits. Sex differences are apparent in both the rat larynx and USV acoustics and are differentially affected by experimental conditions. Therefore, the purpose of this review paper is to highlight the known sex differences in rat USV production, acoustics, and laryngeal biology detailed in the literature across the lifespan. Full article

(This article belongs to the Special Issue Recent Studies of Rodent Ultrasonic Vocalizations and Their Use in Experimental Models)

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11 pages, 1994 KiB

Open AccessBrief Report

Extracellular Dopamine Levels in Nucleus Accumbens after Chronic Stress in Rats with Persistently High vs. Low 50-kHz Ultrasonic Vocalization Response

by Kadri Kõiv, Kai Tiitsaar, Karita Laugus and Jaanus Harro

Brain Sci. 2021, 11(4), 470; https://doi.org/10.3390/brainsci11040470 - 08 Apr 2021

Cited by 4 | Viewed by 2063

Abstract

Fifty-kHz ultrasonic vocalizations (USVs) in response to an imitation of rough-and-tumble play (‘tickling’) have been associated with positive affective states and rewarding experience in the rat. This USV response can be used as a measure of inter-individual differences in positive affect. We have [...] Read more.

Fifty-kHz ultrasonic vocalizations (USVs) in response to an imitation of rough-and-tumble play (‘tickling’) have been associated with positive affective states and rewarding experience in the rat. This USV response can be used as a measure of inter-individual differences in positive affect. We have previously shown that rats with persistently low positive affectivity are more vulnerable to the effects of chronic variable stress (CVS). To examine whether these differential responses are associated with dopaminergic neurotransmission in the nucleus accumbens (NAc), juvenile male Wistar rats were categorized as of high or low positive affectivity (HC and LC, respectively), and after reaching adulthood, extracellular dopamine (DA) levels in the NAc shell were measured using in vivo microdialysis after three weeks of CVS. Baseline levels of DA were compared as well as the response to K⁺-induced depolarization and the effect of glial glutamate transporter EAAT2 inhibition by 4 mM l-trans-pyrrolidine-2,4-dicarboxylate (PDC). DA baseline levels were higher in control LC-rats, and stress significantly lowered the DA content in LC-rats. An interaction of stress and affectivity appeared in response to depolarization where stress increased the DA output in HC-rats whereas it decreased it in LC-rats. These results show that NAc-shell DA is differentially regulated in response to stress in animals with high and low positive affect. Full article

(This article belongs to the Special Issue Recent Studies of Rodent Ultrasonic Vocalizations and Their Use in Experimental Models)

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