Analysis of ultrasonic vocalizations emitted by intruders during aggressive encounters among rats (Rattus norvegicus)

This investigation was concerned with the identification of the ultrasonic vocalizations produced by intruders during aggressive interactions and the role of these signals in agonistic behavior of rats. In the first experiment, experienced resident males were paired with both devocalized and intact vocalizing naive intruder males. Devocalization of the intruder males resulted in a drastic decrease in 50-kHz vocalizations and the elimination of all 22-kHz vocalizations. This almost total absence of ultrasonic vocalizations was not accompanied by any change in resident aggressive behavior or intruder defensive and submissive behavior. In a second experiment, naive intruders were tested with either deafened or intact resident males. Similarly, preventing residents from hearing intruder ultrasounds had no detectable effect on any aggressive behavior. These experiments are not consistent with the correlative evidence that intruder-produced 22-kHz vocalizations inhibit the aggressive behavior of the resident. The results also show that most of the ultrasonic vocalizations emitted during aggressive encounters are probably produced by the intruder.     

Sensory cues that elicit ultrasonic vocalizations in female rats (Rattus norvegicus)

Female rats emit ultrasonic vocalizations during copulation. Female vocalizations are associated with darting and other proceptive behavior. In addition, females frequently call while approaching the male. A series of experiments was undertaken to determine whether female rats emit ultrasonic vocalizations in response to other rats or to their odors. Females were exposed either to bedding soiled by males or females or to devocalized conspecifics separated from the subject by a barrier. Females vocalized more to male cues than to female cues, regardless of whether the odor cues were from soiled bedding or from a devocalized conspecific. In addition, subjects vocalized more when presented with a devocalized female rather than a neutral stimulus. Furthermore, devocalized adult males, separated by a barrier, were more effective than either devocalized castrated or juvenile males in eliciting vocalizations; in turn, castrates and juveniles were more effective than neutral stimuli. Female calling was likely induced by odors from the male. In one experiment, the female subject was positioned in such a way that she could neither see or touch the stimulus male. Presentation of tape-recorded male vocalizations did not affect calling by the female. Vocalizations emitted by females in response to male odors may attract males or may facilitate subsequent copulatory behavior by the male.     

Stimulus control of maternal responsiveness to Norway rat (Rattus norvegicus) pup ultrasonic vocalizations

Mother rats (Rattus norvegicus; 6 to 8 days postpartum) approach and maintain proximal orientation to a pup that is emitting ultrasonic vocalizations (USVs) far more than do virgin females (W. J. Farrell & J. R. Alberts, 2002). We used a playback regimen to examine the roles of acoustic and nonacoustic cues in regulating maternal proximal orientation toward vocalizing pups. When presented with recorded USVs, mothers of 6- to 8-day-old pups and nulliparous virgin females exhibited equivalent levels of proximal orientation toward the playback speaker. Mothers did show enhanced proximal orientation toward recorded USVs, however, if a silent pup was positioned below the speaker. Pup odors appear to be crucial for the maternal response to vocalizing pups, as peripherally induced anosmia attenuated maternal proximal orientation toward a vocalizing pup. Furthermore, spatial contiguity between olfactory and auditory stimuli was required for a maximal maternal response.     

Responses of observer rats (Rattus norvegicus) to complex, diet-related signals emitted by demonstrator rats

We explored the effects of complex, food-identifying signals emitted by demonstrator Long-Evans rats (Rattus norvegicus) on food preferences of their observers. In Experiments 1 and 2, observers identified each of 2 or 3 foods their demonstrators had eaten before interacting with observers. In Experiment 3, individual observers interacted with groups of demonstrators. Some of these demonstrators had eaten one food, some another. Observers then chose between the two foods. The greater the proportion of demonstrators in a group that had eaten a diet, the greater the proportion of that diet the observers ate. In Experiment 4, each observer interacted over several weeks with a series of demonstrators and preferred each of the foods its demonstrators had eaten. In sum, the food preferences of observers were affected by several different types of complex, food-identifying signals like those one might expect rats to encounter outside the laboratory.     

Brief maternal interaction increases number, amplitude, and bout size of isolation-induced ultrasonic vocalizations in infant rats (Rattus norvegicus)

The number, amplitude, duration, and bout structure of isolation-induced ultrasonic vocalization (USV) of infant rats (Rattus norvegicus) were measured on postnatal Day 10. Measurements were made before and after a brief, 1-min, active interaction with their mother or before and after a "pick-up" control procedure. Consistent with prior studies, the number of USVs emitted was significantly increased in the period following the maternal reunion but not after the control procedure. The average amplitude of USVs was also greater following maternal reunion. Finally, analyses characterizing the bout structure of USV production indicated that the average bout size (i.e. number of USVs/bout) was increased severalfold following the reunion with the mother, accounting for the greater rate of USV production during the second isolation period.     

Food stealing by young Norway rats (Rattus norvegicus)

Six experiments were undertaken to explore factors affecting young rats' (Rattus norvegicus) frequencies of stealing food from conspecifics when identical food is available in surplus. It was found that (a) rats would walk across a bed of pellets to steal the particular pellet a peer was eating, (b) frequency of stealing within a pair did not decrease over days, (c) rats stole unfamiliar foods more frequently than familiar foods, (d) younger rats stole from older rats more frequently than older rats stole from younger ones, (e) hungry rats stole more frequently than replete rats, and (f) rats that had stolen a pellet of unfamiliar food from an anesthetized conspecific subsequently exhibited an enhanced preference for that food. Results suggest that food stealing is a mode of active seeking of information about what foods to eat.     

Auditory categorization of complex sounds by rats (Rattus norvegicus)

Little research has explored the auditory categorization abilities of mammals. To better understand these processes, the authors tested the abilities of rats (Rattus norvegicus) to categorize multidimensional acoustic stimuli by using a classic category-learning task developed by R. N. Shepard, C. I. Hovland, and H. M. Jenkins (1961). Rats proved to be able to categorize 8 complex sounds on the basis of either the direction or rate of frequency modulation but not on the basis of the range of frequency modulation. Rats' categorization abilities were limited but improved slowly and incrementally, suggesting that learning was not facilitated by selective attention to acoustic dimensions.     

Maternal responsiveness to infant Norway rat (Rattus norvegicus) ultrasonic vocalizations during the maternal behavior cycle and after steroid and experiential induction regimens

When removed from the nest and placed in a cool environment, Norway rat (Rattus norvegicus) pups emit ultrasonic vocalizations that can elicit maternal search behavior. The authors examined the behavior of pregnant dams, mothers, and virgin females during exposure to a pup that was either warm and silent or cool and vocalizing. Results indicate potentiated maternal reactions to a vocalizing pup: Mothers approached and maintained proximal orientation to a vocalizing pup far more than did virgin females. Elevated levels of proximal orientation appeared within hours of birth, increased during the 1st week postpartum, and declined by the time of weaning. Estrogen plus progesterone administration facilitated virgin females' proximal orientation toward vocalizing pups, whereas prolonged exposure to pups in the absence of hormones was without effect, suggesting that the ontogeny of the maternal response is regulated, at least in part, by maternal hormones.     

Social identification of toxic diets by Norway rats (Rattus norvegicus)

In the present experiment, a naive rat (an observer) interacted with two conspecifics (demonstrators) that had recently eaten a diet unfamiliar to the observer, ate two unfamiliar foods in succession, one of which was the food its demonstrators had eaten, suffered toxicosis, and finally, was offered a simultaneous choice between the two diets it had eaten prior to toxicosis induction. During the choice test, observers exhibited an aversion to that diet their respective demonstrators had not eaten. This result indicates that exposure of a rat to conspecifics that have eaten a diet can act, as does actual ingestion of a diet, to reduce that diet's subsequent associability with toxicosis. I discuss this finding as suggesting that interaction with conspecifics may provide an alternative to individual trial and error learning in identification of toxic foods by rats that ingest a number of novel foods in succession before becoming ill.     

Effects of male pre-ejaculatory vocalizations on female receptive behavior in the rat (Rattus norvegicus)

Both male and female rats (Rattus norvegicus) emit ultrasounds during copulation. Bursts of ultrasounds from males that occur as ejaculation approaches are lower in frequency, longer in duration, and louder than those that appear earlier in the ejaculatory series. We attempted to determine if these pre-ejaculatory calls affect female sexual behavior. The behavior of females paired with devocalized males was compared with that of females paired with intact males, and in a second experiment tape-recorded vocalizations were played to females paired with devocalized males. Females were less receptive when paired with devocalized males; they were less likely to remain stationary when males attempted to mount. Playback of both types of calls restored female immobility toward control levels, although pre-ejaculatory calls were more effective than mating ones. Pre-ejaculatory calls restored running and training levels somewhat toward control level but to a lesser extent than female immobility.     

Olfactory discrimination of individual littermates in rats (Rattus norvegicus)

Adult male rats (Rattus norvegicus) were trained in a Y-maze to discriminate the presence of a littermate from its absence. Transfer of training in subsequent tests indicated that (a) the animals were capable of distinguishing among individuals when relatedness and familiarity were held constant, (b) this ability was not due to training, and (c) their performance was based solely on odor cues. The results are discussed in relation to social behavior in rats.     

Transitive inference in rats (Rattus norvegicus).

Although Piagetian theory proposes that the ability to make transitive inferences is confined to humans above age 7, recent evidence has suggested that this logical ability may be more broad based. In nonverbal tests, transitive inference has been demonstrated in preschool children and 2 species of nonhuman primates. In these experiments, I demonstrate evidence of transitive inference in rats (Rattus norvegicus). I used an ordered series of 5 olfactory stimuli (A < B < C < D < E) from which correct inferences were made about the novel B versus D pair. Control procedures indicated that performance did not depend on the recency with which the correct answer was rewarded during training and may be disrupted by the addition of logically inconsistent premises (F > E and A > F). The possibility that logical transitivity may reflect a form of spatial paralogic rather than formal deductions from a syllogistic-verbal system is discussed.     

Recognition of food by individual, food-naive, weaning rats (Rattus norvegicus)

To control and observe first feeding experiences, pups were reared without access to food. At weaning age, individual pups received simultaneous access to a palatable, noncaloric diet and a similar diet containing starch. Each diet contained a flavor cue. Within 20 min of sampling both diets pups preferentially ingested the caloric alternative. Further tests indicated that pups learned a preference for flavor cues paired specifically with ingestion of starch. In caloric discrimination tests in which the diets were not distinguished by artificial flavors, pups did not show the rapid preference for the caloric diet seen in earlier experiments. We suggest that recognition and preference for the caloric diet is based on its rapid postingestive effects rather than readily preferred sensory features of the starch. Our findings demonstrate the abilities of individual, food-naive pups to rapidly recognize food and indicate a role for associative learning in the onset of independent feeding.     

Sex differences in urinary odors produced by young laboratory rats (Rattus norvegicus)

Responses of adult female rats to male and female pup urine were examined in three experiments. Investigatory sniffing of male and female pup urine deposits by maternal rats was compared in a series of simultaneous choice tests given at 3-day intervals between Day 2 and Day 17 postpartum. Male urine was consistently preferred. Introduction of male, but not female, pup urine to the nest was also found to significantly elevate maternal licking of anogenital regions of pups. Thus, urine from pups of various ages contains sex-identifying odors that differentially elicit spontaneous maternal interest. The odor of male urine may provide a sufficient stimulus to account for the greater anogenital licking that males of this species normally receive. Nonmaternal, naive, adult females behaved like maternal rats, preferring male urine in the choice test. This indicates that the maternal condition of a dam is not necessary either for the olfactory discrimination or for the male odor preference.     

Preference for novel flavors in adult Norway rats (Rattus norvegicus)

The authors fed rats 1 of 2 distinctively flavored, roughly equipalatable diets for 3 days then offered them an ad libitum choice between the 2 diets. For 3 days, subjects exhibited a reduced relative intake of whichever diet they had previously eaten (Experiment 1). Such reduction in relative intake was as effective as a toxicosis-induced conditioned aversion in determining subjects' food choices (Experiment 2). The strength of exposure-induced reduction in relative intake did not depend on similarity of the 2 diets offered for choice either to each other or to subjects' maintenance diet (Experiment 3) but did require continuous exposure to a diet (Experiment 4). These experiments provide the first evidence of a robust, exposure-induced decrease infood preference in rats lasting for days rather than minutes.     

Maternal aggression: disruption by perioral anesthesia in lactating Long-Evans rats (Rattus norvegicus)

Role of perioral somatosensation in the display of maternal aggression in Long-Evans Norway rats (Rattus norvegicus) was investigated during early lactation by local anesthesia of the mystacial pads with lidocaine, which blocks conduction in the infraorbital nerve. Acute perioral anesthesia markedly reduced the likelihood that maternal aggression was expressed; this effect of perioral anesthesia was not ameliorated by a repeated test with the same treatment or by pretreatment fighting experience. The dams that fought with the intruder during perioral anesthesia did so after greatly increased sniffing contact and with decreased vigor compared with controls. Males that were attacked tended to freeze, whereas males that were not attacked were active. Thus, trigeminal afferents are critical for the initiation and normal execution of maternal aggression responses in Norway rats.     

Cooperative behavior of laboratory rats (Rattus norvegicus) in an instrumental task

Cooperation is a cognitively demanding, complex social behavior, found primarily in primates. Here we investigated mutualism in rats (Rattus Norvegicus), a simple form of cooperation in which two subjects work on operant task, receiving immediate and simultaneous sucrose reward for a joint action. To receive the sucrose reward, familiar pairs of rats were required to nose poke simultaneously. Following 44 training days, we examined the relation of social contact and ultrasonic vocalizations to the rat's cooperative behavior by testing the effects of inserting opaque, wire-mesh, or no partition--between subjects. Cooperative behavior (simultaneous nose-poking): (a) increased gradually during initial training; (b) decreased with the opaque partition (restricting visual, acoustic, and physical communication); (c) increased with a wire mesh partition restricting only physical contact); and (d) increased with the number of 50 kHz USV "happy" calls and the intensity of social interaction. The possibility of studying the development of cooperative behavior in laboratory rats using a simple procedure based on commercially available equipment may prove useful in modeling determinants of social behavior.     

Penile responses of rats (Rattus norvegicus) in extended ex copula tests

Prolonged tests of rats' penile responses outside the context of copulation (ex copula) were undertaken to facilitate analysis of these penile components of copulatory behavior. Penile erections and flips were evoked for 1 hr following penile sheath retraction (SR), and rats were retested for 30 min after a rest interval of 5 min to 4 hr. The number of penile responses declined sharply over the course of the hour. Following a 5-min rest, there was little likelihood of additional responses. Within 2 hr some measures of penile response potential approached their original high asymptotes; other measures were still depressed after 4-hr rest. In control tests, the penile sheath was unretracted (SU) during the first 60 min, and hence few or no penile responses occurred. This condition caused no reduction in the number of erections and flips in the subsequent 30-min SR test; hence the reduction in response potential during and after SR tests was due to the responses displayed, not to the conditions of restraint. Ejaculation occurred frequently in the SU condition but rarely in SR tests, results suggesting that sheath retraction may normally inhibit ejaculation in ex copula tests, and perhaps during copulation as well.     

Perioral somatosensory determinants of nursing behavior in Norway rats (Rattus norvegicus)

Prior to assuming the upright crouching posture over their pups during nursing bouts, lactating rats typically engage in several oral behaviors, including nuzzling, licking and rearranging pups. By acutely depriving dams of various aspects of perioral stimulation from pups (with anesthesia of the mystacial pads or of the tongue, with mouth suturing, or with muzzling), we found the following: (1) Distal stimulation from pups maintains proximity-seeking behavior, but is insufficient to stimulate nursing behavior. (2) Lack of tongue feedback decreases pup licking and hastens the onset of crouching. (3) Snout, but not tongue, contact with pups is required for hovering over them. (4) The position of the dam while hovering over her litter enables the pups to gain access to her ventrum, thereby provoking her upright, crouching posture. (5) Older pups are capable of bypassing the dam's perioral attentions and stimulating crouching directly by burrowing under the dam's ventrum.     

Life-span changes in the copulatory behavior of male rats (Rattus norvegicus)

The copulatory behavior of 5-, 10-, 15-, and 20-month-old sexually naive male rats (Long-Evans) was studied during 2-hr tests with receptive females. There was no apparent change in sexual arousal as measured by latency to initiate copulation across age, with subjects from all groups exhibiting comparable latencies to first mount and first mount with intromission. The numbers of ejaculations achieved were also similar across ages. Significant age differences were found for frequency of mounts, with 20-month-olds having the highest mean frequency. The persistent mounting by older males appeared to account for significant group differences in interintromission interval and ejaculation latency. It is suggested that motor deficits may impair the ability of older males to achieve intromission, increasing the number of mount bouts as well as the number of mounts per bout, thus extending the length of each copulatory series.