Maternal care, isolation-induced infant ultrasonic calling, and their relations to adult anxiety-related behavior in the rat.

In the rat, variations in maternal care affect the development of stable individual differences in anxiety-related behavior. Here, it was asked whether such experience-dependent differences can be detected already during early life. As a measure for anxiety in pups, isolation-induced ultrasonic vocalizations were used, and their dependency on different maternal behaviors, namely licking, retrieval behavior, and responsiveness to playback of pup calls, was tested. Consistent with reported differences of adult rats with high or low levels of maternal care experienced, the rarely licked offspring appeared to be more anxious, since they emitted more calls when separated from their mother and litter. Based on these findings, it was examined whether infant calling can be used as a predictor of adult anxiety-related behavior. Results show that infant call emission was negatively correlated with immobility and calling during fear conditioning. These relationships seem to be mediated at least partly by maternal care. In total, measuring ultrasonic vocalizations can provide information about an affective trait of infant and adult rats, which gives the opportunity to study the development of emotionality from early life onward. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Electrophysiological and ultrasonic correlates of reproductive behavior in the male rat.

Monitored the ultrasonic vocalizations of 13 male Long-Evans rats and determined the correlation of these vocalizations with electrophysiological activity measured by chronically implanted hippocampal and cortical electrodes during mating with a female rat. Hippocampal theta rhythms were significantly correlated with high activity, mounting, intromissions, and preejaculatory excitatory behavior and were also significantly associated with 50-kHz short ultrasonic vocalizations. Postmount or postintromission behaviors (grooming, exploration) were closely correlated with an absence of ultrasonic vocalizations and the onset of irregular low-amplitude hippocampal EEG recordings. Long 22-kHz vocalizations occurred during the postejaculatory refractory period. Shorter 22-kHz vocalizations occurred during mating and were associated with unsuccessful intromissions or mounting attempts. Postejaculatory long 22-kHz vocalizations were significantly associated with irregular high-amplitude hippocampal EEG tracings, while preejaculatory short 22-kHz vocalizations were also accompanied by sleeplike irregular high-amplitude hippocampal EEG tracings with cortical spindling. Findings suggest that ultrasonic vocalizations are indicators of the sexual arousal of mating rats. (14 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Social contacts and production of 50-kHz short ultrasonic calls in adult rats.

The goal of the study was to provide evidence that the production of 50-kHz calls by adult rats is driven by potential or direct social contacts. The calls have been studied during daily visits to a cage by single or paired rats. Repeated exposure of rats to the cage frequently visited by other rats or direct contact between rats significantly increased the number of 50-kHz calls. The increase in production of 50-kHz calls was reduced by 78% after intrapreoptic-anterior hypothalamic injection of MK-801, an N-methyl-D-aspartate-type glutamate receptor antagonist. Calls emitted in all situations had a similar acoustic profile. It was found that 50-kHz calls were produced in anticipation of, and/or during, direct social contacts among adult rats and were predominantly initiated by olfactory stimuli. The calls seem to express an appetitive behavioral state in which the central glutamatergic mechanism is implicated. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Nucleus accumbens amphetamine microinjections unconditionally elicit 50-kHz ultrasonic vocalizations in rats.

The authors have hypothesized that, in adult rats, 50-kHz ultrasonic vocalizations (USVs) index a state characterized by high arousal and expectations of reward. This study was conducted to investigate whether dopamine agonism of the nucleus accumbens (NAcc) could evoke such an appetitive state, by examining the effects of NAcc amphetamine (AMPH) microinjections on USVs. Intra-NAcc AMPH injections (0.3, 1.0, 3.0, 10.0 μg unilaterally) produced robust, dose-dependent increases in 50-kHz USVs, which could not be accounted for by concomitant increases in locomotor activity (LA). However, AMPH injections into dorsal control caudate putamen sites produced a modest, dose-dependent increase in LA without significant increases in 50-kHz USVs. These findings indicate that NAcc AMPH microinjections selectively evoke 50-kHz USVs in rats, supporting the notion that dopamine elevations in the NAcc may unconditionally elicit a state of reward anticipation. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Identification of types II, IX and X collagens at the insertion site of the bovine achilles tendon

The authors provide initial documentation that juvenile rats emit short, high-frequency ultrasonic vocalizations (high USVs, approximately 55 kHz) during rough-and-tumble play. In an observational study, they further observe that these vocalizations both correlate with and predict appetitive components of the play behavioral repertoire. Additional experiments characterized eliciting conditions for high USVs. Without prior play exposure, rats separated by a screen vocalized less than playing rats, but after only 1 play session, separated rats vocalized more than playing rats. This findings suggested that high USVs were linked to a motivational state rather than specific play behaviors or general activity. Furthermore, individual rats vocalized more in a chamber associated with play than in a habituated control chamber. Finally, congruent and incongruent motivational manipulations modulated vocalization expression. Although play deprivation enhanced high USVs, an arousing but aversive stimulus (bright light) reduced them. Taken together, these findings suggest that high USVs may index an appetitive motivation to play in juvenile rats.     

Changes in mating vocalizations over the ejaculatory series in rats (Rattus norvegicus).

Rats (Rattus norvegicus) produce ultrasonic calls during mating. We examined changes in the structure and pattern of such vocalizations over the ejaculatory series. In Experiment 1, vocalizations were recorded from 11 pairs of rats through 3 ejaculatory series and analyzed spectrographically. We classified 4 categories of call by spectral frequency and duration. Calls of low frequency, long duration, and high intensity occurred more often shortly before the ejaculation and were associated with mounting without intromission, a behavior that often occurs shortly before ejaculation. The high-frequency calls did not vary in number across the series. In Experiment 2, vocalizations were recorded from males paired with devocalized females. Males produced all vocalization patterns produced by pairs in Experiment 1. Results suggest that most pre-ejaculatory calls are produced by males and may potentially affect female sexual behavior. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Anticipation of play elicits high-frequency ultrasonic vocalizations in young rats.

The authors provide initial documentation that juvenile rats emit short, high-frequency ultrasonic vocalizations (high USVs, ～55 kHz) during rough-and-tumble play. In an observational study, they further observe that these vocalizations both correlate with and predict appetitive components of the play behavioral repertoire. Additional experiments characterized eliciting conditions for high USVs. Without prior play exposure, rats separated by a screen vocalized less than playing rats, but after only 1 play session, separated rats vocalized more than playing rats. This finding suggested that high USVs were linked to a motivational state rather than specific play behaviors or general activity. Furthermore, individual rats vocalized more in a chamber associated with play than in a habituated control chamber. Finally, congruent and incongruent motivational manipulations modulated vocalization expression. Although play deprivation enhanced high USVs, an arousing but aversive stimulus (bright light) reduced them. Taken together, these findings suggest that high USVs may index an appetitive motivation to play in juvenile rats. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Analysis of ultrasonic vocalizations emitted by intruders during aggressive encounters among rats (Rattus norvegicus).

Determined the ultrasonic vocalizations produced by intruders during aggressive interactions and investigated the role of these signals in agonistic behavior of rats. In Exp I, 7 experienced resident male Long-Evans rats were paired with both devocalized and intact vocalizing naive intruder males (n?=?14). Devocalization of the intruder males resulted in a drastic decrease in 50-kHz vocalizations and the elimination of all 22-kHz vocalizations. This almost total absence of ultrasonic vocalizations was not accompanied by any change in resident aggressive behavior or intruder defensive and submissive behavior. In Exp II, 16 naive intruders were tested with either deafened or intact resident males (n?=?8). Similarly, preventing residents from hearing intruder ultrasounds had no detectable effect on any aggressive behavior. These experiments are not consistent with the correlative evidence that intruder-produced 22-kHz vocalizations inhibit the aggressive behavior of the resident. Results show that most of the ultrasonic vocalizations emitted during aggressive encounters were probably produced by the intruder. (10 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Reduction of dopamine synaptic activity: Degradation of 50-khz ultrasonic vocalization in rats.

Vocal deficits are prevalent and debilitating in Parkinson's disease. These deficits may be related to the initial pathology of the nigrostriatal dopamine neurons and resulting dopamine depletion, which contributes to dysfunction of fine motor control in multiple functions. Although vocalization in animals and humans may differ in many respects, we evaluated complex (50-kHz) ultrasonic mate calls in 2 rat models of Parkinson's disease, including unilateral infusions of 6-hydroxydopamine to the medial forebrain bundle and peripheral administration of a nonakinesia dose of the dopamine antagonist haloperidol. We examined the effects of these treatments on multiple aspects of the acoustic signal. The number of trill-like (frequency modulated) 50-kHz calls was significantly reduced, and appeared to be replaced by simpler (flat) calls. The bandwidth and maximum intensity of simple and frequency-modulated calls were significantly decreased, but call duration was not. Our findings suggest that the nigrostriatal dopamine pathway is involved to some extent in fine sensorimotor function that includes USV production and complexity. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Male-produced ultrasonic vocalizations and mating patterns in female rats.

Investigated the influence of male-produced 50-kHz vocalizations on mating behavior and choice of partner in estrous female rats. In Exp I, 17 estrous female Long-Evans rats were given a mating-choice test; 2 tethered males, one of which was devocalized, were used as incentives. Darting was directed toward the vocalizing male more frequently than toward the muted test partner, but ultrasonic vocalizations had no influence on visit rate or the amount of time that the females spent with each male. When 2 intact or 2 muted males were used as stimulus objects, the females' solicitation behavior was more evenly distributed between the 2 males. In Exp II, 16 estrous females were given a mating-choice test between 2 muted males; tape-recorded 50-kHz vocalizations or tape hiss was transmitted from a speaker located behind one of the males. Females spent equal amounts of time with the tethered males in both the vocalization and tape-hiss conditions; however, females directed more darting toward the males that were tethered in front of the speaker transmitting the ultrasonic vocalizations than toward the other muted tethered males. Findings demonstrate that the principal function of the male-produced ultrasounds is to facilitate and orient the solicitation behavior of the estrous female during mating. The vocalizations have little demonstrable effect in attracting the female to the immediate physical proximity of the male. (22 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Anticipation of rewarding electrical brain stimulation evokes ultrasonic vocalization in rats.

Adult rats emit increased rates of 50-kHz ultrasonic vocalizations (USVs) before receiving social and pharmacological rewards. This study sought to determine whether anticipation of rewarding electrical stimulation of the brain (ESB) would also elicit these vocalizations. In Experiments 1 and 2, rats showed increased 50-kHz USVs before receiving experimenter-delivered ventral tegmental area (VTA) and lateral hypothalamic (LHy) ESB on a fixed time 20-s schedule. In Experiments 3 and 4, rats increased their rate of 50-kHz USVs in response to cues that predicted the opportunity to self-stimulate the VTA or LHy. Interestingly, unexpected termination of either type of ESB evoked 20-kHz, rather than 50-kHz, USVs. In Experiment 5, a cue that predicted daily 1-hr feeding sessions increased 50-kHz USVs, whereas a cue that predicted footshock decreased 50-kHz USVs. These effects could not be explained simply by changes in locomotor activity or general arousal. Together, these findings support the hypothesis that short 50-kHz USVs may selectively index a state of reward anticipation in rats. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Relation between 22-kHz ultrasonic signals and sociosexual behavior in rats.

The copulatory performance of male rats, tested in a large seminaturalistic environment, was assessed to determine the relation between 22-kHz ultrasonic vocalizations and a range of sociosexual behaviors. The 7 sexually experienced Charles River male rats were tested until sexual exhaustion. Ultrasonic signals were shown to occur in a wider range of sociosexual circumstances than previously reported; for example, the calls occurred in particular social circumstances during the preejaculatory period as well as during the postejaculatory interval. There was no consistent evidence that the emission of this call during the postejaculatory period consistently functions to keep the female away from the male. The nature and occurrence of postejaculatory ultrasonic signals showed increasing variability in successive ejaculatory series. The results of this and previous studies are interpreted within a semiotic theory of communication. The 22-kHz call is described as a message that makes available the information that the sender is in a socially depressed and withdrawn state. (14 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Primate vocalizations during social separation and aggression: effects of alcohol and benzodiazepines

The most common group of squirrel monkey vocalizations, peeps, are emitted during different social situations including social separation, affiliative interactions, feeding and aggressive confrontations. The present experiments investigated whether peeps and other vocalizations emitted during different social contexts are pharmacologically altered in a similar manner. First, vocalizations were characterized during (1) social separation in juveniles, and (2) "resident-intruder" aggressive confrontations between dominant monkeys from different social groups. Then, the effects of alcohol (EtOH) and the benzodiazepine chlordiazepoxide (CDP) on vocalizations during social separation and during aggression were examined. Isolated juveniles emitted only one type of call, the isolation peep. Resident monkeys primarily emitted peeps, but also emitted cackles, chucks, noisy calls and pulsed calls. Aggressive peeps were similar in structure and frequency (kHz) to isolation peeps, but were shorter in duration. At the same doses, both CDP (0.3-3 mg/kg) and EtOH (0.1-1.0 g/kg) reduced explosive motor behaviors and isolation peeps in juvenile monkeys during social separation and increased threat displays and aggression peeps in resident monkeys during confrontations with an intruder monkey from a different social group. Thus, similarly structured vocalizations that were emitted during social separation and aggression were very sensitive to EtOH and CDP, but the social context determined the direction and magnitude of effects.     

Cooperative behavior of laboratory rats (Rattus norvegicus) in an instrumental task.

Cooperation is a cognitively demanding, complex social behavior, found primarily in primates. Here we investigated mutualism in rats (Rattus Norvegicus), a simple form of cooperation in which two subjects work on operant task, receiving immediate and simultaneous sucrose reward for a joint action. To receive the sucrose reward, familiar pairs of rats were required to nose poke simultaneously. Following 44 training days, we examined the relation of social contact and ultrasonic vocalizations to the rat's cooperative behavior by testing the effects of inserting opaque, wire-mesh, or no partition - between subjects. Cooperative behavior (simultaneous nose-poking): (a) increased gradually during initial training; (b) decreased with the opaque partition (restricting visual, acoustic, and physical communication); (c) increased with a wire mesh partition restricting only physical contact); and (d) increased with the number of 50 kHz USV “happy” calls and the intensity of social interaction. The possibility of studying the development of cooperative behavior in laboratory rats using a simple procedure based on commercially available equipment may prove useful in modeling determinants of social behavior. (PsycINFO Database Record (c) 2011 APA, all rights reserved)     

The role of gonadal steroid receptor activation in the restoration of sociosexual behavior in adult male rats

This work tested the hypothesis that gonadal steroid receptor activation was necessary for the restoration of several sociosexual behaviors (such as copulatory behavior, partner preference, 50-kHz vocalizations, and scent marking) in testosterone-treated gonadectomized male rats. Gonadal steroid receptors were blocked by systemic administration of the antiandrogen hydroxyflutamide, the antiestrogen RU 58668, or both antagonists simultaneously in a restoration paradigm. Inhibiting androgen receptors with hydroxyflutamide blocked the restoration of male copulatory behavior, partner preference (time spent with a sexually receptive female over a nonreceptive female), 50-kHz ultrasonic vocalizations, and scent marking. On the other hand, we did not find that blocking estrogen receptors with RU 58668 inhibited the restoration of copulatory behavior or partner preference in testosterone-treated gonadectomized male rats, even though the level of brain nuclear estrogen receptor occupation was significantly reduced to the level found in gonadectomized males. However, the restoration of scent marking and 50-kHz vocalizations were impaired by RU 58668. Blocking both nuclear androgen and estrogen receptors with the two antagonists simultaneously did not have a greater inhibitory effect than treatment with each antagonist alone. Therefore, the activation of nuclear estrogen receptors is necessary for the restoration of some, but not all, sociosexual behaviors, which are also androgen receptor-dependent. Besides nuclear estrogen receptors, there are additional, but unknown, targets of estradiol that play a role in mediating copulatory behavior in adult male rats. Moreover, the signals from multiple gonadal steroid signaling pathways converge in the regulation of some sociosexual behaviors in adult male rats.     

Fear conditioning to discontinuous auditory cues requires perirhinal cortical function.

Pretraining lesions of rat perirhinal (PR) cortex impair fear conditioning to ultrasonic vocalizations (USVs) but have no effect on conditioning to continuous tones. This study attempted to deconstruct USVs into simpler stimulus features that cause fear conditioning to be PR-dependent. Rats were conditioned to one of three cues: a multicall 19-kHz USV, a 19-kHz discontinuous tone, and a 19-kHz continuous tone. The discontinuous tone duplicated the on/off pattern of the individual calls in the USV, but it lacked the characteristic frequency modulations. Well-localized neurotoxic PR lesions impaired conditioning to the USV, the discontinuous tone, and the training context. However, PR lesions had no effect on conditioning to the continuous tone. The authors suggest that the lesion effects on fear conditioning to both cues and contexts reflect the essential role of PR in binding stimulus elements together into unitary representations. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Sexual dimorphism in ultrasonic vocalizations of mice (Mus musculus): Gonadal hormone regulation.

Male mice, during courtship and sexual behavior, vocalize substantially more 70-kHz ultrasounds than do females. Four experiments conducted with 109 male and female DBA/2J and ADK2F? mice demonstrated that testosterone propionate (TP) substantially increased ultrasonic emissions and mounting by ovariectomized females and that long-term gonadectomized males and females increased their amount of ultrasound production in response to TP to approximately the same levels. From these results it is suggested that the sexual dimorphism normally seen in ultrasonic vocalizations can be accounted for by the activational effects of androgen in adulthood. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Analysis of ultrasonic vocalizations emitted by residents during aggressive encounters among rats (Rattus norvegicus).

Determined the extent to which aggressive resident rats emit 40–70-kHz vocalizations and the effect of these signals on intruders. In Exp I, 16 deafened and intact intruder male Long-Evans rats were given 2 encounters with 8 resident Ss. Deafened intruders engaged in a higher duration of immobile or freezing postures than intact Ss. Exp II indicated that the augmentation of freezing found among deafened intruders was not due to an inability to detect ultrasounds made by residents since intruders encountering devocalized resident males showed no reliable differences in specific motor patterns from intruders paired with intact residents. Results demonstrate that 40–70-kHz vocalizations were produced almost entirely by intruding Ss since there were no significant changes in occurrence of these calls when resident males were devocalized. (13 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Ultrasounds during agonistic interactions between female rats (Rattus norvegicus).

Defensive and vocal behaviors of 18 female Long-Evans rats (Rattus norvegicus) in encounters with aggressive, lactating conspecifics were examined in order to determine if female rats emit ultrasounds during agonistic interactions and to characterize any such calls. The Ss, selected during estrus or diestrus, were exposed to 1-min attacks at 25-min intervals. Between attacks the Ss were threatened by the aggressor but protected by a wire-mesh cage. Female rats emitted both high- (32–60 kHz) and low-frequency (20–32 kHz) ultrasonic calls in agonistic encounters, with the rate of high-frequency calls enhanced during estrus. Low-frequency ultrasounds were shorter in duration and higher in frequency than those emitted by male rats in similar conditions. It is concluded that female rats emit ultrasonic calls during defensive responding and that the characteristics and rate of calling vary as functions of sex and gonadal hormone state. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Responses of White-Faced Capuchins (Cebus capucinus) to Naturalistic and Experimentally Presented Food-Associated Calls.

In the context of foraging, many animal species produce specific calls that attract others. Researchers hypothesize that these vocalizations function to inform others about food; however, few studies have investigated whether food-associated calls alone are sufficient to cause individuals to respond as if they have been informed about food. Playback experiments on white-faced capuchins (Cebus capucinus) investigated whether listeners could infer the presence of food merely by hearing food-associated calls. Recipients looked significantly longer toward the call source and approached the speaker more often after hearing food-associated calls, as compared with control calls. Because these responses are not indicative of feeding, it is unclear whether listeners associated the calls with food. Nonetheless, these responses, specific to food-associated calls, may increase individuals' chances of finding food. (PsycINFO Database Record (c) 2010 APA, all rights reserved)