Ultrasonic Calls Research Articles

Courtship ultrasonic vocalizations and social status in mice

A series of experiments was conducted to investigate whether the poorer sexual performance of subordinate than dominant male mice, Mus domesticus, was linked to lower sexual motivation. Ultrasonic calls uttered by a male in the presence of a female were used as an index of sexual interest. Males were housed in pairs for 5 days and dominant/subordinate roles were assigned. Subordinates, when tested in their home cage immediately after the removal of the dominant male, uttered more ultrasounds than the latter. When the dominant male was tested before the subordinate, there was no difference in the number of ultrasounds uttered and the subordinates' performance was consistently poorer. The fewer calls recorded when subordinate males were tested after the dominant partner was not associated with less defence/escape behaviour, nor could it be explained as habituation to female odour, as a consequence of being tested after the dominant partner. Within sexually experienced pairs, the urine of dominant males interacting with a female for 3 min reduced the number of ultrasounds uttered by the subordinate in the presence of a female. It is suggested that an inhibitory factor in the dominant male's urine functions as an indirect competitive mechanism when direct competition is prevented by removing the dominant subject.

Long Ultrasonic Calls in Male Rats Following Mating, Defeat and Aversive Stimulation: Frequency Modulation and Bout Structure

Abstract Ultrasonic calls by rats may represent affective expressions and serve communicative functions. The temporal patterning and frequency modulation of the long, 21-30 kHz ultrasonic calls were studied in 7 male rats. Following ejaculation, defeat and aversive stimulation large samples of consecutive long calls were recorded and analyzed off-line using a spectrum analyzer. The analysis was limited to long calls because other types of calls were relatively rare under the circumstances of this study and the emitter could be determined by a typical breathing pattern with reasonable certainty only for long calls. Log survivor analysis of the intervals between calls revealed that rats emit 95 % of long calls in bouts of less than 6 calls. Except for the higher bout rate after defeat, there were no significant differences between tests in call duration, percent time spent vocalizing, bout duration and intervals between bouts. However, there were significant differences between individuals across tests in call duration, number of calls per bout and bout rate. The pattern and capacity to breathe are likely important limiting factors for several temporal characteristics of rat ultrasounds, in particular maximal call duration and range of interval duration within a bout. Post-ejaculatory calls were often strongly modulated in frequency (i.e. pitch) in the medial and terminal segments. These segments of calls emitted after defeat or aversive stimulation were essentially monotonous. We propose that rats emit at least 2 types of long ultrasonic calls-one monotonous, the other modulated-each reflecting a different affective state of the animal. The modulated type may reflect a state of behavioral inhibition such as initiated by ejaculation whereas the monotonous type may reflect a state of intense fear induced by an actual physical threat in situations where escape is blocked. Both types may serve a "desist-contact" function.

Infant rat separation is a sensitive test for novel anxiolytics

1. Rat pups emit ultrasonic calls during brief episodes of social separation. These calls have been variously described as “distress” calls and may be related to the separation cries expressed by the young of many mammalian species. 2. Ultrasonic call of rat pups are modulated by environmental stimuli such as ambient temperature, olfactory and tactile stimuli associated with the nest. 3. Calls are also sensitive to a variety of purported anxiolytic and anxiogenic drugs, including the benzodiazepines, serotonin agonists, and ligands at the NMDA-glycine receptor complex. 4. In addition to providing a simple test for the anxiolytic properties of drugs, this model may also provide new insights about the development and neurobiology of anxiety.

Rat pup isolation calls are reduced by functional antagonists of the NMDA receptor

Compounds that reduce ion flux through N-methyl-D-aspartate (NMDA) coupled cation channels were evaluated for their effects on rat pup ultrasonic vocalizations (USV). Previous studies have demonstrated that rat pups emit ultrasonic calls during social isolation and that several classes of anxiolytics decrease, while putative anxiogenics increase, the number of these calls. The competitive NMDA antagonists 2-amino-7-phosphonoheptanoic acid (AP-7) and (±)-3-(2-carboxypiperazin-4-yl)-propyl-1-phosphonic acid (±)-CPP) as well as a partial agonist at the strych-nine-i glycine receptor, 1-aminocyclopropanecarboxylic acid (ACPC), reduced USV at doses that did not affect either motor activity or core temperature. A dose of glycine sufficient to elevate hippocampal glycine concentrations by 85% antagonized the effects of ACPC, but not AP-7. Glycine alone did not alter USV, but NMDA when given by itself increased USV by almost 50% at subconvulsant doses. Moreover, a dose of NMDA that did not affect USV antagonized the effects of AP-7 but not ACPC. Taken together, these findings are consistent with previous studies using conflict procedures which indicate that agents which reduce activity at NMDA receptor coupled cation channels may constitute a new class of anxiolytic agents.

Startle-inducing acoustic stimuli evoke ultrasonic vocalization in the rat

The present study demonstrates that acoustic stimuli which induce a startle response (ASR) also evoke ultrasonic vocalization in the rat. Sound recordings were done on three consecutive days of testing during sessions of 20 acoustic stimuli each and on the following day for three minutes following 5 acoustic stimuli (nonstimulus condition). Startle-inducing stimuli evoked continuous ultrasonic calling which was maintained throughout testing. Immediately following each acoustic stimulus, however, vocalization was interrupted by a period of silence (gap). The mean duration of sounds was reduced and the interpulse interval tended to increase during acoustic stimulation as compared to the nonstimulus condition. It is concluded that startle-eliciting stimuli induce a state of fear in the rat and that the acoustic-startle-elicited ultrasonic vocalization may provide a novel model in the study of anxiety.

Behavioural changes in the offspring of rats exposed to diazepam during gestation

Primiparous pregnant Sprague-Dawley dams were administered a single daily sc. injection of diazepam (0.1 and 1 mg/kg) or vehicle over gestation days 14–20. No differences in neonatal mortality and weight gain were found between the control and diazepam-exposed pups. Conversely, male pups prenatally treated with this benzodiazepine exhibited subtle behavioural alterations either during early postnatal life or during adulthood. In particular, a significant decrease in the locomotor activity of the diazepam-treated groups was found at the end of the second postnatal week (14–16 days). Furthermore, the administration of diazepam during gestation produced marked changes in the length of ultrasonic calls of rat pups removed from their nest. Finally, adult male rats (120 days of age) prenatally exposed to diazepam showed a notable impairment in copulatory activity as well as a significant decrease in the duration of ultrasonic (22 kHz) post-ejaculatory calls emitted during sexual behaviour. These findings suggest that late gestational exposure to diazepam induces both short- and long-term behavioural changes in rat offspring, changes characterized by altered activity patterns and emotional-motivational responsiveness to environmental challenges.

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.

Dissociation of hypothalamic effects on ultrasound production and copulation

Two studies were conducted to compare the brain mechanisms for copulation with those controlling other sexual behaviors, such as the ultrasonic calls that help hamsters and other rodents attact potential mates. Specifically, male and female golden hamsters were castrated and hormone-primed prior to being observed for rates of ultrasound production and levels of sex-typical copulatory behavior (mounts, intromissions and ejaculations in males; lordosis in females). Such tests were conducted before and after subjects received sham operations or bilateral lesions of the preoptic area (POA), anterior hypothalamus (AH) or ventromedial hypothalamus (VMN). The results confirmed previous work in showing the POA lesions decrease rates of intromission, ejaculation and ultrasound production, while VMH lesions decrease lordosis duration. More surprising was the tendency of VMN lesions to increase rates of ultrasonic calling by both males and females. For males, these effects identify differences between the neural circuits controlling copulatory and noncopulatory sexual behaviors. For females, they suggest a mechanism for the behavioral incompatibility of ultrasound production and lordosis. In particular, they raise the possibility that the suspension of ultrasonic calling that normally accompanies lordosis reflects an increase in VMN activity that simultaneously provokes lordosis and inhibits vocalization.

Ultrasonic vocalizations by male hamsters: parameters of calling and effects of playbacks on female behaviour

Male and female hamsters, Mesocricetus auratus, were observed during prolonged matings. Ultrasonic vocalizations by the male were frequent initially and declined during testing, but were positively associated with the duration of female lordosis. Most calls were uttered while sniffing the female, although early in the test period when most ejaculations were occurring, high rates were also observed during non-contact behaviour such as grooming. Following exposure to the first female, introduction of a novel female stimulated the return of high rates of male calling. In a follow-up experiment, males uttered more ultrasonic calls in the 30-s period following ejaculation than in the preceding 30-s interval. These results provide evidence that males utter ultrasonic vocalizations that enhance lordosis during extended sexual interactions, and that the patterns of male calling are consistent with behaviours that maintain receptivity and ensure successful fertilization. Two other experiments examined whether different male calls have different effects on female behaviour. Males utter at least two structurally distinct types of ultrasonic vocalizations during sexual behaviour: one is produced during interaction with a female in lordosis (during-female), and the second is uttered following removal of the female (post-female). In the first experiment, playbacks of during- and post-female calls were equally effective in prolonging the duration of lordosis in females relative to taped noise. In a second experiment, however, tape-recorded post-female calls induced more ultrasonic vocalizations from females than during-female calls; both call types elicited more calling from females than taped noise. Therefore, although there were differences in potency, during- and post-female calls did not differ in the types of responses elicited from females under two different conditions. Thus, these male calls induce context-appropriate responses in females. In a final eperiment, structural differences were found in the male vocalizations occurring just before and after ejaculation. Together, these experiments show that ultrasonic vocalizations by male hamsters consistently vary in rate and structure during sexual interactions, and suggest that the responses of females may vary accordingly.

The emission and elicitation of mouse ultrasonic vocalizations: The effects of age, sex and gonadal status

‘Subject’ mice of varying gonadal status (castrate males; intact or neonatally gonadectomized females and males) were paired for 3-min with intact ‘stimulus’ females and ultrasonic vocalizations were monitored. Vocalization patterns from home cages differed from the test pairings. The results suggested that the age, experience and gonadal status of the subject influenced the vocalizations from the pair. As the source of ultrasonic calls from these vocally intact pairs could not be individually identified, the ‘subjects’ were paired with a range of ultrasonically silent (inferior laryngeal nerve-transected) stimulus animals. Vocalizations were detected from all combinations of animals. Gonadally intact females were most effective in eliciting ultrasonic vocalizations from the subjects and gonadally intact males were least effective. The responses of castrate males were lower than from intact males. Anesthetized adults of either sex elicited only poor vocalization responses from other adults. Ultrasonic calls have often previously been studied using vocally intact ‘subject’ and ‘stimulus’ animals: the present results confirm the difficulty of establishing who is who in such situations.

クマネズミと Wistar 系ラットの幼獣における超音波コール

クマネズミと Wistar 系ラットの幼獣における超音波コール

The influence of psychotropic drugs on the ultrasonic calling of mouse pups.

The influence of a range of commonly used psychotherapeutic drugs on the ultrasonic calling of mouse pups was assessed. The major tranquilizers chlorpromazine and haloperidol were without effect. Whereas tranylcypromine and imipramine were also inactive, amitriptyline suppressed the rate of calling. Some anxiolytic compounds such as meprobamate and amobarbital were without influence, although others such as diazepam, chlordiazepoxide and ipsapirone decreased the number of calls. The influence of these drugs on body temperature was measured, as it is known to markedly influence the rate of ultrasonic calling. Although six out of ten drugs decreased body temperature, there was no evidence that this was related to the rate of ultrasonic calling. The possibility that the recording of ultrasonic calls could be used to screen for psychotropic activity is discussed.

Prenatal antagonism of stress by naltrexone administration: early and long-lasting effects on emotional behaviors in mice.

The effects of prenatal exposure to stress and to naltrexone on emotional behaviors were studied in CD1 mice during ontogeny and in the adulthood. During ontogeny (a) lower body weights were initially found in pups born by mothers injected with naltrexone; (b) treatments did not affect sensory motor development except in the case of the cliff aversion reflex which occurred earlier in pups prenatally exposed to stress; (c) measures of ultrasonic vocalizations in stressful context showed that the amount of vocalizations emitted by pups born by stressed mothers was significantly higher than that emitted by pups born by naltrexone injected and control mothers (d) an examination of mother-offspring interactions on the very first day of observation indicated a consistent trend in stressed mothers to be more responsive to their pups. In adulthood, ultrasonic calls in courtship after short and long periods of isolation showed a time-dependent decrease of vocalizations in males prenatally exposed to naltrexone. These results indicate that the modifications of emotionality evident during early development are directly related to the reactivity of the mothers to the experimental treatments.

Effects of prenatal exposure to methyl mercury on ultrasonic calling in rat pups

Effects of prenatal exposure to methyl mercury on ultrasonic calling in rat pups

Ultrasonic vocalization in response to unavoidable aversive stimuli in rats: Effects of benzodiazepines

The effects of two benzodiazepine derivatives (diazepam, 0.5–1 mg/kg; alprazolam, 1.25 – 2.5 mg/kg) on ultrasonic calling elicited in adult rats by unavoidable aversive stimuli (footshocks) were investigated. The results show that either diazepam or alprazolam affected the duration of ultrasonic calls. In particular, a significant decrease in the length of ultrasounds was found in the group of animals treated with these benzodiazepines. The effects of diazepam were counteracted by the benzodiazepine-antagonist Ro 15–1788. On the other hand, neither a neuroleptic agent, such as haloperidol (0.5 – 1 mg/kg), nor an antidepressant, such as desipramine (5 – 10 mg/kg) influenced the parameters of ultrasonic emission in this experimental situation. The present results suggest that ultrasonic vocalization in response to unavoidable aversive stimuli could be considered as a potential new tool for studying drugs with antianxiety properties.

Mating System, Mate Choice and Ultrasonic Calling in a Zaprochiline Katydid (Orthoptera: Tettigoniidae)

We describe sexual communication and the mating system of an undescribed genus of zaprochiline katydid. Males produce an ultrasonic calling song described as a series of simple pulses at a carrier frequency near 50 kHz. Zaprochilines contrast with most other katydids in having a narrow diet consisting of pollen. Males in nature exhibited a resource-defence mating system by calling in choruses near flowers which were attractive to females. We determined whether females discriminated among calling males as mates. An early-season sample of male calls showed a correlation between song frequency and both body size and the size of the glands that produce a large, nutritious spermatophore which is eaten by the female. The prediction that larger males would have a mating advantage over small individuals was supported in laboratory experiments. However, examination of paired males in nature failed to reveal any evidence of such a mating advantage. Furthermore, in other laboratory experiments it was found that females preferred high frequency call models, representative of small males, over low frequency calls. It is suggested that females do not prefer calls of large males because only in the early part of the season does male song give information on the size of the male and his spermatophore glands. In addition, spermatophore nutrients may be less important to the nutrition of female zaprochiline than other katydiyds, due to the high-protein pollen diet of this species. Since higher frequencies of calls show relatively greater attenuation with distance, the high frequency calls preferred by females may be perceived as males calling closeby.

Mother-offspring interaction and pup development in genetically deaf mice.

The role of ultrasonic calls emitted by pups on maternal behavior has been investigated by using genetically deaf (dn/dn) and normal-hearing (+/+) mice of the GFF strain. The behavior and the sensory-motor development of unfostered and cross-fostered pups, as well as the behavior of the mothers, was analyzed. Deaf pups emitted fewer ultrasonic calls than pups with normal hearing. The cross-fostering procedure decreased the amount of vocalizations produced by normal pups, thus stressing the reinforcement effect of maternal behavior on pups' ultrasonic communication. No difference in maternal behavior emerged between deaf and normal-hearing mothers toward their pups. However, cross-fostered pups received less maternal care than pups raised by their natural mothers, this effect being more evident in deaf pups reared by mothers with normal hearing, than vice versa. Deafness, in both mothers and pups, seemed to be associated with increased locomotor activity, possibly to offset their auditory handicap in mother-offspring relationships. Furthermore, deaf pups showed a faster gain in weight than normal pups, this capability being affected by the genotype of the rearing parent. On the whole, these data could suggest that maternal behavior in deaf mice has became independent of ultrasonic stimuli emitted by the pups. Other biobehavioral characteristics of deaf mice indicate a more active role played by these pups in mother-offspring interaction in comparison with pups with normal hearing.

Chronic exposure to a novel odor increases pups' vocalizations, maternal care, and alters dopaminergic functioning in developing mice

This study was designed to assess the stress effect of manipulation of the olfactory environment in developing mice. In a first experiment it was found that mouse pups could be stressed (as measured by an increase in ultrasonic calls) by removing the litter from the dam for 15 min/day for the first 14 days of life and exposing them to a novel odor (clean bedding). This stress procedure also produced a long-term modification in maternal behavior. The stress response (ultrasounds) and the modification of maternal behavior were prevented by providing the litter with home cage bedding during maternal separation. In a second experiment it was demonstrated that early stress influenced apomorphine-induced wall climbing behavior in 15-day-old mice, suggesting stress-induced alterations in the dopaminergic system. Pups exposed to clean bedding during infancy exhibited more wall climbing behavior than pups never separated from the mother. Moreover, preventing the early stress response during mother-offspring separation, by providing pups with home cage bedding, eliminated the increase in apomorphine-induced wall climbing. Taken together these results suggest that olfactory cues are decisive in characterizing stressful situations inducing both immediate and long-lasting effects in mouse pups.

Ultrasonic vocalization in rat pups: Effects of early postnatal exposure to SCH 23390 (a DA 1-receptor antagonist) and sulpiride (a DA 2-receptor antagonist)

Early postnatal administration of SCH 23390 and sulpiride induced marked changes in the ultrasonic vocalization elicited by the removal of rat pups from their nest. In particular, SCH 23390 produced a significant increase in the length, as well as in the sound pressure level, of ultrasonic calls; moreover, a significant decrease in minimum and maximum frequency values was found in pups treated with this DA 1-receptor antagonist. Sulpiride significantly reduced the rate of calling, as well as the pressure level of sounds, whereas it did not influence other parameters of the ultrasonic emission. These behavioural alterations seemed to be the consequence of an impaired functional maturation of the dopamine (DA) system; however, the different changes caused by SCH 23390 and sulpiride, respectively, suggest that DA 1- and DA 2-receptor populations could play a distinct role in the ultrasonic calling during early postnatal life.

Genetic influences on ultrasonic vocalizations in young mice.

Ultrasonic calls produced by young mice elicit maternal investigation and retrieval, and their characteristics have been shown to vary with age and genotype. In this study, we completed a full Mendelian cross of two inbred strains BALB/cJ and DBA/2J. The major result was the detection of directional dominance for a high rate of calling. Other characteristics were influenced by additive and maternal effects in the absence of directional dominance. We estimate the number of loci involved in the rate of calling to be about 1—facilitating studies of a gene-to-behavior pathway.