Rat ultrasonic vocalization in aversively motivated situations and the role of individual differences in anxiety-related behavior

Borta, Andreas; Wöhr, Markus; Schwarting, Rainer K.W.

doi:10.1016/j.bbr.2005.08.009

Cited by 160 publications

(143 citation statements)

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“…USVs serve as ethologically-critical social signals (Brudzynski, 2005;Litvin et al, 2007) and offer a unique window into the emotional state of the animal (Borta et al, 2006;Brudzynski, 2007;Knutson et al, 2002;Panksepp, 2007). Rats emit USVs at frequencies of ~22 kHz and ~50 kHz in conjunction with negative and positive emotional states, respectively (see Brudzynski, 2007;Knutson et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

Asymmetrical stimulus generalization following differential fear conditioning

Bang

Allen

Jones

et al. 2008

Neurobiology of Learning and Memory

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Rodent ultrasonic vocalizations (USVs) are ethologically critical social signals. Rats emit 22 kHz USVs and 50 kHz USVs, respectively, in conjunction with negative and positive affective states. Little is known about what controls emotional reactivity to these social signals. Using male SpragueDawley rats, we examined unconditional and conditional freezing behavior in response to the following auditory stimuli: three 22 kHz USVs, a discontinuous tone whose frequency and on-off pattern matched one of the USVs, a continuous tone with the same or lower frequencies, a 4 kHz discontinuous tone with an on-off pattern matched to one of the USVs, and a 50 kHz USV. There were no differences among these stimuli in terms of the unconditional elicitation of freezing behavior. Thus, the stimuli were equally neutral before conditioning. During differential fear conditioning, one of these stimuli (the CS + ) always co-terminated with a footshock unconditional stimulus (US) and another stimulus (the CS − ) was explicitly unpaired with the US. There were no significant differences among these cues in CS + -elicited freezing behavior. Thus, the stimuli were equally salient or effective as cues in supporting fear conditioning. When the CS + was a 22 kHz USV or a similar stimulus, rats discriminated based on the principal frequency and/or the temporal pattern of the stimulus. However, when these same stimuli served as the CS − , discrimination failed due to generalization from the CS + . Thus, the stimuli differed markedly in the specificity of conditioning. This strikingly asymmetrical stimulus generalization is a novel bias in discrimination.

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Section: Introductionmentioning

confidence: 99%

Asymmetrical stimulus generalization following differential fear conditioning

Bang

Allen

Jones

et al. 2008

Neurobiology of Learning and Memory

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“…Ultrasonic vocalizations in the 22-25 kHz range are reliably emitted in aversive situations and are believed to reflect an unpleasant emotional-affective state such as fear and anxiety. Ultrasonic vocalizations are sensitive to drugs affecting anxiety-like behavior such as diazepam and morphine; they correlate with anxiety-like behavior in the EPM test and are organized in the limbic system, including the amygdala (Borta et al, 2006;Calvino et al, 1996;Hodgson et al, 2008;Jourdan et al, 1995;Knutson et al, 2002;Ko et al, 2005;Neugebauer et al, 2007;Oliveira and Barros, 2006). We analyzed the duration (total time spent vocalizing) rather than rate of vocalizations because the duration has been shown to be a more sensitive measure of anxiolytic and antidepressant efficacy (Hodgson et al, 2008).…”

Section: Discussionmentioning

confidence: 99%

“…The total duration of vocalizations (arithmetic sum of the duration of individual events) was recorded for 1 min, starting with the onset of the mechanical stimulus. Audible and ultrasonic vocalizations reflect supraspinally organized nocifensive and affective responses to aversive stimuli (Borszcz and Leaton, 2003;Borta et al, 2006;Calvino et al, 1996;Hodgson et al, 2008;Jourdan et al, 1995;Knutson et al, 2002;Ko et al, 2005;Neugebauer et al, 2007;Oliveira and Barros, 2006;Yu et al, 2002).…”

Section: Audible and Ultrasonic Vocalizationsmentioning

confidence: 99%

“…Ultrasonic vocalizations in the 22-25 kHz range are emitted in various unconditioned and conditioned aversive situations and reflect an unpleasant emotional-affective state (Borta et al, 2006;Calvino et al, 1996;Hodgson et al, 2008;Jourdan et al, 1995;Knutson et al, 2002;Ko et al, 2005;Neugebauer et al, 2007;Oliveira and Barros, 2006). Ultrasonic vocalizations evoked by innocuous (500g/30 mm 2 ) and noxious (2000g/30 mm 2 ) stimulation of the knee were measured before and during administration of drugs or vehicle (ACSF) into the CeA (Fig.…”

Section: Ultrasonic Vocalizationsmentioning

confidence: 99%

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Group III mGluR7 and mGluR8 in the amygdala differentially modulate nocifensive and affective pain behaviors

Palazzo

et al. 2008

Neuropharmacology

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SummaryThe amygdala plays an important role in the emotional-affective component of pain and in pain modulation. Group III metabotropic glutamate receptors (mGluRs) regulate pain-related activity in the amygdala, but the behavioral consequence and contribution of individual subtypes are not known yet. The present study determined the effects of mGluR7 and mGluR8 activation in the central nucleus of the amygdala (CeA) on nocifensive and affective pain responses and on pain-related anxiety-like behavior of adult rats. The pain state was induced by intraarticular injections of kaolin/carrageenan into one knee joint to produce a localized monoarthritis. Subtype-selective agonists were administered into the CeA by microdialysis in normal rats and in rats with arthritis. An mGluR7-selective agonist (N,N I -dibenzyhydryl-ethane-1,2-diamine dihydrochloride, AMN082, 25 µM) decreased spinal withdrawal reflex thresholds and increased audible and ultrasonic vocalizations evoked by brief (15 s) compression of the knee. AMN082 also decreased the open-arm preference in the elevated plus maze (EPM) test, suggesting anxiety-like behavior. In arthritic animals, however, AMN082 failed to modulate the increased spinal reflexes and vocalizations and anxiety-like behavior. An mGluR8-selective agonist (S-3,4-dicarboxyphenylglycine, S-3,4-DCPG, 10 µM) had no effect in normal animals but inhibited the increased spinal reflex responses and audible and ultrasonic vocalizations of arthritic rats. S-3,4-DCPG also increased the open-arm choices of arthritic rats, suggesting anxiolytic effects. The results suggest that under normal conditions mGluR7, but not mGluR8, facilitates pain responses and has anxiogenic properties whereas mGluR8, but not mGluR7, can inhibit nocifensive and affective behaviors and anxiety in a model of arthritic pain.

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“…Low frequency vocalizations, often termed 22-kHz calls, are emitted when rats are exposed to predators [5], foot-shocks [6][7][8][9][10], during inter-male aggression [11,12], drug withdrawal [13,14], handling [15], and social isolation [16]. Remarkably, anxiolytic drugs can reduce such vocalizations [17][18][19].…”

Section: Introductionmentioning

confidence: 99%

Social Transmission of Avoidance Behavior Under Situational Change in Learned and Unlearned Rats

2016

Animal Behavior

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Rats emit distinct types of ultrasonic vocalizations, which differ depending on age, the subject's current state and environmental factors. Since it was shown that 50-kHz calls can serve as indices of the animal's positive subjective state, they have received increasing experimental attention, and have successfully been used to study neurobiological mechanisms of positive affect. However, it is likely that such calls do not only reflect a positive affective state, but that they also serve a communicative purpose. Actually, rats emit the highest rates of 50-kHz calls typically during social interactions, like reproductive behavior, juvenile play and tickling. Furthermore, it was recently shown that rats emit 50-kHz calls after separation from conspecifics. The aim of the present study was to test the communicative value of such 50-kHz calls. In a first experiment, conducted in juvenile rats situated singly on a radial maze apparatus, we showed that 50-kHz calls can induce behavioral activation and approach responses, which were selective to 50-kHz signals, since presentation of 22-kHz calls, considered to be aversive or threat signals, led to behavioral inhibition. In two other experiments, we used either natural 50-kHz calls, which had been previously recorded from other rats, or artificial sine wave stimuli, which were identical to these calls with respect to peak frequency, call length and temporal appearance. These signals were presented to either juvenile (Exp. 2) or adult (Exp. 3) male rats. Our data clearly show that 50-kHz signals can induce approach behavior, an effect, which was more pronounced in juvenile rats and which was not selective to natural calls, especially in adult rats. The recipient rats also emitted some 50-kHz calls in response to call presentation, but this effect was observed only in adult subjects. Together, our data show that 50-kHz calls can serve communicative purposes, namely as a social signal, which increases the likelihood of approach in the recipient conspecific.

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Rat ultrasonic vocalization in aversively motivated situations and the role of individual differences in anxiety-related behavior

Cited by 160 publications

References 64 publications

Asymmetrical stimulus generalization following differential fear conditioning

Asymmetrical stimulus generalization following differential fear conditioning

Group III mGluR7 and mGluR8 in the amygdala differentially modulate nocifensive and affective pain behaviors

Social Transmission of Avoidance Behavior Under Situational Change in Learned and Unlearned Rats

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