Successful acquisition of an olfactory discrimination test by Asian elephants, Elephas maximus

The present study demonstrates that Asian elephants, Elephas maximus, can successfully be trained to cooperate in an olfactory discrimination test based on a food-rewarded two-alternative instrumental conditioning procedure. The animals learned the basic principle of the test within only 60 trials and readily mastered intramodal stimulus transfer tasks. Further, they were capable of distinguishing between structurally related odor stimuli and remembered the reward value of previously learned odor stimuli after 2, 4, 8, and 16 weeks of recess without any signs of forgetting. The precision and consistency of the elephants' performance in tests of odor discrimination ability and long-term odor memory demonstrate the suitability of this method for assessing olfactory function in this proboscid species. An across-species comparison of several measures of olfactory learning capabilities such as speed of initial task acquisition and ability to master intramodal stimulus transfer tasks shows that Asian elephants are at least as good in their performance as mice, rats, and dogs, and clearly superior to nonhuman primates and fur seals. The results support the notion that Asian elephants may use olfactory cues for social communication and food selection and that the sense of smell may play an important role in the control of their behavior.     

Successful acquisition of an olfactory discrimination paradigm by South African fur seals, Arctocephalus pusillus

The present study demonstrates that South African fur seals, Arctocephalus pusillus, can successfully be trained to discriminate between objects on the basis of odor cues. Using a task based on a food-rewarded two-choice discrimination of simultaneously presented odor stimuli the animals acquired the basic operant conditioning paradigm within 480 to 880 stimulus contacts. Moreover, the fur seals could readily transfer to new S+ and S- stimuli, were capable of distinguishing between fish- and non-fish odors as well as between two fish odors, and were able to remember the reward value of previously learned odor stimuli even after 2- and 15-week breaks. The precision and consistency of the fur seals' performance in tests of discrimination ability and memory demonstrate the suitability of this paradigm for assessing olfactory function in this pinniped. An across-species comparison of several measures of olfactory learning capabilities such as speed of initial task acquisition and ability to master transfer tasks shows that A. pusillus is similar in performance to non-human primates, but inferior to rodents such as mice and rats. The results support the assumption that fur seals may use olfactory cues for social communication and food selection and that the sense of smell may play an hitherto underestimated role in the control of their behavior.     

Rapid and precise control of sniffing during olfactory discrimination in rats

Olfactory perception relies on an active sampling process, sniffing, to rapidly deliver odorants from the environment to the olfactory receptors. The respiration cycle strongly patterns the flow of information into the olfactory systems, but the behavioral significance of particular sniffing patterns is not well understood. Here, we monitored the frequency and timing of nasal respiration in rats performing an odor-mixture-discrimination task that allowed us to test subjects near psychophysical limits and to quantify the precise timing of their behavior. We found that respiration frequencies varied widely from 2 to 12 Hz, but odor discrimination was dependent on 6- to 9-Hz sniffing: rats almost always entered and maintained this frequency band during odor sampling and their accuracy on difficult discrimination dropped when they did not. Moreover, the switch from baseline respiration to sniffing occurred not in response to odor delivery but in anticipation of odor sampling and was executed rapidly, almost always within a single cycle. Interestingly, rats also switched from respiration to rapid sniffing in anticipation of reward delivery, but in a distinct frequency band, 9-12 Hz. These results demonstrate the speed and precision of control over respiration and its significance for olfactory behavioral performance.     

Habenular lesions and discrimination responding to olfactory and visual stimuli

Twenty albino rats with either bilateral habenular lesions or sham operations were trained to discriminate on the basis of olfactory cues between two compartments of a Grice apparatus modified for odor presentation. The discriminative stimulus consisted of different relative concentrations of the odor substance Lilial ranging from 0.1% to 10% air-diluted concentrations. The animals were initially trained using a 10% relative odor stimulus and subsequently tested with a descending series of odorant concentrations. All animals except one acquired the initial discrimination, but successive lowering of the odor concentration disrupted the performance of the experimental group while all controls successfully reached criterion at the lowest concentration used. The rat failing to make the initial odor discrimination was able to discriminate between the two compartments when a visual cue was substituted for the olfactory stimulus. We conclude that the habenular area serves as an important link between olfactory sensory input and motor systems in the rat. It appears that the behavioral changes observed are related more to threshold elevation or an impairment in olfactory integration than to generalized disruption of response inhibition mechanisms.     

Ontogeny of odor discrimination: a method to assess novel odor discrimination in neonatal rats.

Recent research using molecular and functional imaging techniques has demonstrated a highly precise spatial representation of odor quality in the rodent olfactory bulb, which is enhanced by extensive lateral inhibitory circuitry. Much of this olfactory bulb circuitry develops postnatally in the rat, leading to the prediction that behavioral discrimination of odor quality may also emerge postnatally. However, currently no behavioral paradigm has been identified to test this prediction. The present report describes the expression and habituation of odor-evoked heart rate-orienting responses in neonatal rats. The results demonstrate that odor-evoked-orienting responses can be observed at least as early as postnatal day 4 (PN 4), and in those animals showing orienting responses, habituation is constant throughout the postnatal period. Furthermore, the results suggest that examination of cross-habituation using this paradigm can be used to explore odor discrimination ability in neonates. These results lay the foundation for future studies of precise mapping of the ontogeny of novel odor discrimination.     

Sniffing controls an adaptive filter of sensory input to the olfactory bulb

Most sensory stimuli are actively sampled, yet the role of sampling behavior in shaping sensory codes is poorly understood. Mammals sample odors by sniffing, a complex behavior that controls odorant access to receptor neurons. Whether sniffing shapes the neural code for odors remains unclear. We addressed this question by imaging receptor input to the olfactory bulb of awake rats performing odor discriminations that elicited different sniffing behaviors. High-frequency sniffing of an odorant attenuated inputs encoding that odorant, whereas lower sniff frequencies caused little attenuation. Odorants encountered later in a sniff bout were encoded as the combination of that odorant and the background odorant during low-frequency sniffing, but were encoded as the difference between the two odorants during high-frequency sniffing. Thus, sniffing controls an adaptive filter for detecting changes in the odor landscape. These data suggest an unexpected functional role for sniffing and show that sensory codes can be transformed by sampling behavior alone.     

Olfactory discrimination in rats with anterior amygdala lesions

In Experiment 1, rats with posterior lateral olfactory tract/anterior amygdala lesions or with control neocortical lesions were tested for retention of a preoperatively learned odor detection task and for learning on new odor discrimination problems. All rats had perfect or near-perfect retention of the detection task, and there were no discernible differences between groups in learning on the new odor discrimination problems. In Experiment 2, an intensity-difference threshold for olfaction was determined in 4 rats before and after lesions of the posterior lateral olfactory tract and anterior amygdala. There were no apparent differences between pre- and postoperative performances on this psychophysical test. These results indicate that lateral olfactory tract projections to the amygdala and posterior olfactory cortex are not essential for normal performance on simple olfactory discrimination tasks.     

Olfactory sensitivity, learning and cognition in young adult and aged male Wistar rats

Psychophysical experiments with male Wistar rats, ranging from 2 to more than 25 months old, revealed age-related differences in olfactory sensitivity. The highest sensitivities were found in rats 13 months old, and the lowest sensitivity was found in the group aged 25 months and older. Consequently, we considered the hypotheses that young rats will require less time and less trials than aged conspecifics to learn an olfactory discrimination task and that olfactory cognitive abilities will be reduced in older individuals. Rats were initially trained in an olfactometer using operant techniques to discriminate between the odor ethyl acetate (EA) and clean air. Next, young adult and 28-month-old rats were tested on seven different go/no-go odor discrimination tasks. Aged rats performed as well as young adults did on all tasks and we conclude that, for a variety of odor discrimination problems, aged rats show no deterioration in learning ability. This is the first report on olfactory sensitivity, learning ability and cognition in Wistar rats that have passed the normal life span for this strain. Data show that the inability to learn and cognitive deficits do not necessarily develop with age.     

Dopamine D(2) receptor activation modulates perceived odor intensity

Dopaminergic modulation affects odor detection thresholds and olfactory discrimination capabilities in rats. The authors show that dopamine D(2) receptor modulation affects odor discrimination capabilities in a manner similar to the modulation of stimulus intensity. Performance in a simultaneous odor discrimination task was systematically altered by manipulations of both odorant concentration and D(2) receptor activation (agonist quinpirole, 0.025-0.5 mg/kg; antagonist spiperone, 0.5 mg/kg). Rats' discrimination performance systematically improved at higher odor concentrations. Blockade of D(2) receptors improved performance equivalent to increasing odor concentration by 2 log units, whereas activation of D(2) receptors reduced odor discrimination performance in a dose-dependent manner. Bulbar dopamine release may serve a gain control function in the olfactory system, optimizing its sensitivity to changes in the chemosensory environment.     

A two-choice discrimination method to assess olfactory performance in pigtailed macaques, Macaca nemestrina

Four pigtailed macaques were trained in a new two-choice olfactory discrimination method. They learned the initial task within 3 months, requiring a maximum of 900 trials. After the method was established, we investigated the olfactory threshold of three monkeys for the odors peanut, iso-amyl acetate, and n-pentanoic acid. The animals detected peanut odor in dilutions as low as 1:10000. They were able to perceive iso-amyl acetate up to a 30000-fold dilution (animals F1 and M2), respectively in a 30 Mio-fold dilution (animal M1). The sensitivity for n-pentanoic acid ranged between a dilution of 1:30000 (F1), 1:100000 (M2), and 1:300000 (M1). A comparison with the thresholds of other species demonstrates that the olfactory sensitivity of pigtailed macaques is not necessarily inferior to that of species that are believed to have a very keen sense of smell, such as dogs and rats. The sensitivity for certain odors seems to reflect their biological relevance for the tested species. The fact that the threshold for peanut odor obtained in this study is lower than the one found in a previous study with pigtailed macaques using a multiple olfactory discrimination method indicates that the new two-choice discrimination method is a better candidate for the assessment of olfactory abilities in pigtailed macaques.     

Discrimination among odorants by single neurons of the rat olfactory bulb

1. Intracellular and extracellular recordings were made from rat olfactory bulb mitral and tufted cells during odor stimulation and during electrical stimulation of the olfactory nerve. Neurons were identified by horseradish peroxidase injections and/or antidromic activation. The presentation of multiple concentrations of at least one odorant in a cyclic artificial sniff paradigm, as reported previously (10), allowed the study of odor responses. This approach was extended to multiple odorants to compare their concentration-response profiles. This procedure avoids the problems of interpretation resulting from nonequivalence of the effective concentrations of different odorants used as stimuli that have characterized previous studies of odor quality effects. Comparisons of intracellular events and responses to electrical stimulation with the odor-induced spike train activity allow us to begin to delineate the local circuitry involved in generating odor-induced responses. 2. The concentration-response profiles of the 72 cells in the present study are comparable to those previously reported for output neurons of the olfactory bulb, showing ordered changes in the temporal patterning of spike activity with step changes in odor concentration. However, eight of the neurons exhibited inhibitory responses to lower concentrations, but excitation, at similar latency, to higher concentrations of the same odorant. These data emphasize that to study pattern changes induced by changing odor quality the influence of stimulus intensity must also be carefully examined. The data also provide evidence that the temporal pattern evoked by an odorant is probably not in itself the code for odor quality recognition. 3. Complete concentration-response profiles, including subthreshold concentrations, to more than one odorant show that, although responses to the different odorant can evolve systematically with concentration, the responses to different odorants can evolve through very different patterns. For example, in some cells, the response patterns to different odors were complementary in form. These results demonstrate that the patterned responses of olfactory bulb neurons can reflect changes in odor quality as well as intensity. 4. Intracellular recording was employed to compare the temporal patterning of spikes during odor stimulation with membrane potential changes. In some cases, the spike pattern was closely correlated with apparent postsynaptic potentials. However, there were several clear exceptions. In five cells, a prominent hyperpolarization, seen in the first sniff of a series of 10 consecutive sniffs, was associated with pauses in spike activity. In the following     

Identification of single dissimilar odors is achieved by humans with a single sniff

The duration that a single odor needs to be sniffed for identification was determined for 18 humans. A hot wire anemometer and an oscilloscope were used to monitor the duration, volume and inhalation rate of sniffs. In Experiment 1 subjects used 1, 3 or 5 natural sniffs, or an unlimited number of natural sniffs to sample seven dissimilar single odors of moderate perceived intensity, and demonstrated that each odor could be identified with a single sniff. In Experiment 2 subjects demonstrated that each of the odors could be identified with the shortest sniff (0.42 sec) they could physically achieve. In Experiment 3 tests with two of the odorants at several concentrations showed that sniff duration influences identification over a narrow range of concentrations that is just above the recognition threshold. These results together with earlier data that described the optimum conditions for the detection of an odor and the perception of odor intensity, provide information that is necessary for the development of a standard olfactometer and standard methods for human olfactory measurements.     

Intracellular responses of identified rat olfactory bulb interneurons to electrical and odor stimulation

1. Intracellular recordings were made from 28 granule cells and 6 periglomerular cells of the rat olfactory bulb during odor stimulation and electrical stimulation of the olfactory nerve layer (ONL) and lateral olfactory tract (LOT). Neurons were identified by injection of horseradish peroxidase (HRP) or biocytin and/or intracellular response characteristics. Odorants were presented in a cyclic sniff paradigm, as reported previously. 2. All interneurons could be activated from a wide number of stimulation sites on the ONL, with distances exceeding their known dendritic spreads and the dispersion of nerve fibers within the ONL, indicating that multisynaptic pathways must also exist at the glomerular region. All types of interneurons also responded to odorant stimulation, showing a variety of responses. 3. Granule cells responded to electrical stimulation of the LOT and ONL as reported previously. However, intracellular potential, excitability, and conductance analysis suggested that the mitral cell-mediated excitatory postsynaptic potential (EPSP) is followed by a long inhibitory postsynaptic potential (IPSP). An early negative potential, before the EPSP, was also observed in every granule cell and correlated with component I of the extracellular LOT-induced field potential. We have interpreted this negativity as a "field effect," that may be diagnostic of granule cells. 4. Most granule cells exhibited excitatory responses to odorant stimulation. Odors could produce spiking responses that were either nonhabituating (response to every sniff) or rapidly habituating (response to first sniff only). Other granule cells, while spiking to electrical stimulation, showed depolarizations that did not evoke spikes to odor stimulation. These depolarizations were transient with each sniff or sustained across a series of sniffs. These physiological differences to odor stimulation correlated with granule cell position beneath the mitral cell layer for 12 cells, suggesting that morphological subtypes of granule cells may show physiological differences. Some features of the granule cell odor responses seem to correlate with some of the features we have observed in mitral/tufted cell intracellular recordings. Only one cell showed inhibition to odors. 5. Periglomerular (PG) cells showed a response to ONL stimulation that was unlike that found in other olfactory bulb neurons. There was a long-duration hyperpolarization after a spike and large depolarization or burst of spikes (20-30 ms in duration). Odor stimulation produced simple bursts of action potentials, Odor stimulation produced simple bursts of action potentials, suggesting that PG cells may simply follow input from the olfactory nerve.(ABSTRACT TRUNCATED AT 400 WORDS)     

Physostigmine enhances performance on an odor mixture discrimination test

Acetylcholine is found within key sectors of the olfactory pathway, and is the neurotransmitter for many bulbopetal axons terminating in the glomerular and internal plexiform layers of the olfactory bulb. The present study determined whether systemically administered physostigmine, a cholinesterase inhibitor, alters the rat's ability to discern among odorant mixtures. Following appropriate training, the performance of eight rats was measured every third day on an odor mixture discrimination test with six levels of difficulty. On each test day (separated from one another by 3 days), a different drug treatment was administered [i.e., 0.00 (saline), 0.05, 0.10, or 0.20 mg/kg physostigmine]. The presentation order of the treatments was counterbalanced across subjects using 4 x 4 Latin squares. The mixture discrimination test consisted of discerning the odor of an airstream coming from the saturated head space of a 1% concentration of ethyl acetate from an airstream saturated with a 1% concentration of ethyl acetate and various concentrations of butanol (i.e., 1, 0.5, 0.1, 0.05, 0.01, or 0.005%). Physostigmine was found to enhance odor discrimination performance on the more difficult discrimination tasks in a dose-related manner, suggesting that cholinergic activation may sharpen the ability of rats to discern subtle differences among complex odor stimuli.     

Taste-potentiated odor aversion learning: role of the amygdaloid basolateral complex and central nucleus.

The present study examined the relative contributions of the amygdaloid basolateral complex (ABL) and central nucleus (CN) to taste-potentiated odor aversion (TPOA) learning--an associative learning task that is dependent on information processing in two sensory modalities. In Experiment 1, rats with neurotoxic lesions of these systems were trained on the TPOA task by presenting a compound taste-odor conditioned stimulus, which was followed by LiCl administration. Results showed that ABL damage caused an impairment in potentiated odor aversion learning but no deficit in the conditioned taste aversion. In contrast, rats with CN damage learned both tasks. Experiment 2 examined the effects of ABL damage on TPOA and odor discrimination learning. The odor discrimination procedure used a place preference task to demonstrate normal processing of olfactory information. Results indicated that although ABL-lesioned animals were impaired on TPOA, there was no deficit in odor discrimination learning.     

Odor-related bulbar EEG spatial pattern analysis during appetitive conditioning in rabbits

Mildly thirsty rabbits were classically conditioned by reinforcement with water to give a discriminative licking response to the presentation of odors. The jaw movement component of the licking conditioned response (JM CR) was elicited only by the reinforced odor; an increase in the relative frequency of sniffing (RR CR) occurred to both reinforced (CS+) and nonreinforced (CS-) odors. Oscillatory electroencephalographic bursts of high-frequency (40-80 Hz) potentials were recorded epidurally from the lateral olfactory bulb with 64-electrode arrays (8 X 8, 3.5 X 3.5 mm) chronically implanted. Emphasis was on comparing bursts during odor presentation with bursts preceding odor arrival on each trial. A "detection" burst was characterized as occurring immediately after odor arrival and before the sniff response. "Discrimination" bursts occurred during the RR CR and before the JM CR onset. Significant air-odor burst differences (together with sniffing) occurred through up to six sessions for both CS+ and CS- odors for "discrimination" bursts but not for "detection" bursts.     

Changes in spontaneous,odor modulated and shock induced behavior patterns following discrete olfactory system lesions

Three groups of male hooded rats were preoperatively matched and then sham operated (SHAM), bilaterally lateral olfactory tract lesioned or anterior olfactory nucleus/anterior commissure lesioned. In one experiment, spontaneous behavior patterns emitted in an exploration field containing different odors were quantified during satiated and food deprived conditions. In other experiments, flinch and jump thresholds to electric shock and running patterns in an appetitively motivated straight alley experiment were measured. All lesioned animals were hyperactive and typically froze and groomed less than SHAMs while sniffing and rearing patterns differentiated the lesioned and SHAM groups in several ways. All animals had similar flinch and jump thresholds and also emitted similar types of responses to electric shock. In the straight alley, odors from normal and stressed rats had little effect on the running time of the experimental animals while a faint cat odor strongly inhibited SHAM running behavior. Responses to a novel chemical odor (trimethylpentane) and to changes in the alley floor or electric shock applied to the floor were minimal in all animals. The results were discussed against a background of other olfactory system lesions and some evidence separating the effects of olfactory cues from nonolfactory lesion effects was presented. Finally, problems associated with tests for olfactory discrimination were discussed. A need for more rigorous and specific discrimination tests in behavioral studies involving anosmia was emphasized.     

A rose by any other name: would it smell as sweet?

We examined whether presenting an odor with a positive, neutral, or negative name would influence how people perceive it. In experiment 1, 40 participants rated 15 odors for their pleasantness, intensity, and arousal. In experiment 2, 30 participants passively smelled 10 odors while their skin conductance (SC), heart rate (HR), and sniffing were recorded. We found significant overall effects of odor names on perceived pleasantness, intensity, and arousal. Pleasantness showed the most robust effect of odor names: the same odors were perceived as more pleasant when presented with positive than with neutral and negative names and when presented with neutral than with negative names. In addition, odorants were rated as more intense when presented with negative than with neutral and positive names and as more arousing when presented with positive than with neutral names. Furthermore, SC and sniff volumes, but not HR, were modified by odor names, and the SC changes could not be accounted for by sniffing changes. Importantly, odor names presented with odorless water did not produce any effect on skin conductance and sniff volumes, ruling out the possibility that the naming-related findings were triggered by an emotional reaction to odor names. Taken together, these experiments show that there is a lot to a name, at least when it comes to olfactory perception.     

Does intranasal application of zinc sulfate produce anosmia in the rat?

Transport of wheat germ agglutinin-horseradish peroxidase (WGA-HRP) from olfactory sensory neurons to the olfactory bulb as well as odor detection and discrimination were examined in rats in which each nasal epithelium had been irrigated with 0.1-0.5 ml 5% zinc sulfate. After treatment, rats showed few or no deficits in discriminating among odors and in detecting high (1%-0.01%) concentrations of ethyl acetate, but some had deficits in detecting lower concentrations of the odor. In most cases, HRP reaction product filled more than 30% of olfactory bulb glomeruli 2-4 days after treatment with ZnSO4. The behavioral outcomes are in agreement with recent reports of considerable savings in olfaction even after severe reduction of afferent projections to the olfactory bulb. We conclude that, in the rat, intranasal application of ZnSO4, as generally practiced, does not produce anosmia.     

Comparison of odor receptive field plasticity in the rat olfactory bulb and anterior piriform cortex

Recent work in the anterior piriform cortex (aPCX) has demonstrated that cortical odor receptive fields are highly dynamic, showing rapid changes of both firing rate and temporal patterning within relatively few inhalations of an odor, despite relatively maintained, patterned input from olfactory bulb mitral/tufted cells. The present experiment examined the precision (odor-specificity) of this receptive field plasticity and compared it with the primary cortical afferent, olfactory bulb mitral/tufted cells. Adult Long-Evans hooded rats, urethan anesthetized and freely breathing, were used for single-unit recording from mitral/tufted and aPCX layer II/III neurons. Partial mapping of receptive fields to alkane odors (pentane, heptane, and nonane) was performed before and immediately after habituation (50-s exposure) to one of the alkanes. The results demonstrated that odor habituation of aPCX responses was odor specific, with minimal cross-habituation between alkanes differing by as few as two carbons. Mitral/tufted cells, however, showed strong cross-habituation within the odor set with the most profound cross effects to carbon chains shorter than the habituating stimulus. The results suggest that although mitral/tufted cells and aPCX neurons have roughly similar odor receptive fields, aPCX neurons have significantly better odor discrimination within their receptive field. The results have important implications for understanding the underlying bases of receptive fields in olfactory system neurons and the mechanisms of odor discrimination and memory.