Ultrasonic vocalizations of rats (Rattus norvegicus) during mating, play, and aggression: Behavioral concomitants, relationship to reward, and self-administration of playback..

Rats (Rattus norvegicus) emit a variety of ultrasonic vocalizations throughout their lifespan that reflect different forms of emotional arousal and accompanying affective states. In this study, high frequency recordings of ultrasonic vocalizations were made during mating, aggression, and both conspecific and heterospecific (dubbed "tickling") rough-and-tumble play behavior. We found that frequency modulated 50-kHz calls (trills and step calls) were positively correlated with positively valenced appetitive behavior during mating, play, and aggression. These calls were also positively correlated with the reward value of these social encounters. However, constant frequency (i.e., flat) 50-kHz calls were not related to appetitive behaviors or reward. In contrast, 22-kHz calls were positively related to aversive/withdrawal behaviors during mating, play, and aggression. Finally, we found that rats self-administered playback of frequency modulated 50-kHz trill calls and avoided playback of 22-kHz calls. Playback of flat 50-kHz calls or tape hiss was neutral. These results suggest that frequency modulated 50-kHz calls index a positively valenced, appetitive, social-emotional state in rats. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Influence of gonadal hormones and sexual behavior on ultrasonic vocalization in rats: II. Treatment of males.

Male Long-Evans rats were tested with estrous female rats in a divided cage to determine whether ultrasonic vocalizing varies as a function of recent sexual behavior or hormonal condition. In Exp I, when males were tested after 3 intromissions, a short latency to vocalization and a high rate of 50-kHz pulses occurred. 40% of the males changed their vocalization to 22-kHz pulses. With sexually fatigued males, long vocalization latencies and low vocalization rates were observed, and no males shifted to 22 kHz. Rates were intermediate with control males. In Exp II, a decline in vocalization rate occurred following castration of male rats compared with sham-operated controls. In both experiments the male nosed the screen divider during high-rate ultrasound production, maximizing contact with the female. Darting by females appeared only when ultrasonic pulse rates were high. The abrupt shift from 50- to 22-kHz vocalizing was characteristic of males with short intromission latencies. Data suggest that gradation of vocalization is correlated with the sexual readiness of the male and that vocalization may facilitate female darting behavior. (25 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)     

Vocal plasticity in budgerigars (Melopsittacus undulatus): Evidence for social factors in the learning of contact calls.

Recorded distance or contact calls of 6 unrelated adult male budgerigars before and during 8 wks of social contact. The 6 birds were housed in 2 separate groups of 3 each in adjoining cages. Birds in each cage could hear but not see the birds in the neighboring cage. At the beginning of the study, none of the birds shared any contact call types. The first appearance of 1 bird's imitation of a cagemate's contact call type occurred after 1 wk. Call type repertoires continued to change; some call types dropped out of the repertoires, and others were modified over time. Birds in the same cage shared the same dominant call type 8 wks later, and the dominant call types differed between the 2 cages. Thus, budgerigars can learn calls as adults, and call type convergence is achieved through mutual vocal imitation of social companions. In the absence of social but not aural contact, vocal imitation was greatly reduced. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

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)     

Long-term effects of early diazepam exposure on social differentiation in adult male rats subjected to the diving-for-food situation.

The present study was designed to investigate the consequences of a chronic diazepam (DZ) exposure (10 mg/kg/day) during the first 3 wks of life on social behavior of adult male rats measured in a situation of restricted access to food, the diving-for-food model. The treatment had no long-term effects on the acquisition of social roles related to feeding. However, DZ-exposed rats were less efficient than controls in carrying food from the feeder to the cage during the first session but were able to adapt and improve their performances during the second one. In the home cage, DZ-exposed rats were mom aggressive toward conspecifics than controls and compensated for their deficit of food by stealing it from the others. These results suggest that an early DZ exposure has long-term consequences on social behavior of rats, possibly reflecting a reduction of the level of emotionality. (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)     

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)     

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)     

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)     

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)     

Effects of halothane and isoflurane on beta-adrenoceptor-mediated responses in the vascular smooth muscle of rat aorta

The present study was designed to investigate the consequences of a chronic diazepam (DZ) exposure (10 mg/kg/day) during the first 3 weeks of life on social behavior of adult male rats measured in a situation of restricted access to food, the diving-for-food model. The treatment had no long-term effects on the acquisition of social roles related to feeding. However, DZ-exposed rats were less efficient than controls in carrying food from the feeder to the cage during the 1st session but were able to adapt and improve their performances during the 2nd one. In the home cage, DZ-exposed rats were more aggressive toward conspecifics than controls and compensated for their deficit of food by stealing it from the others. These results suggest that an early DZ exposure has long-term consequences on social behavior of rats, possibly reflecting a reduction of the level of emotionality.     

Brain regional neuropeptide changes resulting from social defeat.

Past work has demonstrated robust brain changes in cholecystokinin (CCK-8) following social defeat. Here the authors analyzed brain regional, CCK-8, substance P, corticotropin releasing factor (CRF), and neuropeptide Y levels in adult male Long-Evans rats defeated in a resident-intruder social aggression paradigm, as indexed by elevated bites received, freezing, and emission of 20-kHz calls. Brains harvested 6 hr after social defeat were dissected into 12 regions (olfactory bulbs, 3 cortical regions [frontal cortex, cortex above the basal ganglia, cortex above the diencephalon], caudate-putamen, basal forebrain, hypothalamus, hippocampus, thalamus, tectum, tegmentum, and lower brain stem). Neuropeptide radioimmunoassays demonstrated the following statistically significant regional changes in defeated rats as compared with nondefeated rats: CCK-8 was reduced in frontal cortex and cortex overlying diencephalon, the olfactory bulbs, caudate-putamen, hippocampus, tectum, and lower brainstem. Neuropeptide Y was elevated in the caudate-putamen. Substance P was elevated in the cortex over the basal ganglia and decreased in basal forebrain. CRF was diminished in the hippocampus. The results highlight more robust CCK modulation by social defeat as compared with 3 other neuropeptide systems involved in brain emotional regulation. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Influence of gonadal hormones and sexual behavior on ultrasonic vocalization in rats: I. Treatment of females.

Ultrasonic vocalizations were measured when male Long-Evans rats were placed with ovariectomized females that had experienced various hormonal and behavioral treatment. In Exp I, 18 males were tested with females in each of the following conditions: nonestrous (OVX), estrogen treated (E), estrogen and progesterone treated (EP), and estrogen and progesterone treated and given 2 intromissions from a stud male prior to testing (EPI). Control conditions included clean cage (CL) and cage soiled by an estrous female (SOI). The treatments differed in effect on rate and maintenance of vocalization, in the order of greatest to least: EP, E, EPI, and OVX (equal), SOI, and CL. In tests in which males produced a high rate of vocalization, some males with short intromission latencies shifted from the normal 50-kHz pulse to a 22-kHz pulse. In Exp II, the effect of the female's vocalization and movement on the rate of and latency to vocalization was measured. 21 males were presented with each of the following stimulus conditions: estrous female with red light (EP), estrous female without red light (EP dark), estrous anesthetized female (EP anes), and nonestrous anesthetized female (OVX anes). Effects on vocalization of various treatments were in descending order: EP and EP-dark (equal), EP anes, and OVX anes. Data suggest that the 50-kHz vocalizations constitute a graded response influenced by the female's hormonal and sexual condition. (16 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

The Effect of Therapist Availability on the Frequency of Patient-Initiated Between-Session Contact.

Does therapist availability affect the frequency of patient-initiated between-session phone contacts? There are few empirical data to inform therapists on this question: This study was designed to redress this literature gap. Results demonstrated that in general, therapists' availability policies did not strongly relate to patient-initiated contacts. However, there were some exceptions: The more willing therapists were to receive crisis intervention and mental status update calls, the fewer calls they received. Additionally, when therapists were less willing to be contacted between sessions, patients with personality disorders and/or poor global functioning tended to make more nonemergency calls to the therapist, whereas patients with elevated suicidality tended to make fewer nonemergency calls between sessions. The implications of the results on therapists' policies and patients' expectations are discussed. (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)     

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.     

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)     

P-selectin and MAC-1 mediate monocyte rolling and adhesion to ECM-bound platelets under flow conditions

Ultrasonic vocalizations were tape recorded from five pairs of copulating mice and subjected to spectrographic analysis. As expected, the mice emitted numerous 70-kHz vocalizations. At the beginning of the test, before copulation began, 70-kHz calls were emitted almost continuously, while calls with lower spectrographic frequencies were not observed. Subsequently, bursts of 70-kHz calling generally began shortly before mounts and intromissions and persisted until dismount. Intermixed with these 70-kHz calls were additional vocalizations of about 40 kHz. Calling rates were highest just prior to intromission. Once intromissions began, 70-kHz calls continued at a lower rate until dismount; however, 40-kHz calls occurred infrequently. In a second experiment, the male was found to emit the majority of the 70-kHz calls and all of the 40-kHz calls. When the male was devocalized, few calls were detected, regardless of whether the female was able to call. If the male was not devocalized, high rates of calling were detected, even if the female was devocalized.     

Ultrasonic vocalizations by male house mice (Mus musculus) to novel odors: Roles of infant and adult experience.

Conducted 2 experiments to examine 70-kHz ultrasonic courtship vocalizations by adult male mice to novel odors following exposure to these odors in infancy and/or adulthood. Exp I, with 72 males, demonstrated that adult males normally do not vocalize to the urine of female rats but would if adult female mice odorized with female rat urine were repeatedly encountered postpubertally. On the other hand, encountering their own mother odorized with female rat urine from birth until weaning did not promote vocalizations to the urine of female rats. Exp II, with 100 males, examined vocalizations to the urine of female mice whose urinary odor was altered by the ingestion of fenugreek, a spice. Greater amounts of vocalization again were seen by males that as adults encountered females that had ingested fenugreek. Again, experience with the novel odor during infancy was not associated with elevated vocalizations during adulthood either to fenugreek-altered urine or to the fenugreek odor itself. Vocalizations to 2 different novel odors occurred only after an adult male had encountered an adult female odorized with the novel odor. (57 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)