Low-frequency sound communication by mouse pups (Mus musculus): wriggling calls release maternal behaviour

Low-frequency calls (wriggling calls), emitted mainly between days 2 and 15 after birth by mouse pups while pushing for the teats during suckling by the mother, are studied with regard to their significance in intraspecific communication. Wriggling calls release maternal behaviour and ‘attention’ responses in the mother. Licking of the pups is the most prominent maternal response, followed by changes of suckling position and by nest building. One function of the wriggling calls is to keep these maternal behaviours at a high level: otherwise their spontaneous rates of occurrence would decrease rapidly after the birth of the pups. Maternal and attention responses can be released in females lying on paralysed pups by playbacks of wriggling calls. The behavioural contexts of the production of wriggling calls and pure ultrasounds are mutually exclusive and the perception and recognition of each type of pup call cannot be confused by the mother.     

Development of echolocation and communication vocalizations in the big brown bat, <Emphasis Type="Italic">Eptesicus fuscus</Emphasis>

Big brown bats form large maternity colonies of up to 200 mothers and their pups. If pups are separated from their mothers, they can locate each other using vocalizations. The goal of this study was to systematically characterize the development of echolocation and communication calls from birth through adulthood to determine whether they develop from a common precursor at the same or different rates, or whether both types are present initially. Three females and their six pups were isolated from our captive breeding colony. We recorded vocal activity from postnatal day 1 to 35, both when the pups were isolated and when they were reunited with their mothers. At birth, pups exclusively emitted isolation calls, with a fundamental frequency range <20 kHz, and duration >30 ms. By the middle of week 1, different types of vocalizations began to emerge. Starting in week 2, pups in the presence of their mothers emitted sounds that resembled adult communication vocalizations, with a lower frequency range and longer durations than isolation calls or echolocation signals. During weeks 2 and 3, these vocalizations were extremely heterogeneous, suggesting that the pups went through a babbling stage before establishing a repertoire of stereotyped adult vocalizations around week 4. By week 4, vocalizations emitted when pups were alone were identical to adult echolocation signals. Echolocation and communication signals both appear to develop from the isolation call, diverging during week 2 and continuing to develop at different rates for several weeks until the adult vocal repertoire is established.     

Individual variation in pup vocalizations and absence of behavioral signs of maternal vocal recognition in Weddell seals (Leptonychotes weddellii)

Individually stereotyped vocalizations often play an important role in relocation of offspring in gregarious breeders. In phocids, mothers often alternate between foraging at sea and attending their pup. Pup calls are individually distinctive in various phocid species. However, experimental evidence for maternal recognition is rare. In this study, we recorded Weddell seal (Leptonychotes weddellii) pup vocalizations at two whelping patches in Atka Bay, Antarctica, and explored individual vocal variation based on eight vocal parameters. Overall, 58% of calls were correctly classified according to individual. For males (n= 12) and females (n= 9), respectively, nine and seven individuals were correctly identified based on vocal parameters. To investigate whether mothers respond differently to calls of familiar vs. unfamiliar pups, we conducted playback experiments with 21 mothers. Maternal responses did not differ between playbacks of own, familiar, and unfamiliar pup calls. We suggest that Weddell seal pup calls may need to contain only a critical amount of individually distinct information because mothers and pups use a combination of sensory modalities for identification. However, it cannot be excluded that pup developmental factors and differing environmental factors between colonies affect pup acoustic behavior and the role of acoustic cues in the relocation process.     

VOCAL INDIVIDUALITY IN MOTHER AND PUP SOUTH AMERICAN FUR SEALS, ARCTOCEPHALUS AUSTRALIS

South American fur seals breeding in Peru are subjected to levels of maternal aggression, and subsequent pup mortality, that are higher than has been reported for any other otariid species. For mothers and pups to maintain contact with each other, a mutual recognition system should exist to facilitate reunion and avoid misdirection of maternal effort. We recorded vocalizations of mothers and pups at Punta San Juan, Peru, during the 1994 and 1995 breeding seasons. Sixteen acoustic variables were measured from a total of 560 calls from 15 mothers and 13 pups. Multivariate analysis showed that calls were variable in several acoustic dimensions. While calls of both mothers and pups showed low variability within and high variability among individuals, mothers' calls were more individualistic. On average, discriminant-function analysis correctly assigned 60% of pup calls and 70% of mother calls to the individual that produced them. Characteristics of the fundamental frequency were most important for distinguishing among mothers, while pup calls, which typically contained less harmonic structure, could be differentiated by formant-like frequency ranges. Thus, calls of mother and pup South American fur seals appear to exhibit sufficient stereotypy to allow for recognition and discrimination among individuals.     

How mothers find their pups in a colony of Antarctic fur seals

In Antarctic fur seals, Arctocephalus gazella, mothers must identify their own young among hundreds or even thousands of pups, if they are to invest in their own offspring and avoid misdirecting their parental care. When returning to their breeding colony from a foraging trip of several days at sea, mothers have to find and identify their young before suckling can occur. There appears to be little confusion about which pup belongs to a mother, and adoption is absent or rare. Using behavioral observations, we investigated the means by which female Antarctic fur seals identified their pups in a breeding colony of about 750 mother-pup pairs on Kerguelen Island. We evaluated the importance of vision, scent communication, vocalizations, and rendezvous locations as possible explanations of how mothers find their pups. Every pup that a mother examined, whether her own or not, exchanged naso-nasal inspection with her, suggesting a strong role for olfactory communication in individual recognition. Both mothers and pups called to each other, and mothers that searched for pups over a longer period gave more calls and encountered more pups. Thus, vocalizations may have been used to attract pups that might be offspring. Nursing usually occurred in the same place from the end of one maternal visit to the colony and the arrival at the beginning of the next visit, suggesting that nursing locations may serve as a meeting place, or rendezvous, for mothers and pups. These results suggest that finding pups is a two-stage process for females, in which pups for sampling are attracted by calls or examined at the previous nursing location, and then individual identification is made by olfactory cues.     

Isolation calls and retrieving behavior in laboratory and wild-derived golden hamsters—No sign for inbreeding depression

Isolated juvenile golden hamsters produce ultrasonic and audible vocalizations, so-called isolation calls, as a reaction to being separated from their mother and nest and their cooling down. Their aim is to stimulate mothers to search and retrieve the pups. In this work, the vocalization of juvenile laboratory (Zoh:GOHA; Institute of Zoology, Martin-Luther-University Halle-Wittenberg) and juvenile wild-derived golden hamsters (captured in northern Syria and southern Turkey) from birth up to the age of 18 days were digitally recorded, analyzed and compared using an ultrasonic microphone and the software Avisoft. Furthermore, the retrieving behavior of the mothers was observed and compared. The results showed that the number of isolation calls was age-specific and the structure of the calls was influenced by body temperature, body mass and sex of the pups. The age of the pups determined retrieval by the maternal golden hamsters; however these did not discriminate between their own pups or foreign pups. In spite of enormous genetic differences between wild-derived and laboratory golden hamsters, only minor differences between the strains were found.     

Perception of Vocal Tract Resonances by Whooping Cranes Grus americana

Although formants (vocal tract resonances) can often be observed in avian vocalizations, and several bird species have been shown to perceive formants in human speech sounds, no studies have examined formant perception in birds' own species-specific calls. We used playbacks of computer-synthesized crane calls in a modified habituation—dishabituation paradigm to test for formant perception in whooping cranes ( Grus americana ). After habituating birds to recordings of natural contact calls, we played a synthesized replica of one of the habituating stimuli as a control to ensure that the synthesizer worked adequately; birds dishabituated in only one of 13 cases. Then, we played the same call with its formant frequencies shifted. The birds dishabituated to the formant-shifted calls in 10 out of 12 playbacks. These data suggest that cranes perceive and attend to changes in formant frequencies in their own species-specific vocalizations, and are consistent with the hypothesis that formants can provide acoustic cues to individuality and body size.     

Reduction in Ultrasonic Vocalizations in Pups Born to Rapid Eye Movement Sleep Restricted Mothers in Rat Model

The effects of rapid eye movement sleep restriction (REMSR) in rats during late pregnancy were studied on the ultrasonic vocalizations (USVs) made by the pups. USVs are distress calls inaudible to human ears. Rapid eye movement (REM) sleep was restricted in one group of pregnant rats for 22 hours, starting from gestational day 14 to 20, using standard single platform method. The USVs of male pups were recorded after a brief isolation from their mother for two minutes on alternate post-natal days, from day one till weaning. The USVs were recorded using microphones and were analysed qualitatively and quantitatively using SASPro software. Control pups produced maximum vocalization on post-natal days 9 to 11. In comparison, the pups born to REMSR mothers showed not only a reduction in vocalization but also a delay in peak call making days. The experimental group showed variations in the types and characteristics of call types, and alteration in temporal profile. The blunting of distress call making response in these pups indicates that maternal sleep plays a role in regulating the neural development involved in vocalizations and possibly in shaping the emotional behaviour in neonates. It is suggested that the reduced ultrasonic vocalizations can be utilized as a reliable early marker for affective state in rat pups. Such impaired vocalization responses could provide an important lead in understanding mother-child bonding for an optimal cognitive development during post-partum life. This is the first report showing a potential link between maternal REM sleep deprivation and the vocalization in neonates and infants.     

Influence of experience on the representation of the “mothering call” in frontoparietal and auditory cortex of pups of the rodent Octodon degus : FDG mapping

Several types and subtypes of vocalizations which have a behavioral impact on degu pups were identified. Among these the complex “mothering call” which is exclusively uttered by females and first during extensive nursing periods in the nest is a candidate for filial learning. In ¹⁴C-2-fluoro-2-deoxyglucose (FDG) experiments two-weeks-old pups raised by normal mothers showed higher metabolic activity in somatosensory frontoparietal and frontal cortex upon play back of a mothering call than pups raised by muted mothers. It is suggested that pups learn to associate the mothering call with close body contact with their mother early in life. In addition, FDG representation of the call, of its components and of tone and noise stimuli were studied in degu auditory cortex. Five fields and some aspects of tonotopic organization were identified. The mothering call activated all fields, but with more spatial extent of labeling in normally raised pups. A rostral field was activated by play-back of the mothering call, noise, and two-tone sequences, but hardly by single-frequency tones and the narrow-band component of the mothering call. Accepted: 13 August 1997     

Juvenile vocalizations ofCtenomys talarum (Rodentia: Octodontidae)

We analysed the physical structure and functional interpretation of juvenile vocalizations ofCtenomys talarum Thomas, 1898. Two sounds, one true vocalization (care-elicitation call) and one mechanical sound (nursing sound) were recorded during the nestling period. Care-elicitation calls were emitted by isolated pups and caused the mother to respond by immediately approaching the pups to take care of them. This maternal response to the care-elicitation calls ofC. talarum pups, together with the production of these vocalizations during the first weeks after birth, when pups depend exclusively on their mother to obtain food and maintain their body temperature, give preliminary support for the recent theory that care-elicitation cries are honest advertisements of offspring need.     

Comprehensive Analysis of Ultrasonic Vocalizations in a Mouse Model of Fragile X Syndrome Reveals Limited, Call Type Specific Deficits

Fragile X syndrome (FXS) is a well-recognized form of inherited mental retardation, caused by a mutation in the fragile X mental retardation 1 (Fmr1) gene. The gene is located on the long arm of the X chromosome and encodes fragile X mental retardation protein (FMRP). Absence of FMRP in fragile X patients as well as in Fmr1 knockout (KO) mice results, among other changes, in abnormal dendritic spine formation and altered synaptic plasticity in the neocortex and hippocampus. Clinical features of FXS include cognitive impairment, anxiety, abnormal social interaction, mental retardation, motor coordination and speech articulation deficits. Mouse pups generate ultrasonic vocalizations (USVs) when isolated from their mothers. Whether those social ultrasonic vocalizations are deficient in mouse models of FXS is unknown. Here we compared isolation-induced USVs generated by pups of Fmr1-KO mice with those of their wild type (WT) littermates. Though the total number of calls was not significantly different between genotypes, a detailed analysis of 10 different categories of calls revealed that loss of Fmr1 expression in mice causes limited and call-type specific deficits in ultrasonic vocalization: the carrier frequency of flat calls was higher, the percentage of downward calls was lower and that the frequency range of complex calls was wider in Fmr1-KO mice compared to their WT littermates.     

Which Call Parameters Signal Threat to Conspecifics in White‐Throated Magpie‐Jay Mobbing Calls?

Abstract Variation in signals often encodes additional information beyond that provided by the main signal. Many species communicate degree of threat using such signal variation. However, multiple signal parameters often covary with threat level, and it is unclear whether receivers are using variation along one or more parameters when assessing threat level. White-throated magpie-jays ( Calocitta formosa ) vary several call parameters when mobbing, and here I report on an experiment testing whether such variation contains information used by conspecific receivers, and which parameters are salient to receivers. I collected data on natural mobbing sequences in two threat contexts and found that mobbing calls were highly variable in both length and inter-call interval, but on average, both parameters were shorter in high threat contexts, while call frequency did not differ. To determine how jays respond to such between-context variation, I conducted a playback experiment in which call length and inter-call interval were independently varied in a factorial design. This is one of the first studies to my knowledge to deconstruct and independently test covarying signal parameters in an anti-predator signaling system. Magpie-jays responded more often to treatments with either short call lengths or short inter-call intervals, in concordance with the natural calling data. However, the two parameters did not appear to act independently; responses were not additive, and short calls at short inter-call intervals elicited no stronger of a response than short calls at long intervals or long calls at short intervals. Receivers can use either parameter when assessing threat level. These data demonstrate that mobbing can signal threat level, that call length and call rate are redundant, and that receivers need not use both to determine whether to approach.     

Bats and frogs and animals in between: evidence for a common central timing mechanism to extract periodicity pitch

Widely divergent vertebrates share a common central temporal mechanism for representing periodicities of acoustic waveform events. In the auditory nerve, periodicities corresponding to frequencies or rates from about 10 Hz to over 1,000 Hz are extracted from pure tones, from low-frequency complex sounds (e.g., 1st harmonic in bullfrog calls), from mid-frequency sounds with low-frequency modulations (e.g., amplitude modulation rates in cat vocalizations), and from time intervals between high-frequency transients (e.g., pulse-echo delay in bat sonar). Time locking of neuronal responses to periodicities from about 50 ms down to 4 ms or less (about 20–300 Hz) is preserved in the auditory midbrain, where responses are dispersed across many neurons with different onset latencies from 4–5 to 20–50 ms. Midbrain latency distributions are wide enough to encompass two or more repetitions of successive acoustic events, so that responses to multiple, successive periods are ongoing simultaneously in different midbrain neurons. These latencies have a previously unnoticed periodic temporal pattern that determines the specific times for the dispersed on-responses.     

Early maternal recognition of offspring vocalizations in rhesus macaques (Macaca mulatta)

This study investigated the development of maternal recognition of infant calls in rhesus macaques (Macaca mulatta). Fifteen mothers and their offspring, of age ranging from several hours to 28 days, served as subjects of an experiment in which the offspring's distress vocalizations were recorded and then played back to their mothers simultaneously with those of an age-matched control infant. The proportion of time looking at, but not the proportion of orientations to the speaker playing the offspring's vocalizations increased significantly as a function of infant age. Specifically, mothers of infants older than 1 week of age responded longer to the playback of their own infant's calls than did mothers of younger infants. These findings provide the firt evidence that offspring recognition in macaques develops between the first and second week of the infant's life and are consistent with the hypothesis that mothers need to be exposed to their infants' calls in order to learn their acoustic characteristics.     

Asic3?/? Female Mice with Hearing Deficit Affects Social Development of Pups

Background

Infant crying is an important cue for mothers to respond adequately. Inappropriate response to infant crying can hinder social development in infants. In rodents, the pup-mother interaction largely depends on pup''s calls. Mouse pups emit high frequency to ultrasonic vocalization (2–90 kHz) to communicate with their dam for maternal care. However, little is known about how the maternal response to infant crying or pup calls affects social development over the long term.

Methodology/Principal Findings

Here we used mice lacking acid-sensing ion channel 3 (Asic3^−/−) to create a hearing deficit to probe the effect of caregiver hearing on maternal care and adolescent social development. Female Asic3^−/− mice showed elevated hearing thresholds for low to ultrasonic frequency (4–32 kHz) on auditory brain stem response, which thus hindered their response to their pups'' wriggling calls and ultrasonic vocalization, as well as their retrieval of pups. In adolescence, pups reared by Asic3^−/− mice showed a social deficit in juvenile social behaviors as compared with those reared by wild-type or heterozygous dams. The social-deficit phenotype in juvenile mice reared by Asic3^−/− mice was associated with the reduced serotonin transmission of the brain. However, Asic3^−/− pups cross-fostered to wild-type dams showed rescued social deficit.

Conclusions/Significance

Inadequate response to pups'' calls as a result of ASIC3-dependent hearing loss confers maternal deficits in caregivers and social development deficits in their young.     

The effects of time,space and spectrum on auditory grouping in túngara frogs

Male túngara frogs (Physalaemus pustulosus) produce complex calls consisting of two components, a ~350 ms FM sweep called the “whine” followed by up to seven ~40 ms harmonic bursts called “chucks”. In order to choose and locate a calling male, females attending to choruses must group call components into auditory streams to correctly assign calls to their sources. Previously we showed that spatial cues play a limited role in grouping: calls with normal spectra and temporal structure are grouped over wide angular separations (≤135°). In this study we again use phonotaxis to first test whether an alternative cue, the sequence of call components, plays a role in auditory grouping and second, whether grouping is mediated by peripheral or central mechanisms. We found that while grouping is not limited to the natural call sequence, it does vary with the relative onset times of the two calls. To test whether overlapping stimulation in the periphery is required for grouping, the whine and chuck were filtered to restrict their spectra to the sensitivity ranges of the amphibian and basilar papillae, respectively. For these dichotic-like stimuli, grouping still occurred (albeit only to 45° separation), suggesting that stream formation is mediated by central mechanisms.     

Psycholinguistic analyses of alarm calls of Japanese monkeys (Macaca fuscata fuscata)

Alarm and estrous calls emitted by Japanese macaques were recorded and analyzed in the Arashiyama West and East groups. Their responses to natural calls as well as to synthesized versions varying in the acoustic parameters that defined the vocalizations were studied. The response patterns shown by Arashiyama West group members, which were subject to a distinct change with only a slight difference of a single parameter, appeared to reflect strict underlying perceptual boundaries. This was analogous to the categorical perception that humans show with speech sounds. In contrast, continuous perception was exhibited by Arashiyama East group individuals. When several sounds were played back in combination to the former group, following stimuli were recognized by quite different cues from those by which the first sound was perceived. The groups' differences in vocal perception are discussed in terms of the ecological differences of the environments they inhabit.     

Absentee Mothering – Not So Absent? Responses of European Rabbit (Oryctolagus cuniculus) Mothers to Pup Distress Calls

Longer‐range acoustic parent‐offspring communication is widespread, but might be absent in species in which young are hidden in burrows during the mother's absence. The European rabbit (Oryctolagus cuniculus) is such a species, with unusually limited maternal care largely restricted to a short daily nursing bout. Based, however, on evidence of frequent infanticide in this species, we hypothesize that rabbits possess a mechanism promoting a maternal response to pup distress calls. We conducted playback experiments with distress calls of pre‐weaning pups played next to the breeding burrows of mothers in a field enclosure (i.e. next to the burrows where mothers give birth and raise their young). Calls were played shortly after pups were born (T1) when infanticide risk is maximal, and shortly before the pups start dispersing from the breeding burrow (T2). A high proportion of mothers (60.6%) responded to pup calls by rapidly returning to their breeding burrow and 40% of them investigated the area around the entrance. Return responses to the playback of pup calls did not differ between mothers during T1 and T2. Thus, our results confirm that rabbit mothers respond rapidly to pup distress calls and that this responsiveness may adaptively serve to repel potentially infanticidal females.     

Translating mouse vocalizations: prosody and frequency modulation1

Mental illness can include impaired abilities to express emotions or respond to the emotions of others. Speech provides a mechanism for expressing emotions, by both what words are spoken and by the melody or intonation of speech (prosody). Through the perception of variations in prosody, an individual can detect changes in another's emotional state. Prosodic features of mouse ultrasonic vocalizations (USVs), indicated by changes in frequency and amplitude, also convey information. Dams retrieve pups that emit separation calls, females approach males emitting solicitous calls, and mice can become fearful of a cue associated with the vocalizations of a distressed conspecific. Because acoustic features of mouse USVs respond to drugs and genetic manipulations that influence reward circuits, USV analysis can be employed to examine how genes influence social motivation, affect regulation, and communication. The purpose of this review is to discuss how genetic and developmental factors influence aspects of the mouse vocal repertoire and how mice respond to the vocalizations of their conspecifics. To generate falsifiable hypotheses about the emotional content of particular calls, this review addresses USV analysis within the framework of affective neuroscience (e.g. measures of motivated behavior such as conditioned place preference tests, brain activity and systemic physiology). Suggested future studies include employment of an expanded array of physiological and statistical approaches to identify the salient acoustic features of mouse vocalizations. We are particularly interested in rearing environments that incorporate sufficient spatial and temporal complexity to familiarize developing mice with a broader array of affective states.     

人为疼痛刺激下金色中仓鼠幼鼠叫声的发育过程

金色中仓鼠幼鼠可以利用可听声和超声信号与母鼠进行交流,这些声音可以反映个体的寒冷、饥饿、疼痛等不同生理状态和需求。因疼痛诱发的叫声对于维持幼鼠的存活也有着重要意义。本实验通过录制人为疼痛刺激下,不同日龄金色中仓鼠的叫声,分析并比较了5 - 30 日龄金色中仓鼠不同发声信号特征(可听声出现频次、可听声持续时程、可听声主频率、超声出现频次、超声持续时程、超声主频率)的性别差异;同时记录了幼鼠的两种发声随日龄的变化趋势。结果发现:幼鼠两种叫声的各种参数均未表现性二型现象。幼鼠超声发生频次随日龄增加而逐渐减少。而可听声却正相反,随日龄增加而逐渐上升,并在20 日龄时达到最高峰,之后逐渐下降。可听声持续时程也随日龄而增加。综上,在人为疼痛刺激下,随着日龄增加,幼鼠更倾向于使用可听 声而非超声与母兽进行交流。