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.     

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.     

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

This investigation was concerned with the extent to which aggressive resident rats emit 40-70-kHz vocalizations and the effect of these signals on intruders. In Experiment 1, deafened and intact intruder males were given two encounters with resident animals. Deafened intruders engaged in a higher duration of immobile or freezing postures than intact animals. Experiment 2 indicated that the augmentation of freezing found among deafened intruders was not due to an inability to detect ultrasounds made by residents since intruders encountering devocalized resident males showed no reliable differences in specific motor patterns from intruders paired with intact residents. The results further demonstrated that 40-70-kHz vocalizations are produced almost entirely by intruding animals since there were no significant changes in occurrence of these calls when resident males were devocalized. Under the constraints of the testing procedures employed, the role of ultrasonic communication during the initial formation of agonistic relations could not be determined experimentally.     

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.     

Positive geotaxis in infant rats (Rattus norvegicus): a natural behavior and a historical correction

Infant rats (Rattus norvegicus) placed on a shallow incline (2 degrees, 4 degrees, or 8 degrees) oriented and moved downhill within 1 min; that is, they displayed positive geotaxis. Their downhill translocation increased with angle of inclination. A variety of possible behavioral elements (e.g., initial orientation, rotational movements, ambulatory velocities) were eliminated as explanations of the geotaxis. Wall contact was recognized as a determinative event: Pups on the inclines showed no orientation with respect to the geogravitational stimulus before contacting a wall. The event of wall contact, however, evoked reliable downhill orientation and more linear movements. Positive geotaxis was created by pups' orientation against walls and an associated increase in movement velocity. This is a distinct perspective on a behavioral response that replaces a traditionally misinterpreted phenomenon. The authors discuss the ecological validity and historical context of these findings.     

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.     

Behavioral responses of juvenile rats (Rattus norvegicus) to neonates after infusion of maternal blood plasma

Individual 18- or 30-day-old male and female Wistar rats (juveniles) were continuously exposed to 3-8-day-old pups for 5 days (sensitization) after intravenous (iv) infusion of maternal blood plasma (PL group) or 5% dextrose and water (IC group) through chronically implanted cannulas and were compared with nonhandled littermate controls (NHC group). The results showed complex interactions with sex and age of the animals tested, depending upon which maternal behaviors were examined. First, plasma from parturient females selectively increased retrieving behavior in 30-day-olds, and it was more powerful in females than in males. Second, on the first day, prior to sensitization, both PL and IC 30-day-olds showed higher frequencies of retrieving, crouching, anogenital licking, and contact than did nonhandled juveniles. Third, 30-day-olds that received maternal blood plasma continued to retrieve pups, with a latency peak for retrieving occurring at 72 hours, suggesting a long-term effect of plasma not seen in control animals. Fourth, 18-day-old subjects did not generally show effects of any of our manipulations, but they did show more nest building and contact behaviors than did 30-day-old subjects. Last, we found that the iv cannulation and infusion procedures led to a persistent dissociation of retrieving behavior from play in older animals and an integration of retrieving with crouching and licking regardless of whether maternal plasma or control infusion was administered. Retrieving behavior was associated with play behaviors (charge and pounce) in younger juveniles and in older, nonhandled control animals irrespective of treatment. For these animals, no integration of retrieving occurred with other maternal behaviors.     

Thermoregulatory behavior in infant Norway rats (Rattus norvegicus) and Syrian golden hamsters (Mesocricetus auratus): arousal,orientation, and locomotion

The responses of 2- and 8-day-old rats (Rattus norvegicus) and hamsters (Mesocricetus auratus) to thermal stimulation were assessed in 4 experiments. In Experiment 1, the surface underlying the pup was cooled, and the latency to escape to a region of warmth was measured. Experiment 2 required pups to locomote farther to gain access to warmth. Experiment 3 was similar to Experiment 1 except the underlying surface was heated. Finally, in Experiment 4, locomotor behavior was assessed during isothermal cooling in which there was no possibility for escape. In general, hamsters exhibited more rapid and robust responses to thermal stimulation than rats. A framework for interpreting these results is presented emphasizing how differences in locomotor and thermogenic capabilities influence thermoregulatory behavior under different task conditions.     

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.     

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.     

Contributions of endothermy to huddling behavior in infant Norway rats (Rattus norvegicus) and Syrian golden hamsters (Mesocricetus auratus)

Infant Syrian golden hamsters (Mesocricetus auratus) do not exhibit endogenous heat production before 3 weeks of age and do not huddle effectively during cold exposure, gaining little thermoregulatory benefit from the presence of multiple littermates. In contrast, infant Norway rats (Rattus norvegicus) produce heat endogenously and are effective at maintaining elevated body temperatures by huddling. Therefore, the ineffective huddling of infant hamsters may be due to the absence of endogenous heat production. The huddling behavior of infants in mixed huddles of 8-day-old hamsters and weight-matched 4-5-day-old rats was observed to explore this possibility. The results indicate that hamsters, even when cold, effectively gain access to heat-producing rats, supporting the idea that endothermy contributes to the behavior of huddling by providing heat to each individual and thermal stimuli to other infants to support aggregation.     

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.     

Social interaction modifies learned aversions, sodium appetite, and both palatability and handling-time induced dietary preference in rats (Rattus norvegicus)

In a series of four experiments, I examined the extent to which socially transmitted diet preference could counteract the effects of a learned aversion (Experiment 1), a palatability-based diet preference (Experiment 2), a polyethylene glycol 20,000-induced sodium appetite (Experiment 3), and a handling-time induced dietary preference (Experiment 4). I found that rats poisoned after eating a novel diet ate very substantial amounts of the averted diet following interaction with conspecifics that had eaten the averted diet. Following interaction with conspecifics that had eaten an unpalatable diet, rats offered a choice between palatable and unpalatable diets ate more than twice as much unpalatable diet as did controls lacking social experience. Sodium-deficient rats offered a choice between sodium-enriched and sodium-adequate diets ate less than half as much sodium-enriched diet, following interaction with conspecifics that had eaten sodium-adequate diet as did control rats lacking social experience. Rats offered a choice between isocaloric, roughly equipalatable foods with long and short handling times (e.g., sunflower seeds with and without shells) chose the food having the longer handling time after interacting with conspecifics eating that food. These findings suggest that social influence is a major factor in guiding diet selection by rats.     

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.     

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.     

Odor cue determinants of urine marking in male rats (Rattus norvegicus)

This study examined the spatial distribution of urine marking by sexually inexperienced male rats under six odor conditions: minimum odor (baseline), conspecific male urine, conspecific female urine, an animal's own urine, male gerbil urine, and amyl acetate. The gerbil urine and amyl acetate conditions were included to test the theory that marking, rather than being elicited by and directed as a display to appropriate conspecifics, occurred to the introduction of any novel or disruptive odor. The subject's own urine was used to test the theory that the animal marked to maintain an optimum level of its own odor in the environment. The results showed that marking was directed predominantly at objects in the environment over which the animal could readily pass. All odor conditions except "own odor" sharply increased marking over baseline levels. Marking decreased with repeated exposure to particular stimuli. The results strongly supported the theory that urine marking, at least in sexually inexperienced male rats, is produced by novel odor stimuli introduced into a familiar environment.     

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.     

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.     

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.