Ultrasonic vocalizations by male house mice (Mus musculus) to novel odors: roles of infant and adult experience

Two experiments were conducted to examine 70-kHz ultrasonic courtship vocalizations by adult male mice (Mus musculus) to novel odors following exposure to these odors in infancy and/or adulthood. The research was performed in hopes of better understanding the experiences giving rise to vocalizations to naturally occurring chemosignals. Experiment 1 demonstrated that adult males normally do not vocalize to the urine of female rats but would come to do so if adult female mice odorized with female rat urine were repeatedly encountered postpubertally. On the other hand, encountering their own mother odorized with female rat urine from birth until weaning did not promote vocalizations to the urine of female rats. Experiment 2 was designed to examine vocalizations to the urine of female mice whose urinary odor was altered by the ingestion of fenugreek, a spice. Although the magnitude of the effect was smaller in this experiment, greater amounts of vocalization again were seen by males that as adults encountered females that had ingested fenugreek. Males with such experience also showed a small but significant elevation in vocalizations to the fenugreek odor itself. Again, experience with the novel odor during infancy was not associated with elevated vocalizations during adulthood either to fenugreek-altered urine or to the fenugreek odor itself. Thus vocalizations to two different novel odors occurred only after an adult male had encountered an adult female odorized with the novel odor. On the other hand, none of the novel odor experiences eliminated vocalizations to the naturally occurring chemosignal in female mouse urine.(ABSTRACT TRUNCATED AT 250 WORDS)     

Potentiation and overshadowing in odor-aversion learning: Role of method of odor presentation,the distal-proximal cue distinction,and the conditionability of odor

Four experiments with rat subjects examined interactions between odors and tastes in compound aversion conditioning. In Experiments 1 and 2, a saccharin taste potentiated the conditioning of an almond odorant presented on a cup near the location of the drinking spout, but overshadowed the same odorant when it was mixed in drinking water. This difference depended on the type of odor administered during conditioning rather than testing (Experiment 2). Experiments 3 and 4 examined implications of two other differences between the cup and drink odors: (1) while the cup odor was a distal cue that suppressed approach to the spout, the drink odor was primarily a proximal cue that suppressed consumption, and (2) the cup odor was less conditionable than the drink odor when the stimuli were conditioned alone. In Experiment 3, unlike the proximal saccharin taste, the proximal drink odor failed to potentiate the conditioning of a different distal odor. In Experiment 4, substantial dilution of the proximal drink's concentration resulted in both weaker conditioning of the stimulus alone, and potentiation of its conditioning by saccharin. The results suggest that the difference in the conditionability of the cup and drink odors, and not their status as distal and proximal cues, may be critical in the production of potentiation. Weakly conditionable target stimuli are uniquely potentiated by saccharin.     

Noradrenergic control of odor recognition in a nonassociative olfactory learning task in the mouse

The present study examined the influence of pharmacological modulations of the locus coeruleus noradrenergic system on odor recognition in the mouse. Mice exposed to a nonrewarded olfactory stimulation (training) were able to memorize this odor and to discriminate it from a new odor in a recall test performed 15 min later. At longer delays (30 or 60 min), the familiar odor was no longer retained, and both stimuli were perceived as new ones. Following a post-training injection of the alpha(2)-adrenoceptor antagonist dexefaroxan, the familiar odor was still remembered 30 min after training. In contrast, both the alpha(2)-adrenoceptor agonist UK 14304 and the noradrenergic neurotoxin DSP-4 prevented the recognition of the familiar odor 15 min after the first exposure. Noradrenaline release in the olfactory bulb, assessed by measurement of the extracellular noradrenaline metabolite normetanephrine, was increased by 62% following dexefaroxan injection, and was decreased by 38%-44% after treatment with UK 14304 and DSP-4. Performance of mice in the recall test was reduced by a post-training injection of the beta-adrenoceptor antagonist propranolol or the alpha(1)-antagonist prazosin, thus implicating a role for beta- and alpha(1)-adrenoceptors in the facilitating effects of noradrenaline on short-term olfactory recognition in this model.     

An olfactory discrimination procedure for mice

This paper describes an olfactory discrimination procedure for mice that is inexpensively implemented and leads to rapid discrimination learning. Mice were first trained to dig in small containers of sand to retrieve bits of buried chocolate. For discrimination training, two containers were presented simultaneously for eight trials per session. One container held sand mixed with cinnamon, and the other held sand mixed with nutmeg. Both containers were baited with chocolate buried in the sand. One odor was designated S+, and mice were allowed to dig and retrieve the chocolate from this container. The other odor was S-, and both containers were removed immediately if subjects began to dig in an S- container. After meeting a two-session acquisition criterion, subjects were given a series of discrimination reversals. In Experiment 1, 12 Swiss-Webster mice (6 male and 6 female) acquired the olfactory discrimination in three to five sessions and completed 3 to 10 successive discrimination reversals within a 50-session testing limit. In Experiment 2, subjects were 14 Pah(enu2) mice, the mouse mutant for phenylketonuria; 7 were homozygotes in which the disorder was expressed (PKU), and 7 were heterozygotes with normal metabolism (non-PKU). Thirteen mice completed pretraining in four to seven sessions, acquisition required 3 to 12 sessions, and all mice completed at least three reversals. Learning rates were similar in PKU and non-PKU mice. We discuss issues related to implementation and several potentially useful procedural variations.     

Recognition of odors and identification of sources

The purpose of the present study was to investigate the accuracy of the memory for odors and for the location of odors. In Experiment 1, 5 unfamiliar odors were presented in each of 2 rooms. Twenty participants were instructed to remember only the odors (odor-only control group) and 20 were instructed to remember both the odors and the room where the odors were presented (odor place group). In Experiment 2, both the odor presentation room and the sex of the experimenters were manipulated to increase the uniqueness of the odor location. The results demonstrated that the memory for an odor is superior to the memory for the location of an odor. The results also indicated that the intention to learn the sources of an odor improves the memory for the source. These results are discussed in the context of the source monitoring framework.     

Similarity in the qualities of individual odors among kin and species in Turkish (Mesocricetus brandti) and golden (Mesocricetus auratus) hamsters.

In this investigation, the authors used habituation techniques to explore similarities and differences in the qualities of individual odors from hamsters. In Experiment 1, male Turkish hamsters (Mesocricetus brandti) treated flank-gland odors of 2 males from 1 litter as similar compared with the odor of a male from another litter, whether the odor donors were familiar or unfamiliar. At the same time, the Turkish hamsters discriminated between the subtle differences in the individual odors of their familiar brothers. In Experiment 2, male Turkish and golden hamsters (Mesocricetus auratus) treated the flank-gland odors of 2 unfamiliar, unrelated conspecifics as similar compared with the flank odor of a heterospecific individual. The results suggest that similarities in individual odors are related to genetic similarity of the odor donors. These similarities could provide a basis for different types of social recognition, including kin and species recognition.     

Simultaneous odor-taste and taste-taste compounds in poison-avoidance learning

In six experiments, rats received an odor or a taste alone or in simultaneous compound with another taste prior to lithium chloride-induced illness. Aversions to the target odor and the target taste were then assessed. In Experiments 1–3, the presence of the taste in compound with the target during conditioning attenuated the strength of the aversions to both the target odor and the target taste. Although these results were consistent with the familiar principles of compound conditioning, they contradicted previous reports of potentiation, rather than attenuation, of odor conditioning by taste. In Experiment 4, taste again attenuated the conditioning of odor when a second odor was presented during the CS-US interval. In Experiment 5, we looked for odor potentiation with a within-subject design, and in Experiment 6, we examined an alternative method of presenting odor. In neither case did we find odor potentiation by taste. Over the range of conditions investigated here, a taste often attenuates, and never potentiates, the conditioning of aversions to both odors and tastes.     

Resistance to extinction of conditioned odor perceptions: evaluative conditioning is not unique

A tasteless odor will smell sweeter after being sampled by mouth with sucrose and will smell sourer after being sampled with citric acid. This tasty-smell effect was found in experiments that compared odor-taste and color-taste pairings. Using odors and colors with minimal taste (Experiment 1), the authors found that repeated experience of odor-taste mixtures produced conditioned changes in odor qualities that were unaffected by intermixed color-taste trials (Experiment 2). An extinction procedure, consisting of postconditioning presentations of the odor in water, had no detectable effect on the changed perception of an odor (Experiments 3 and 4). In contrast, this procedure altered judgments about the expected taste of colored solutions. Evaluative conditioning (conditioned changes in liking) is claimed to be resistant to extinction. However, these results suggest that resistance to extinction in odors is related to the way they are encoded rather than to their hedonic properties.     

Taste preconditioning augments odor-aversion learning

On the basis of previous work that has shown a taste can potentiate odor-aversion conditioning in AX+ conditioning, 6 experiments used rats to examine the effects of pairing a preconditioned taste (A) with a novel odor cue (X) in an A+/AX+ aversion conditioning design. Experiments 1A and 1B demonstrated that a preconditioned taste produced a robust odor aversion that was significantly stronger than a potentiated odor aversion. The results of Experiment 2 showed that the robust odor aversion produced by A+/AX+ conditioning was not the result of the potentiated odor aversion summating with generalization from the taste aversion. The augmented odor aversion was produced only when the taste and odor stimuli were presented simultaneously (Experiment 3) and the preconditioned taste aversion was intact at compound conditioning (Experiment 4). Pairing a novel odor with a preconditioned taste was not sufficient to condition an aversion to odor (Experiment 5), although other results implicated a role for an association between odor and taste in the odor augmentation effect (Experiment 6). The present results have implications for current models of taste + odor interactions in flavor-aversion conditioning.     

Olfactory predator recognition in predator-naïve gray mouse lemurs (Microcebus murinus)

Olfactory cues of predators, such as feces, are known to elicit antipredator responses in animals (e.g., avoidance, activity). To date, however, there is little information on olfactory predator recognition in primates. We tested whether the odor of feces of different predator categories (historical Malagasy predators and introduced predators) and of Malagasy nonpredators (control) induces antipredator behavior in captive born, predator-na?ve gray mouse lemurs. In an olfactory predator experiment a mouse lemur was exposed to a particular odor, fixed at a preferred location, where the animal was trained to get a reward. The behavior of the mouse lemur toward the respective stimulus category was videotaped and quantified. Results showed that mouse lemurs avoided the place of odor presentation when the odor belonged to a predator. They reacted with a significantly enhanced activity when exposed to odors of carnivores compared to those of nonpredatory controls. These findings are in favor of a genetic predisposition of olfactory predator recognition that might be based on the perception of metabolites from meat digestion.     

Simultaneous conditioning in honeybees (Apis mellifera).

Honeybees (Apis mellifera) were classically conditioned with odor as conditioned stimulus (CS), sucrose as unconditioned stimulus (US), and proboscis extension as response. The purpose of Experiment 1 (Ns = 26 and 27) was to look for facilitation of forward conditioning by CS-US overlap, but rapid conditioning without overlap left little room for improvement. In 2 further experiments, CS and US were simultaneous, and response to odor alone was measured in subsequent tests. In Experiment 2, a Simultaneous group (N = 25) responded more to the training odor than did an Unpaired control group (N = 25). In Experiment 3, a differentially conditioned Simultaneous group (N = 29) responded more to an odor paired with sucrose in training (S+) than to an odor presented alone (S-). The implications of the results for the problem of the role of amount of reward in honeybee learning are considered.     

Augmentation of taste conditioning by a preconditioned odor.

Five experiments explored facilitated taste-aversion conditioning (odor-mediated taste augmentation), using rats that experienced odor (A) and taste (X) in an A+/AX+ design. Augmentation occurred when the stimuli were presented simultaneously during AX+ conditioning, and significantly weaker conditioning occurred after a sequential presentation (Experiment 1). Experiments 2 and 3 demonstrated that augmented conditioning decreased if the odor aversion was reduced through preexposure or extinction following A+ conditioning. A second-order conditioning explanation was not supported by the results of Experiment 4. Experiment 5 showed that extinction of the odor aversion after AX+ conditioning did not alter the strength of the augmented taste aversion. Odor-mediated taste augmentation is similar to potentiation, in which odor and taste cues operate in a synergistic, not competitive, manner.     

Odor production and utilization under conditions of nonreward and small reward

A series of five experiments was conducted to examine odor production and utilization under conditions of contrasting large and small reward. Using daily, eight-trial double-alternation sequences of reward (L)-nonreward (N) or small reward (S), i.e., LLNNLLNN and LLSSLLSS, appropriate patterning was shown only when an empty goalbox was initially encountered on N or S trials (Experiments 1–5). Manipulations designed to increase frustration, for example, preceding double-alternation training with a block of large-reward trials in Experiment 2, or increasing the L vs S ratio in Experiment 3, failed to yield patterning when small reward was presented at the start of the S-trial confinement period. Patterning was shown when small reward was presented at the end of the S-trial confinement (Experiments 4 and 5). Immediate vs delayed (30 sec) S or N trial goalbox removal failed to result in differences in patterning (Experiments 1 and 2). To distinguish odor production from odor use, subjects trained on an LLSSLLSS pattern preceded subjects trained on an LLNNLLNN pattern (Experiment 5). Because patterning failed to develop in the LLSSLLSS subjects and the first subject in the LLNNLLNN group, it was concluded that a discriminably different cue was not produced on S trials under the LLSSLLSS sequence when small reward was delivered at the beginning of the goalbox confinement period. Shifting small-reward delivery to the end of goalbox confinement resulted in the immediate display of patterning by the first LLNNLLNN subject, and the subsequent development of patterning by the LLSSLLSS subjects.     

Undernutrition by rearing in large litters delays the development of reflexive, locomotor, and memory processes in mice

In three experiments, the effects of early postnatal undernutrition on the ontogeny of several behavioral capacities of varying complexity were investigated in the mouse. Following birth, mouse pups in all experiments were reared in either "normally nourished" or "undernourished" conditions by maintaining litter sizes at 6 or 16, respectively. Experiments 1 and 2 examined the development of adultlike patterns of swimming behaviors and spontaneous locomotor activity, respectively, as a function of litter size. The maturation of both behavior patterns was delayed by about 2 days in the 16-litter mice. In Experiment 3, normally nourished and undernourished mice received 25 trials in a shock-escape T-maze at 9, 11, and 13 days of age, followed by similar retention tests 24 hr later. Although litter size had little effect upon correct turns at each age during training, mice reared in litters of six exhibited significant retention of prior training by 12 days of age, whereas comparable retention was not noted for the large litter mice until 14 days of age. Overall, these results suggest that nutritional deficits, imposed by rearing in large litters during the postnatal period of rapid central nervous system maturation, retard the development of behavioral capacities involving both unlearned and learned responses.     

Enhancement of spatial learning by predator odor in mice: Involvement of amygdala and hippocampus

Olfaction has particular links with learning and memory compared with other sensory cues, due to the interrelations between their neural circuitry. The present study deals with the effects of a putative stressor (i.e. a predator odor) on visuo-spatial learning in mice. Firstly, the results show that a predator odor spread during the Morris water maze task led to learning enhancement. In addition, a stereotaxic approach was used to investigate the involvement of the amygdala in this hippocampus-dependent type of learning. Thus, the performance of mice in visuo-spatial learning under predator odor conditions was dramatically reduced by an ibotenate bilateral amygdala lesion. The involvement of the amygdala was confirmed by a reduced expression of c-fos in the CA1 hippocampus of amygdala-lesioned mice at the end of the learning procedure.Mild exposure to a predator odor during hippocampus-dependent learning therefore leads to an enhancement of performance through the co-activation of the amygdala, probably by a stress mediated mechanism.     

Strain and sex differences on olfactory discrimination learning in C57BL/6J and DBA/2J inbred mice (Mus musculus)

In this study, the authors explored potential strain and sex differences in nonspatial cognitive ability. Beginning around 90 days of age, male and female C57BL/6J (C57) and DBA/2J (DBA) inbred mice (Mus musculus) were tested on a task of simple odor discrimination learning with 3 repeated reversals. Males learned the task more readily than females, and DBA mice learned the task more readily than C57 mice. All differences became evident after repeated testing. Similarity of perseveration measures indicated the differences were not due to inhibitory deficits. Instead, a phase analysis localized differences to a transitional period of reversal learning. Females increased transitional errors that more likely indicated adaptive sampling strategies than memory failures. C57 females used this strategy indiscriminately, but DBA females sampled as a function of environmental uncertainty.     

Chronic exposure to a novel odor increases pups' vocalizations, maternal care, and alters dopaminergic functioning in developing mice

This study was designed to assess the stress effect of manipulation of the olfactory environment in developing mice. In a first experiment it was found that mouse pups could be stressed (as measured by an increase in ultrasonic calls) by removing the litter from the dam for 15 min/day for the first 14 days of life and exposing them to a novel odor (clean bedding). This stress procedure also produced a long-term modification in maternal behavior. The stress response (ultrasounds) and the modification of maternal behavior were prevented by providing the litter with home cage bedding during maternal separation. In a second experiment it was demonstrated that early stress influenced apomorphine-induced wall climbing behavior in 15-day-old mice, suggesting stress-induced alterations in the dopaminergic system. Pups exposed to clean bedding during infancy exhibited more wall climbing behavior than pups never separated from the mother. Moreover, preventing the early stress response during mother-offspring separation, by providing pups with home cage bedding, eliminated the increase in apomorphine-induced wall climbing. Taken together these results suggest that olfactory cues are decisive in characterizing stressful situations inducing both immediate and long-lasting effects in mouse pups.     

Recognition of conspecific odors by laboratory rats (Rattus norvegicus) does not show context specificity

This experiment investigated how contextual cues affect recognition of conspecific odors in laboratory rats (Rattus norvegicus). Rats received 5 encounters with the same odor in the same context. For the 6th test encounter, all rats received a simultaneous presentation of the original odor and a novel odor. The authors tested 1 group of rats (context same) in the same context as before. For the remaining 2 groups, the test encounter was in a different context that 1 group (context different) had experienced but that 1 group (context novel) had not. A significant preference to investigate the novel odor by context-same and context-different rats, but not by context-novel rats, suggests that odor recognition can occur following transfer to a different, but familiar, test context, indicating a lack of context specificity.     

Numerical competence in rats (Rattus norvegicus): Davis and Bradford (1986) extended

The task of rats (Rattus norvegicus) was to enter 1 box of a defined ordinal number among an array of boxes. In Experiments 1 and 2, the rats correctly chose the 4th box from arrays of 6 and 12 boxes, respectively. In Experiments 3 and 4, in which the ordinal number of the correct box was increased in a graduated fashion, they were able to select the correct box even when its position was higher than 10th among 12 and 18 boxes, respectively. In Experiment 5, the possibility that the rats had used cues to the openability of the box doors was ruled out. In Experiments 6 and 7, the rats succeeded in the task even when the total number of boxes was varied from trial to trial. In Experiment 8, both small- and large-sized boxes were used to control for the possibility of using the cumulative length of the boxes as a cue. Overall, the results suggest that performance was based on numerical cues. Intentional acts were occasionally observed but appeared not to be essential for solving the task.     

An automated odor test for rats

The odor-testing apparatus described consists of a circular open-field area opening into four glass tubes, each with an odor source at the far end. When a rat is introduced, each tube is blocked by a grid; when the rat has touched each grid (sampled each odor), the tubes automatically open and recording of preference behavior starts. Two measures of preference are recorded by a photocell outside each tube, the number of visits and the time spent near the odor source. A uniformity test with food odor in all tubes showed that the apparatus did not promote position bias. In two separate sensitivity tests, one with food odor and one with estrous female urine odor, male rats significantly preferred an attractive odor in one tube to odorless controls. The apparatus yields relatively sensitive and reliable odor preference determinations by ensuring sampling of each odor before data are recorded and by eliminating visual, auditory and gustatory cues.