Vocalization Rate Research Articles

Variations in maternal behavior in rats selected for infant ultrasonic vocalization in isolation

Individual differences in maternal behavior in rodents are associated with altered physiology and behavior in offspring across their lifespan and across generations. Offspring of rat dams that engage in high frequencies of high-arched-back nursing and pup-licking (High-LG) show attenuated stress responses compared to those engaging in lower frequencies (Low-LG). Selective breeding also produces widespread alterations in physiology and behavior that are stable over generations. To examine processes underlying generational and developmental influences on anxiety in an animal model, we developed two lines of rats that emit either extremely high (High-USV) or low (Low-USV) rates of 45kHz ultrasonic vocalizations in isolation at postnatal day 10. Compared to the Low-USV line, High-USV rats display increased indices of anxiety- and depression-like behavior in adulthood. The current study assessed maternal behaviors as well as oxytocin and vasopressin receptor density in High-USV and Low-USV dams to determine if selective breeding had produced differences that paralleled those found in Low- and High-LG dams. We found that Low-USV dams engage in more high-arched nursing and pup-licking than High-USV dams. Differences in oxytocin and vasopressin receptor levels were not widespread throughout the brain, with line differences in the piriform cortex and nucleus accumbens. This research illustrates the potential interplay between genetically determined (USV line) and environmental (postnatal mother–infant interactions) factors in accounting for the phenotypes associated with maternal separation induced postnatal vocalizations.

Does vocal learning accelerate acoustic diversification? Evolution of contact calls in Neotropical parrots.

Learning has been traditionally thought to accelerate the evolutionary change of behavioural traits. We evaluated the evolutionary rate of learned vocalizations and the interplay of morphology and ecology in the evolution of these signals. We examined contact calls of 51 species of Neotropical parrots from the tribe Arini. Parrots are ideal subjects due to their wide range of body sizes and habitats, and their open-ended vocal learning that allows them to modify their calls throughout life. We estimated the evolutionary rate of acoustic parameters of parrot contact calls and compared them to those of morphological traits and habitat. We also evaluated the effect of body mass, bill length, vegetation density and species interactions on acoustic parameters of contact calls while controlling for phylogeny. Evolutionary rates of acoustic parameters did not differ from those of our predictor variables except for spectral entropy, which had a significantly slower rate of evolution. We found support for correlated evolution of call duration, and fundamental and peak frequencies with body mass, and of fundamental frequency with bill length. The degree of sympatry between species did not have a significant effect on acoustic parameters. Our results suggest that parrot contact calls, which are learned acoustic signals, show evolutionary rates similar to those of morphological traits. This is the first study to our knowledge to provide evidence that change through cultural evolution does not necessarily accelerate the evolutionary rate of traits acquired through life-long vocal learning.

The immediate and subsequent effects of response interruption and redirection on vocal stereotypy, motor stereotypy and heart rate

ABSTRACTA three-component multiple-schedule analysis was used to evaluate the immediate and subsequent effects of response interruption and redirection (RIRD) with stimulus control (SC) on levels of motor and vocal stereotypy and heart rate in a 19-year-old male with autism. After a wristband was established as a discriminative stimulus for implementation of RIRD contingent on engagement in motor or vocal stereotypy, the present treatment evaluation was conducted. During baseline sessions, there were no planned consequences for stereotypy. During treatment sessions, RIRD was implemented contingent on each event of targeted stereotypy. Motor and vocal stereotypies were evaluated using 5-s partial interval recording (PIR) and heart rate was monitored via momentary time sampling. Results showed that RIRD with SC produced immediate reductions in motor and vocal stereotypy to near-zero rates during treatment and did not produce subsequent increases in stereotypy when the intervention was removed. Heart rate remained consistent across all conditions. Following the above analysis, generalization probes were carried out in three additional settings. The utility of including SC procedures when implementing RIRD, considerations in using heart rate as a measure of distress, and avenues for future research is discussed.

Female mice ultrasonically interact with males during courtship displays.

During courtship males attract females with elaborate behaviors. In mice, these displays include ultrasonic vocalizations. Ultrasonic courtship vocalizations were previously attributed to the courting male, despite evidence that both sexes produce virtually indistinguishable vocalizations. Because of this similarity, and the difficulty of assigning vocalizations to individuals, the vocal contribution of each individual during courtship is unknown. To address this question, we developed a microphone array system to localize vocalizations from socially interacting, individual adult mice. With this system, we show that female mice vocally interact with males during courtship. Males and females jointly increased their vocalization rates during chases. Furthermore, a female's participation in these vocal interactions may function as a signal that indicates a state of increased receptivity. Our results reveal a novel form of vocal communication during mouse courtship, and lay the groundwork for a mechanistic dissection of communication during social behavior.

Maternal buffering of stress response in free‐ranging Pacific harbor seal pups in Alaska

AbstractWe examined the effects of maternal buffering in free‐ranging Pacific harbor seal pups during capture and handling research procedures. We predicted that pups held with their mother would benefit from social buffering and exhibit lower cortisol concentrations resulting from capture and handling than dependent pups caught without their mothers and weaned pups. We expected that pups captured with their mother that experienced a short separation would exhibit increased stress‐induced vocal behavior and activity level compared to dependent weaned pups caught alone. The results showed that the presence of the mother significantly buffered the stress response, as measured by reduced serum cortisol concentrations, in pups captured with their mothers as compared to dependent pups captured alone. Cortisol concentrations of mothers with pups initially were higher than nonlactating females, then diminished. Pups showed a significantly higher rate of vocalization soon after maternal separation compared to single pups separated for a longer period of time. Newly separated pups, especially males, showed a high level of activity compared to the other pups. The results provide unique quantitative evidence of the physiology underlying the maternal‐pup bond in a marine mammal, and the role that maternal buffering may play on the stress response of the offspring.

Prenatal exposure to a common organophosphate insecticide delays motor development in a mouse model of idiopathic autism.

Autism spectrum disorders are characterized by impaired social and communicative skills and repetitive behaviors. Emerging evidence supported the hypothesis that these neurodevelopmental disorders may result from a combination of genetic susceptibility and exposure to environmental toxins in early developmental phases. This study assessed the effects of prenatal exposure to chlorpyrifos (CPF), a widely diffused organophosphate insecticide endowed with developmental neurotoxicity at sub-toxic doses, in the BTBR T+tf/J mouse strain, a validated model of idiopathic autism that displays several behavioral traits relevant to the autism spectrum. To this aim, pregnant BTBR mice were administered from gestational day 14 to 17 with either vehicle or CPF at a dose of 6 mg/kg/bw by oral gavages. Offspring of both sexes underwent assessment of early developmental milestones, including somatic growth, motor behavior and ultrasound vocalization. To evaluate the potential long-term effects of CPF, two different social behavior patterns typically altered in the BTBR strain (free social interaction with a same-sex companion in females, or interaction with a sexually receptive female in males) were also examined in the two sexes at adulthood. Our findings indicate significant effects of CPF on somatic growth and neonatal motor patterns. CPF treated pups showed reduced weight gain, delayed motor maturation (i.e., persistency of immature patterns such as pivoting at the expenses of coordinated locomotion) and a trend to enhanced ultrasound vocalization. At adulthood, CPF associated alterations were found in males only: the altered pattern of investigation of a sexual partner, previously described in BTBR mice, was enhanced in CPF males, and associated to increased ultrasonic vocalization rate. These findings strengthen the need of future studies to evaluate the role of environmental chemicals in the etiology of neurodevelopment disorders.

Infrasound in mating displays: a peacock's tale

Male peafowl display to females with erection and movement of their elaborately ornamented train. We hypothesized that the male's concave train serves as a radiator of acoustic signals, and thus examined both the production and perception of acoustic signals associated with these displays in Indian peafowl, Pavo cristatus. We discovered that male train displays produced infrasonic signals, which were perceived by both male and female peafowl. Both males and females responded to a subset of infrasonic signals by increasing the time they spent walking/running and being alert during playbacks relative to baseline controls. Male peafowl also increased rates of vocalization in response to infrasonic signals, but not to audible train-based signals. The apparent intra- and intersexual saliency of these signals suggests that they play a potent role in peafowl social signalling. Infrasonic signals are likely adaptive in the peacock's natural habitat, as they would attenuate minimally as they are propagated through dense vegetation that otherwise would attenuate high frequencies in audible signals and obstruct visual signals.

Playful handling of laboratory rats is more beneficial when applied before than after routine injections

The ability of positive affective states to counteract negative states engendered by routine medical procedures remains poorly studied. In laboratory rats, positive affect typically associated with rough-and-tumble play can be induced through human “hand play” – the experience of being “tickled” by a human in a manner mimicking the social interactions normally occurring during physical–social play. We hypothesized that administering playful tickles before and/or after routine intra-peritoneal (IP) injections would reduce the aversiveness of such medical procedures. Accordingly, from 32 to 41 days of age, male Sprague–Dawley rats (N=96) were either given a daily IP saline injection (INJ), or restrained similarly but not injected (control, CON), and exposed to one of four experimental treatments: no tickling, namely, left undisturbed before and after the restraint procedure (TN), or tickled for 2min immediately before (TB), after (TA), or before and after (TBA) the restraint procedure. Rat affective response measures included rates of 50- and 22-kHz ultrasonic vocalization (USV) (validated as indicators of positive and negative affect, respectively), as well as audible vocalization rates (indicating pain and discomfort), duration of the restraint procedure, and ease-of-handling scores. Comparing INJ with CON conditions, injections reduced 50-kHz USV during (CON: 98.99±3.54calls/min, INJ: 59.2±2.42, P<0.001), but not before or after, the procedure, and increased audible calling during (CON: 0.44±0.182, INJ: 0.67±0.250, P=0.0006) the procedure. Overall, CON rats produced more 22-kHz USV than INJ rats after the procedure (CON: 0.53±0.158, INJ: 0.37±0.134, P≤0.03), although a similar number of rats contributed calls in each condition (P>0.05). Tickling did not affect the responses of rats to injection, specifically, but increased 50-kHz USV compared to TN during the period(s) when applied (Before – TN: 8.3±1.18, TB: 150.7±3.16, TA: 30.9±2.19, TBA: 154.4±3.04; After – TN: 12.4±1.39, TB: 72.5±2.59, TA: 150.5±3.59, TBA: 182.6±2.67, P<0.0001), and during the restraint procedure (TN: 33.6±3.45, TB: 101.1±4.27, TA: 76.98±4.90, TBA: 105.1±3.59, P<0.0001). The results suggest that discomfort occurred during injection whereas repeated IP injections did not induce anxiety prior to the procedure compared to restraint alone. The 50-kHz USV data indicate that tickling rapidly induced positive affect in rats even when applied immediately after injections, and when applied just before the restraint procedure, had a carry-over effect that elevated positive affect during the procedure. In sum, when mildly aversive treatments must be administered repeatedly, the current findings indicate that brief tickling is more beneficial when applied pre- than post-procedure, suggesting a way to minimize potential welfare- and behaviour-disruptive effects of routine medical procedures.

Effects of neonatal fluoxetine exposure on behavior across development in rats selectively bred for an infantile affective trait.

Infants born to women with depressive symptoms are at higher risk for insecure attachment and behavioral problems. Thus current medical practice is to continue psychotropic medication of pregnant women with depression despite concerns about its behavioral teratology. There are few animal studies focused on long-term behavioral effects of prenatal antidepressant exposure; in addition, studies have not looked at individual differences in baseline affective state as a source of response variability. In this study, fluoxetine, a selective serotonin reuptake inhibitor (SSRI), was administered to male and female rat pups from postnatal days 2-7 to model exposure to antidepressants in the human third trimester. Four behavioral measures were conducted from the neonatal to adult age periods in Low and High lines selectively bred for their rate of ultrasonic vocalizations after brief maternal separation. Neonatal fluoxetine administration decreased distress calls in both lines, but to a greater extent in High line rats than Low line. Neonatal fluoxetine also impaired motor coordination in neonates. Neonatal fluoxetine administration decreased social behavior in both juvenile and adult subjects. Fluoxetine-related reductions in anxiety behavior were not observed at the two older ages. As expected, High line subjects displayed more anxiety behavior than Low line subjects at all three test ages. These results suggest that there are may be significant behavioral consequences of antidepressant use during late pregnancy on offspring maternal attachment and social behavior, with implications for increased risk of autism spectrum disorders.

Vocalization-whisking coordination and multisensory integration of social signals in rat auditory cortex.

Social interactions involve multi-modal signaling. Here, we study interacting rats to investigate audio-haptic coordination and multisensory integration in the auditory cortex. We find that facial touch is associated with an increased rate of ultrasonic vocalizations, which are emitted at the whisking rate (∼8 Hz) and preferentially initiated in the retraction phase of whisking. In a small subset of auditory cortex regular-spiking neurons, we observed excitatory and heterogeneous responses to ultrasonic vocalizations. Most fast-spiking neurons showed a stronger response to calls. Interestingly, facial touch-induced inhibition in the primary auditory cortex and off-responses after termination of touch were twofold stronger than responses to vocalizations. Further, touch modulated the responsiveness of auditory cortex neurons to ultrasonic vocalizations. In summary, facial touch during social interactions involves precisely orchestrated calling-whisking patterns. While ultrasonic vocalizations elicited a rather weak population response from the regular spikers, the modulation of neuronal responses by facial touch was remarkably strong.

Effects of maternal deprivation and the duration of reunion time on rat pup ultrasonic vocalization responses to isolation: possible implications for human infant studies.

In a paradigm that may serve as a translational model for maternal separation experiences of human infants in neonatal intensive care units, we examined how the duration of reunion with the dam influenced the phenomenon of maternal potentiation of ultrasonic vocalizations, in which isolated rat pups increase rates of vocalization following brief interactions with dams. We report that maternal potentiation in 12-13 day-old rats did not occur after reunions with their anesthetized dam that lasted longer than 15-min. However, after 18 hr maternal separation, isolated pups given reunions with their anesthetized dam increased vocalization rate even with reunions as long as 3 hr. Using a split-cage apparatus that prevented physical contact, the impact of 18 hr separations on maternal potentiation was partially offset by experiencing olfactory and/or auditory stimuli of the mother. These results suggest that maintaining partial maternal sensory exposure during prolonged maternal separation can reduce responses elicited by subsequent maternal separation.

Physiological and behavioural responses to weaning conflict in free-ranging primate infants

Weaning, characterized by maternal reduction of resources, is both psychologically and energetically stressful to mammalian offspring. Despite the importance of physiology in this process, previous studies have reported only indirect measures of weaning stress from infants, because of the difficulties of collecting physiological measures from free-ranging mammalian infants. Here we present some of the first data on the relationship between weaning and energetic and psychological stress in infant mammals. We collected data on 47 free-ranging rhesus macaque infants on Cayo Santiago, Puerto Rico, showing that faecal glucocorticoid metabolite (fGCM) concentrations were directly related to the frequency of maternal rejection, with fGCM concentrations increasing as rates of rejection increased. Infants with higher fGCM concentrations also engaged in higher rates of mother following, and mother following was associated with increased time on the nipple, suggesting that infants that experienced greater weaning-related stress increased their efforts to maintain proximity and contact with their mothers. Infants experiencing more frequent rejection uttered more distress vocalizations when being rejected; however, there was no relationship between rates of distress vocalizations and fGCM concentrations, suggesting a disassociation between behavioural and physiological stress responses to weaning. Elevated glucocorticoid concentrations during weaning may function to mobilize energy reserves and prepare the infant for continued maternal rejection and shortage of energetic resources.

Delphinid behavioral responses to incidental mid-frequency active sonar.

Opportunistic observations of behavioral responses by delphinids to incidental mid-frequency active (MFA) sonar were recorded in the Southern California Bight from 2004 through 2008 using visual focal follows, static hydrophones, and autonomous recorders. Sound pressure levels were calculated between 2 and 8 kHz. Surface behavioral responses were observed in 26 groups from at least three species of 46 groups out of five species encountered during MFA sonar incidents. Responses included changes in behavioral state or direction of travel, changes in vocalization rates and call intensity, or a lack of vocalizations while MFA sonar occurred. However, 46% of focal groups not exposed to sonar also changed their behavior, and 43% of focal groups exposed to sonar did not change their behavior. Mean peak sound pressure levels when a behavioral response occurred were around 122 dB re: 1 μPa. Acoustic localizations of dolphin groups exhibiting a response gave insight into nighttime movement patterns and provided evidence that impacts of sonar may be mediated by behavioral state. The lack of response in some cases may indicate a tolerance of or habituation to MFA sonar by local populations; however, the responses that occur at lower received levels may point to some sensitization as well.

Using Mand Training to Increase Vocalization Rates in Infants

The present study examined the effects of a mand training procedure on the rates of vocalizations in two infants. Both typically developing girls were less than six months old at the onset of the study. An ABCBC reversal design was employed to compare the rates of vocalizations in baseline conditions, a mand-training condition, and a differential reinforcement for other (DRO) condition. A state of deprivation was held constant for both infants across all three conditions in which neither infant was fed for one hour prior to the experimental session. The order of conditions was reversed for the second infant and sessions lasted no longer than three minutes, one time per day. Findings suggested significant effects of the mand-training condition on increased rates of vocalizations for both infants. These results are discussed in terms of verbal behavior analysis, our assumptions about the developmental trajectory of the function of language, and the implications for early language intervention programs.

A simulation study of acoustic-assisted tracking of whales for mark-recapture surveys.

Collecting enough data to obtain reasonable abundance estimates of whales is often difficult, particularly when studying rare species. Passive acoustics can be used to detect whale sounds and are increasingly used to estimate whale abundance. Much of the existing effort centres on the use of acoustics to estimate abundance directly, e.g. analysing detections in a distance sampling framework. Here, we focus on acoustics as a tool incorporated within mark-recapture surveys. In this context, acoustic tools are used to detect and track whales, which are then photographed or biopsied to provide data for mark-recapture analyses. The purpose of incorporating acoustics is to increase the encounter rate beyond using visual searching only. While this general approach is not new, its utility is rarely quantified. This paper predicts the “acoustically-assisted” encounter rate using a discrete-time individual-based simulation of whales and survey vessel. We validate the simulation framework using existing data from studies of sperm whales. We then use the framework to predict potential encounter rates in a study of Antarctic blue whales. We also investigate the effects of a number of the key parameters on encounter rate. Mean encounter rates from the simulation of sperm whales matched well with empirical data. Variance of encounter rate, however, was underestimated. The simulation of Antarctic blue whales found that passive acoustics should provide a 1.7–3.0 fold increase in encounter rate over visual-only methods. Encounter rate was most sensitive to acoustic detection range, followed by vocalisation rate. During survey planning and design, some indication of the relationship between expected sample size and effort is paramount; this simulation framework can be used to predict encounter rates and establish this relationship. For a case in point, the simulation framework indicates unequivocally that real-time acoustic tracking should be considered for quantifying the abundance of Antarctic blue whales via mark-recapture methods.

Whistle source levels of free-ranging bottlenose dolphins and Atlantic spotted dolphins in the Gulf of Mexico

Whistles of bottlenose dolphins (Tursiops truncatus) and Atlantic spotted dolphins (Stenella frontalis) in the eastern Gulf of Mexico were recorded and measured with a calibrated towed hydrophone array. Surveys encountered groups of both bottlenose (N = 10) and spotted dolphins (N = 5). Analysis of those data produced 1695 bottlenose dolphin whistles and 1273 spotted dolphin whistles with a high signal-to-noise ratio. Whistle frequency metrics were lower in bottlenose than spotted dolphins, while whistle duration was longer in spotted dolphins, data that may help inform automatic classification algorithms. Source levels were estimated by determining the range and bearing of an individual dolphin from the array and then adding the predicted transmission loss to the calculated received level. The median bottlenose dolphin source level was 138 dB re 1μPa at 1 m with a range of 114-163 dB re 1μPa at 1 m. The median spotted dolphin source level was 138 dB re 1μPa at 1 m with a range of 115-163 dB re 1μPa at 1 m. These source level measurements, in conjunction with estimates of vocalization rates and transmission loss models, can be used to improve passive acoustically determined dolphin abundance estimates in the Gulf of Mexico.

The role of the pineal gland in the photoperiodic control of bird song frequency and repertoire in the house sparrow, Passer domesticus

Temperate zone birds are highly seasonal in many aspects of their physiology. In mammals, but not in birds, the pineal gland is an important component regulating seasonal patterns of primary gonadal functions. Pineal melatonin in birds instead affects seasonal changes in brain song control structures, suggesting the pineal gland regulates seasonal song behavior. The present study tests the hypothesis that the pineal gland transduces photoperiodic information to the control of seasonal song behavior to synchronize this important behavior to the appropriate phenology. House sparrows, Passer domesticus, expressed a rich array of vocalizations ranging from calls to multisyllabic songs and motifs of songs that varied under a regimen of different photoperiodic conditions that were simulated at different times of year. Control (SHAM) birds exhibited increases in song behavior when they were experimentally transferred from short days, simulating winter, to equinoctial and long days, simulating summer, and decreased vocalization when they were transferred back to short days. When maintained in long days for longer periods, the birds became reproductively photorefractory as measured by the yellowing of the birds' bills; however, song behavior persisted in the SHAM birds, suggesting a dissociation of reproduction from the song functions. Pinealectomized (PINX) birds expressed larger, more rapid increases in daily vocal rate and song repertoire size than did the SHAM birds during the long summer days. These increases gradually declined upon the extension of the long days and did not respond to the transfer to short days as was observed in the SHAM birds, suggesting that the pineal gland conveys photoperiodic information to the vocal control system, which in turn regulates song behavior.

Vocal Patterns in Infants with Autism Spectrum Disorder: Canonical Babbling Status and Vocalization Frequency

Canonical babbling is a critical milestone for speech development and is usually well in place by 10 months. The possibility that infants with autism spectrum disorder (ASD) show late onset of canonical babbling has so far eluded evaluation. Rate of vocalization or "volubility" has also been suggested as possibly aberrant in infants with ASD. We conducted a retrospective video study examining vocalizations of 37 infants at 9-12 and 15-18 months. Twenty-three of the 37 infants were later diagnosed with ASD and indeed produced low rates of canonical babbling and low volubility by comparison with the 14 typically developing infants. The study thus supports suggestions that very early vocal patterns may prove to be a useful component of early screening and diagnosis of ASD.

Validation of Optimum Algorithm Parameters Required to Estimate Vocal Tract Shape for Children Using LPC Analysis

Severe or profound deafness in hearing impaired children, can curb their ability to speak due to the lack of auditory feedback. There has been a considerable attempt in developing commercial speech training aids for such children which give feedback of acoustic and articulatory parameters. Speech training aids based on visual feedback of vocal tract shape (VTS) are reported to be useful for the improvement in speech production. Since realistic VTS estimation for adult speakers and their validation has already been done successfully, VTS estimation is now necessarily required in case of children too, so that they get trained in speech at an early age. The investigation on vocal tract shape estimation based on LPC analysis of speech by appropriately selecting some of the algorithm parameters such as vocal tract length, LPC order, and speech sampling rate has been done in our previous work. This paper attempts to validate the obtained results for vocal tract shapes corresponding to certain recorded vowels from children belonging to specific age groups. Since MRI images of VTS are unavailable for articulating children, validation of our results is based on the results from researchers who have used other indirect techniques to obtain VTS.

Effects of Parental Interaction on Infant Vocalization Rate, Variability and Vocal Type

Examination of infant vocalization patterns across interactive and noninteractive contexts may facilitate better understanding of early communication development. In the current study, with 24 infant-parent dyads, infant volubility increased significantly when parent interaction ceased (presenting a “still face,” or SF) after a period of normal interaction (“face-to-face,” or FF). Infant volubility continued at the higher rate than in FF when the parent re-engaged (“reunion,” or RE). Additionally, during SF, the variability in volubility across infants decreased, suggesting the infants adopted relatively similar rates of vocalization to re-engage the parent. The pattern of increasing volubility in SF was seen across all of the most common speech-like vocal types of the first half-year of life (e.g., full vowels, quasivowels, squeals, growls). Parent and infant volubility levels were not significantly correlated. The findings suggest that by six months of age infants have learned that their vocalizations have social value and that changes in volubility can affect parental engagement.