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. Author manuscript; available in PMC: 2015 Jun 2.
Published in final edited form as: Dev Psychobiol. 2011 Mar 22;53(7):677–684. doi: 10.1002/dev.20540

Sex and Experience Influence Behavioral Responses of Adult Rats to Potentiated and Nonpotentiated Ultrasonic Vocalizations of Pups

Shelly-Ann Rohitsingh 1, Jonathan A Smith 2,3, Harry N Shair 2,3,✉
PMCID: PMC4451066  NIHMSID: NIHMS693242  PMID: 21432845

Abstract

Responsiveness of adult rodent caretakers to infant rodents is necessary for their survival and proper development. Both olfactory and auditory cues are known to influence adult behavior toward the young. In the present study, we found that adults respond differentially to a recording of potentiated vs. non-potentiated ultrasound vocalizations of a 12-day-old rat pup, either in the presence or absence of olfactory cues. The combination of olfactory and potentiated ultrasonic vocalization produced the greatest effect. Adult behavior was also affected by the adults’ sex and parental experience in an interaction. Parental experience of females made them more responsive to the type of ultrasonic vocalization; males were little affected. Female experience, of course, includes the hormonal changes due to pregnancy and lactational state. The results are consistent with a communicatory function for isolation-induced ultrasonic vocalization.

Keywords: ultrasonic vocalization, olfaction, affiliation, communication, mother-infant behavior, parental experience, and sex

INTRODUCTION

Rat pups, like most infant mammals, communicate vocally with their caretakers. Isolated rat pups help ensure a quick return to proximity with the dam by the emission of isolation-induced ultrasound vocalizations (USV’s). Isolation-induced USV’s start as low rates from infant rodents at the age of 2–3 days old, peak at around 7–10 days, and disappear around 17–25 days (Allin & Banks, 1971; Hofer, Masmela, Brunelli, & Shair, 1998). The period of high USV emission is much the same period in which the rat pups are mobile enough to leave the nest, but not competent enough to survive on their own. There is, thus, a prima facie reason to wonder whether the function of USV is to help survival during this time. In fact, dams will go out from the nest to retrieve vocalizing isolated pups, although olfactory cues may have a necessary role in this response (Brunelli, Shair, & Hofer, 1994; Farrell & Alberts, 2002b; Smotherman, Bell, Starzec, Elias, & Zachman, 1974). Once back in contact with the dam and/or littermates, the pups no longer emit USV’s. These patterns of pup behaviors match well with two features of attachment behavior as defined by Bowlby (1969): concepts of proximity maintenance and safe haven.

There are two different types of isolation-induced USV’s that have been well studied: nonpotentiated and potentiated USV’s. When isolation does not occur shortly after contact with the dam or other potential caretaker, nonpotentiated USV’s are emitted. Maternally potentiated USV’s are emitted by the rat pup after a brief interaction with an awake, unanesthetized dam or after brief contact with an anesthetized dam (Kraebel, Brasser, Campbell, Spear, & Spear, 2002; Ricceri, Cutuli, Venerosi, Scattoni, & Calamandrei, 2007; Shair, 2007). The sonic characteristics of nonpotentiated USV’s depend on many factors including thermal, olfactory, and tactile stimuli. The sonic parameters have been described for postnatal ages 10, 15, and 17 (Brudzynski, Kehoe, & Callahan, 1999). One study from our laboratory investigated some of the sonic characteristics for both nonpotentiated and potentiated USV in the same postnatal day 10 pups animals (Myers et al., 2004). Nonpotentiated USV’s had an average length of 72–73 ms and a rate of emission of 70/min. Potentiated USV’s were louder, tended to be longer, and had different bout structure than nonpotentiated USV’s.

The evidence that USV’s produced by rat infants (approximately 40 kHz) have a communicatory function is based on evidence of detection, brain processing, and behavioral changes (Shair, 2007). For example, in a manner analogous to the way humans process speech, lactating dams preferentially process USV’s, but not white noise, in the left hemisphere of the brain (Ehret, 1987). Virgin females do not. Additionally, dams approach and maintain proximal orientation to a rat pup that is emitting USV’s more than virgin females will. Hormonal priming causes virgin females to behave like dams (Farrell & Alberts, 2002a). The parental responsiveness of adult male rodents, sires and naïve males, to USV’s in particular has not yet been investigated.

This study aimed to elucidate better if sex differences and experience can affect parental behavioral responses to these two types of USV’s and to rat pups. We examined, in a manner similar to the protocol of Farrell and Alberts (2002a), proximal orientation of adult rodents through the roles of auditory and olfactory cues. It was hypothesized that all adult rodents would respond the most to potentiated USV’s and that dams would have the highest rates of response and enhanced proximal orientation to potentiated USV’s and olfactory cues. A lesser possibility was that naïve adult males might avoid potentiated USV as it signals the presence of the dam nearby.

METHODS

Subjects

Thirty adult rats of the randomly bred N:NIH strain (outbred founders supplied by NIH) were reared and housed in our colony in polycarbonate terraria (40 × 20 × 24 cm3) with hardwood chip bedding. Food and water were available ad libitum. Colony room temperature (~21°C) and humidity (~40%) were regulated. The light/dark cycle was 12/12: lights on at 07:00 AM. Four types of adult rodents were tested: dams (n = 12), sires (n = 6), virgin females (n = 6), and or nonparentally experienced males (n = 6). Dams and sires were housed in the cages with their litters from before the day of conception until the day of testing. Inexperienced adults were never directly exposed to pups until the day of testing. These adults were, however, stored in the same room as the litters, although at least two shelf racks below. It is possible, therefore, that the inexperienced adults had some exposure to pup odors.

Litters were bred by housing an adult male and adult female together and visually checking for pregnancies and births. The day of birth was counted as postnatal day 0 (PND0). Litters were left undisturbed until the day of habituation (PND11 ± 1). Only one of the parents of any litter was tested in the experiment. A single pup from each litter was chosen at random, anesthetized with urethane, and used as a “target” pup in the orientation test. Other pups from the litters served as silent “target” pups during the tests of the parentally inexperienced adults.

Adult animals ranged in age from PND100 to PND300. All parental animals and the nonparental females were between 100 and 150 days old. Due to the fact that our colony of randomly bred N:NIH rats was being closed during the investigation, the only nonparentally experienced males available ranged in age from 250 to 300 days old. As retired breeders, these males had been sexually active and were also ~100 g heavier than the sires.

All experimental procedures were consistent with governmental regulations and approved by the Institutional Animal Care and Use Committee of the New York State Psychiatric Institute.

Apparatus

Adult responsiveness to auditory and olfactory cues from an anesthetized pup was assessed using a clear, Plexiglas apparatus that allowed the observation of the adult’s behaviors, similar to the apparatus used in the Alberts laboratory (Farrell & Alberts, 2002a). Our apparatus consisted of a single cage (22 × 30 × 22 cm3) with a 10 cm cylindrical Plexiglas pup holder (diameter 7 cm) extending perpendicularly from one side. The anesthetized pup was placed prone in the cylinder. A speaker was placed at the distal, open end of the cylinder. A wire mesh barrier prevented physical contact between main cage and proximal end of the cylinder while allowing the passage of auditory, olfactory, and visual stimuli. A line on the outside of the floor divided the cage into two halves to aid in the quantification of the adults’ orientation (near cylinder vs. away from cylinder). Ultrasonic vocalizations were played by a speaker positioned at the end of the cylinder. The speaker was connected to a laptop that played USV previously recorded from isolated 12–13 days old N:NIH pups using the Bat Sound Pro Program, version 3.3 (Pettersson Electronik AB, Uppsala, Sweden). We ensured the validity of the signal heard by the adults by recording inside the test cage the signal produced by our system. After adjusting the volume of the playback to the appropriate level, the signal recorded was identical to the original signal.

Auditory Stimuli

A library of USV recordings of isolated pups was created with the D240× ultrasonic detector, sampling frequency 100 kHz (Pettersson Electronik). Two 2-min recording were selected and used for all tests: one recording from a pup during a first isolation from the nest (nonpotentiated) and the second from the same pup isolated immediately after a reunion with its dam (potentiated). We picked the pup with the clearest recording that was in the 3rd quartile in vocalization rate under both conditions. We used recordings from the same pup in each condition to ensure that, except for the differences caused by potentiation, the two stimuli would have the greatest similarity possible. The chosen pup was the same age as the litters of the dams and sires tested (PND12 ± 1). The auditory characteristics of the two recordings match well with previous studies, see Table 1 (Brudzynski et al., 1999; Myers et al., 2004). Note that for this pup, after maternal potentiation, vocalizations averaged significantly longer, louder, and had a lower minimum frequency. Each recording was repeated five times during the 10 min exposure sessions described below.

Table 1.

Characteristics of the USV recordings used as auditory stimuli during the tests of adult responses

Condition # Pulses Pulse duration (ms) Pulse maximum frequency (kHz) Pulse minimum frequency (kHz) Pulse frequency at maximum amplitude (kHz) Maximum amplitude (dB)
Mean ± standard error of the mean
Nonpotentiated 137 114 ± 3.70 46.18 ± .39 39.39 ± .38 43.53 ± .21 −12.76 ± .54
Potentiated 247 151 ± 3.54 46.22 ± .13 37.44 ± .16 43.58 ± .11 −7.50 ± .37
ANOVA results
F(1, 183) 46.72, p = .000 1.74, ns 62.22, p = .000 .05, ns 66.74, p = .000
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ms, milliseconds; kHz, kilohertz; dB, decibel; ns, not significant.

Procedures

On the day of habituation at PND10–11, either the sire or the dam was placed in the test cage and left undisturbed for 1 hr. No auditory or olfactory cues were presented. The litter and other parent were placed on a heating pad set to maintain nest temperature to ~34.5°C. After the habituation hour, the selected adult was returned to the home cage, which was replaced in the colony room. Parentally inexperienced adults were removed from their home cages and treated in the same manner.

On the following day, the day of testing, the adults were removed and the selected adult was again placed in the test cage for a second habituation period (40 min), following the procedure of Farrell and Alberts (2002a). After the habituation period, the loudspeaker was placed in position at the end of the holding tube and a series of eight 10 min sessions begun. The sessions varied in whether (1) there was or (2) was not a pup in the holding tube and whether the auditory stimulus was (1) not present, (2) nonpotentiated USV, or (3) potentiated USV. Thus, the sessions were: (1) potentiated USV’s without a rat pup, (2) nonpotentiated USV’s without a rat pup, (3) silence without a rat pup, (4) potentiated USV’s with a rat pup, (5) nonpotentiated USV’s with a rat pup, and (6) silence with a rat pup. Note that each session with silence (s 3 and 6) was repeated twice in order to have one silent session with each of the two USV conditions. Therefore, there were, a total to eight sessions. Test order of the eight sessions was varied randomly, except that the silent periods came directly before or after their associated USV condition.

Behavior of the adult rodent was observed and each instance of four behaviors was noted in 15 s blocks for 10 min. The observed behaviors were self-grooming, biting or grabbing at the mesh, rising with both forepaws off the floor, and crossing the midline of the test chamber. The amount of time the adult spent in the half of the chamber near the holding tube, as well as the time spent lying quietly, was recorded.

Data Analyses

Data in the bar graphs and table are presented as means ± standard error of the mean. Statistics (Systat, Inc., Chicago, IL) included paired t-tests and ANOVAs as described in the Results Section. ANOVAs were followed by posthocs for repeated measures with Bonferroni adjustments. One-way a priori ANOVAs with repeated measures were performed to test a specific goal of the research: whether or not adults have an altered response to potentiated vs. nonpotentiated USV.

RESULTS

Combination of Silent Periods

In the test situation, there were two periods of silence in each tube condition (Pup in Tube and Empty Tube). Using paired t-tests, we examined whether the behavior during two silences differed depending on whether it was earlier or later in the test series. Before Bonferroni correction, there was only one significant finding: adults were observed Lying Quietly more during the second silent period when the tube contained an anesthetized pup (means 1st period 18.7, 2nd period 29.1, t = 2.60, df = 28, p = .015). Although this finding did not remain significant after the Bonferroni adjustment for 10 tests was made, we investigated whether the identity of the adult could help explain the result. There were significant effects of Sex and Sex × Experience on Lying Quietly during silent periods, but no interactions with test period. Therefore, the two silent periods in each tube condition were combined in all further analyses.

Effects of Auditory and Olfactory Cues Independent of Adult Sex and Experience

The conditions of the test chamber had significant effects on the behavior of the adults (see Figure 1). An ANOVA (Tube Condition × Test Epoch with repeated measures on Test Epoch) on each of the six behaviors was highly significant except for the percentage of the observation period the adult spent in the cage half closer to the tube (Time near Tube, p = .07). When there were no auditory or olfactory cues, adults were observed immobile (Lie Quiet) more frequently and directing the least activity toward the tube (Latency, Biting, Self groom, and Rise). Beyond that, the auditory and olfactory cues appear to work in an additive fashion. For the statistically significant behaviors, post-hoc analyses showed that Potentiated USV-Pup in Tube was the only condition which was always significantly different than Silent-Tube Empty. For the variables Bite/Grab and Latency to Approach Tube, it was also significantly greater than Isolation-induced USV-Tube Empty and there was a trend for a similar difference in the number of Rises. Even in the Tube Empty condition (see Figure 1, “d” superscripts), adults spent less time Lying Quietly in the presence of Potentiated USV than when Silent. There was a trend for the same thing to be true for Bite/Grab. If there was a pup in the tube, behavioral differences evoked by the auditory stimuli did not reach statistical significance.

FIGURE 1.

FIGURE 1

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Measures of adult behaviors in response to auditory and olfactory conditions in the test arena. Test conditions included whether the holding tube contained a pup or was empty and whether potentiated USV, isolation-induced USV, or no USV emanated from the tube. Data were collapsed across all types of adult subjects. An ANOVA was performed separately on each behavior (Tube Condition × Test Epoch with repeated measures on Test Epoch). Alphabetic superscripts over the bars indicate significant differences of at least p < .05 of posthocs for repeated measures with Bonferroni corrections. Lines over the bars indicate the results of one-way ANOVAs with repeated measures on potentiated versus nonpotentiated USV only. *p < .05; tp < .10.

Direct comparisons of the effects of the type of USV revealed that potentiated USV increased the amount of time adults spent biting/grabbing at the wire whether or not there was a pup behind it (see Figure 1 for indications of the results of one-way ANOVAs with repeated measures). There were also trends for potentiated USV to produce more Rises (Pup in Tube), a faster latency to approach (Tube Empty), and less time inactive (Tube Empty).

There were sufficient dams tested (n = 12) to analyze as was done for all adults described above, with the terms Sex and Experience removed. The picture of the results obtained was quite similar. Four of the six variables showed an effect of Tube Condition. As above, there was only a trend for an effect on Time near Tube (p = .06). Unlike the results for all adults, the amount of Self Grooming by dams did not differ significantly. Lying Quiet and Bite/Grab had the most significant differences among the columns, with potentiated USV and the presence of a pup producing more active responses of dams, as was shown by all adults above.

Effects of Sex and Experience on Responses to Potentiated USV

The data for those periods with potentiated USV, i.e., Pup in Tube and Tube Empty, were analyzed by three-way ANOVAs (Sex × Experience × Tube Condition with repeated measures on Tube Condition). There were no significant main effects of Sex or Experience, but all but two behaviors had significant Sex × Experience interactions. Latency showed a three-way interaction. No values for Time near Tube approached significance.

In order to define better the effects of Experience, we analyzed each Sex separately for the five behaviors with significant interactions. As shown in Figure 2, the response of females was significantly affected by previous experience. Dams approached the tube more quickly than virgin females and were observed self-grooming and biting or grabbing at the wire screen more frequently. They spent less time lying quietly than the naïve females. There was no effect on rising. There were, furthermore, no interactions of Experience and Tube Condition. Potentiated USV influenced the females whether or not there was a pup in the tube.

FIGURE 2.

FIGURE 2

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Effects of parental experience on behaviors of females and males in response to potentiated USV. Test conditions included whether the holding tube contained a pup or was empty. The recording of Potentiated USV was playing in all conditions. An ANOVA on each behavior was performed independently for each sex (Experience × Tube Condition with repeated measures on Tube Condition). Significant effects are indicated in the figure.

In the case of males, experience had no significant main effects on behavior. Only Rise came close to significance. Naïve males tended to rise more than sires, but there were many adults in all conditions that did not rise at all. There was a significant Experience × Tube Condition interaction for the Latency to Approach the tube. Having a pup in the tube caused parentally experienced males to decrease the time to approach, but had the opposite effect on naïve males.

Similar analyses were performed to learn whether experience influenced the response during the Isolation-Induced USV and Silent periods. When isolation-induced USV was present, the only significant result was that dams spent less time immobile (Lie Quiet) than virgin females. There were no significant main effects of Experience during the silent periods.

DISCUSSION

Previous research demonstrates that young rodents alter the parameters of their USV production depending on environmental conditions and previous experience (Branchi, Santucci, Vitale, & Alleva, 1998; Conely & Bell, 1978; Shair, Brunelli, Masmela, Boone, & Hofer, 2003). There are also studies that demonstrate that USV by young pups can elicit responses from adult animals (Brunelli et al., 1994; D’Amato, Scalera, Sarli, & Moles, 2005; Smotherman et al., 1974). The present results join the less extensive literature showing that adult animals respond differentially to the amount and kinds of USV produced (Bell, Nitschke, Bell, & Zachman, 1974; Bolivar & Brown, 1995). In this study, maternally potentiated, isolation-induced USV produced more approach and more activity than either nonpotentiated, isolation-induced USV or no USV. These results are consistent with our hypotheses that USV serves a communicatory function. This hypothesis was previously based on the conditions that produced USV in the pups (Shair, 2007). We have now shown that different types of USV can differentially influence its receivers with potentiated USV producing a more vigorous response. Our results also confirm the important effect of olfactory cues: having a pup in the tube produced more approach and more activity than when no pup was there. Unlike results with nonpotentiated USV (Brunelli et al., 1994; Farrell & Alberts, 2002b; Smotherman et al., 1974), however, olfactory cues may not be a necessary accompaniment for maternally potentiated USV to have an effect (e.g., Figure 1, Lying Quiet and Bite/Grab).

Although there were no significant main effects of sex or parental experience on the response to potentiated USV, both factors did have an influence. Most behaviors showed significant Sex × Experience interactions. When each sex was analyzed separately, adult females showed profound effects of prior parental experience on their responses. In the presence of potentiated USV, dams were more active and directed more behavior to the holding tube than did naïve females. This result extends the study that both maternal experience and hormonal priming caused adult females to more responsive to the effects of isolation-induced USV (Farrell & Alberts, 2002a). Thus, potentiated USV has its greatest effects on the animals whose response is most likely to ensure survival.

A lesser, a priori hypothesis was that parentally naïve males would avoid potentiated USV because it signals the recent presence of the dam. Male responses, however, were little affected by previous experience, but unfortunate limitations to the study reduce confidence in this and other negative results.

Interpretations of the negative results from the present study are limited by several factors. First, our colony of randomly bred N:NIH rats was being closed during the investigation, which limited the number and characteristics of the animals available for study. The effects of age, weight, and breeding status confound the male parental experience results as the only nonparental adult males available were a group of retired breeders, approximately 100 days older and 150 g heavier than the sires. There were, furthermore, only six adults in the three groups other than the Dams. Testing a larger number of males might reveal a difference based on experience. Another apparent negative result requires some explanation. The ANOVAs and posthoc tests found no significant result of whether or not there was a pup in the tube as nonpotentiated USV was playing, unlike several previous studies that found olfactory cues to be a necessary accompaniment of the auditory (Brunelli et al., 1994; Farrell & Alberts, 2002b; Smotherman et al., 1974). Again this is likely to be due to a lack of power. Specific comparisons of the effect of nonpotentiated isolation-induced USV depending on pup presence or absence showed a significant result for Lying Quiet and a trend for Time near Tube. Only Self Grooming had a “p” value >.12.

Future work will also be required to test whether our results were influenced by the specifics of the USV’s used. As only single examples of potentiated USV and isolation-induced USV were used, it is not definite that the results will generalize to the two kinds of USV. Perhaps the adults’ differences in response were due to idiosyncratic features of one or both of the USV recordings. Perhaps there would have been more (or less) differences in responses with other examples, especially if we had used USV recordings from the dams’ and sires’ own litters. We do not know, moreover, which features of the vocalizations were critical in producing the responses. The two recordings differed in number of USV, average duration, maximum amplitude of each pulse, and the minimum frequency of the pulse. Was it one of these factors that influenced behavior or some as yet unknown cue? One study in mice has shown that mouse dams do not preferentially retrieve those pups emitting the most USV (Bolivar & Brown, 1995). A study with rats has shown that dams preferentially spend more time with pups vocalizing less, but the pups vocalizing less had been previously isolated while the other group had not (Zimmerberg, Rosenthal, & Stark, 2003). Studies dissecting the vocalizations into component parts will be needed if one wants to known the “vocabulary” of infant rat USV (Ehret, 2005; Ehret & Haack, 1981, 1982).

Despite the study’s limitations, the results demonstrate that isolation-induced USV fulfils some of the requirements for a communicatory signal. Not only does USV alter the behavior of the receiver, the type of USV (potentiated vs. nonpotentiated) affects the receiver’s response. Finally, the sex and prior experience of the receiver influence the response as well.

Acknowledgments

Contract grant sponsor: New York State Office of Mental Health and NIMH

Contract grant number: R21MH077863 (HNS)

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