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     

Cross-modal integration between odors and abstract symbols

This study aimed to investigate the cross-modal association of an “abstract symbol,” designed for representation of an odor, with its corresponding odor. First, to explore the associations of abstract symbols with odors, participants were asked to match 8 odors with 19 different abstract symbols (Experiment 1). Next, we determined whether congruent symbols could modulate olfactory perception and olfactory event-related potentials (ERPs) (Experiment 2). One of two odors (phenylethanol (PEA) or 1-butanol) was presented with one of three conditions (congruent or incongruent symbol, no-symbol), and participants were asked to rate odor intensity and pleasantness during olfactory ERP recordings. Experiment 1 demonstrated that certain abstract symbols could be paired with specific odors. In Experiment 2 congruent symbol enhanced the intensity of PEA compared to no-symbol presentation. In addition, the respective congruent symbol increased the pleasantness of PEA and the unpleasantness of 1-butanol. Finally, compared to the incongruent symbol, the congruent symbol produced significantly higher amplitudes and shorter latencies in the N1 peak of olfactory ERPs. In conclusion, our findings demonstrated that abstract symbols may be associated with specific odors.     

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.     

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)     

Identification of unpleasant odors is independent of age.

The purpose of this study was to investigate (a) the relationship between identification proficiency for specific odors and chronological age and (b) to determine whether the relationships were related to perceived quality (i.e., judgments of familiarity, intensity, and hedonics) of the odor item. Data from 472 subjects (227 men, 245 women) ranging in age from 18 to 79 years were assessed in a cued identification test comprising 16 odors. The results indicated a reliable age effect in overall odor identification performance. Further analyses indicated that the observed age-related deficit was odorant-specific, with some odors being equally well identified across age cohorts and others showing sensitivity to the process of aging. Additional examination regarding the observed age-differential effects across the different odor types indicated that these may be understood according to the pleasantness/upleasantness associated with the odor. Specifically, odors perceived as unpleasant showed age invariance whereas odors rated as pleasant exhibited age sensitivity.     

Olfactory lateralization: odor intensity but not the hedonic estimation is lateralized

An earlier study in humans comparing the olfactory sensitivity of both nostrils revealed a small but significant advantage of the right nostril for detection and for olfactory quality discrimination. However lateralization was not evaluated for the perception of odor intensity and hedonic evaluation (pleasantness/unpleasantness). Thus we investigated lateralization of olfactory intensity and hedonic evaluation in right-handed healthy volunteers (n=186) from the HeDoS-F database (Hedonic Database of Smell-Franconia). For olfactory evaluation the Sniffin' Stick Test was employed with the parameters detection, discrimination, identification and extended by analogue hedonic and intensity rating scales. Over all odors subjects rated the perceived intensity significantly higher following stimulation of the right compared to the left nostril. The analysis of the single odors of the Sniffin' Stick Test consistently confirmed higher intensity ratings for the right compared to the left nostril reaching a statistically significant difference for 10 out of 16 odors. In contrast we found no significant differences between the nostrils for the hedonic estimates over all odors. Differences in odor detection, discrimination and identification did not reach a statistically significant level, but for all these parameters the scores of the right nostril were slightly higher compared to the left nostril. For odor identification, however, a statistical tendency was observed. Based on our results we concluded that olfactory intensity estimates represent the most sensitive parameter of olfactory lateralization.     

The capacity of humans to identify odors in mixtures

One hundred and twenty-three subjects were given the task of identifying the constituents of stimuli consisting of 1-5 odorants. The highest level of identification occurred with single odors and few subjects correctly identified the constituents of mixtures. Since the stimuli were common, dissimilar odors, the results suggest that the capacity of humans to process information about odors perceived simultaneously may be limited, or that odors in mixtures blend to form a new odor with few of the characteristics of the constituent odors.     

Optimum perception of odor intensity by humans

The sniff duration that provides optimum perception of odor intensity was determined for 17 humans. Subjects were trained to match the duration of their sniff to the duration of a buzzer that sounded for 0.2, 0.5, 1.0 or 2.0 sec. Sniff characteristics were monitored with a hot wire anemometer and an oscilloscope. Intensity estimates were obtained at the four durations for three concentrations of phenyl ethanol, butanol and propionic acid. Optimum perception of intensity occurred between 0.39 and 0.64 sec for phenyl ethanol and propionic acid and a value of no more than 1.63 sec is proposed for butanol. The longer duration for butanol is attributed to the delayed response of nerves in the throat which appear to respond to this odorant but not to the others. The complexity of the intensity sensation and implications of the results for neurophysiological studies of intensity coding are discussed and the properties of an olfactometer for odor intensity measurements are outlined.     

Influence of odor cueing on the retrieval processes for autobiographical memories

This study investigated the influence of odor cueing on the retrieval process for autobiographical memories. In Experiment 1, forty two participants were asked to retrieve autobiographical memories in response to a label cue only, or a label cue with a congruent odor cue, or label cue with an incongruent odor cue. The results showed that in the label cue only condition and the incongruent odor cue condition, the latency with a concurrent task was slower than with no concurrent task. However, this was not observed in the congruent odor cue condition. In order to verify the results of Experiment 1, in Experiment 2, twenty participants were investigated with regard to autobiographical memories cued by odors having a high or low rate of identification. The results showed that memories cued by odors with a high rate of identification were retrieved faster. These results suggest that dual processing by odor and label promotes retrieval processes for autobiographical memories.     

Rapid olfactory processing implicates subcortical control of an olfactomotor system

Sniffs are modulated in response to odor content. Higher concentrations of odor induce lesser-volume sniffs. This phenomenon implicates a neural feedback mechanism that measures sensory input (odor concentration) and modulates motor output (sniffing) accordingly. Here we used air-dilution olfactometry to probe the time course of this olfactomotor mechanism. A stainless-steel computer-controlled olfactometer, equipped with mass flow controllers, temperature and humidity control, and on-line photo-ionization detection, was coupled to a highly sensitive pneumatotachograph that measured nasal flow. The olfactometer was used to generate four ascending concentrations of the odorants propionic acid and phenethyl alcohol. Sniff volume was inversely related to odor concentration (P > 0.0001). Sniffs were uniform and concentration independent for the initial 150 ms but acquired a concentration-dependent flowrate as early as 160 ms following sniff onset for propionic acid (P > 0.05) and 260 ms for phenethyl alcohol (P > 0.05). Considering that odorant transduction takes around 150 ms and odorant-induced cortical evoked potentials have latencies of around 300 ms, the rapid motor adjustments measured here suggest that olfactomotor sniff feedback control is subcortical and may rely on neural mechanisms similar to those that modulate eye movements to accommodate vision and ear movements to accommodate audition.     

Effects of altered olfactory experiences on the development of infant rats' responses to odors

A “natural” olfactory learning paradigm was used to assess the effects of an altered perinatal olfactory environment on the development of odor-elicited behavor in young rats. Infant rats (from 3 to 12 days of age) reared by dams fed a eucalyptol-adulterated diet responded to the odor of eucalyptol with high levels of activity, mouthing, and probing, and also demonstrated a marked preference for that odor in a two-choice situation (Experiment 1). The effects were observed only in pups whose dam was fed eucalyptol-adulterated diet and were not observed in pups exposed to nonmaternal sources of odor. The intensity of behavioral activity elicited by eucalyptol odor varied, to some extent, with the concentration of the eucalyptol in the dam's diet during prenatal exposure (Experiment 2). Cross-fostering revealed that these effects were due almost entirely to the pups' postnatal exposure to the eucalyptol odor (Experiment 3). These findings indicate that novel odors specifically associated with the mother can gain control over orientation and ingestion-related behaviors. © 1996 John Wiley & Sons, Inc.     

Speed and accuracy of olfactory discrimination in the rat

The sense of smell is typically thought of as a 'slow' sense, but the true temporal constraints on the accuracy of olfactory perception are not known. It has been proposed that animals make finer odor discriminations at the expense of additional processing time. To test this idea, we measured the relationship between the speed and accuracy of olfactory discrimination in rats. We found that speed of discrimination was independent of odor similarity, as measured by overlap of glomerular activity patterns. Even when pushed to psychophysical limits using mixtures of two odors, rats needed to take only one sniff (<200 ms at theta frequency) to make a decision of maximum accuracy. These results show that, for the purpose of odor quality discrimination, a fully refined olfactory sensory representation can emerge within a single sensorimotor or theta cycle, suggesting that each sniff can be considered a snapshot of the olfactory world.     

Neural correlates of social odor recognition and the representation of individual distinctive social odors within entorhinal cortex and ventral subiculum

Recognition of individual conspecifics is important for social behavior and requires the formation of memories for individually distinctive social signals. Individual recognition is often mediated by olfactory cues in mammals, especially nocturnal rodents such as golden hamsters. In hamsters, this form of recognition requires main olfactory system input to the lateral entorhinal cortex (LEnt). Here, we tested whether neurons in LEnt and the nearby ventral subiculum (VS) would show cellular correlates of this natural form of recognition memory. Two hundred ninety single neurons were recorded from both superficial (SE) and deep layers of LEnt (DE) and VS while male hamsters investigated volatile odorants from female vaginal secretions. Many neurons encoded differences between female's odors with many discriminating between odors from different individual females but not between different odor samples from the same female. Other neurons discriminated between odor samples from one female and generalized across collections from other females. LEnt and VS neurons showed enhanced or suppressed cellular activity during investigation of previously presented odors and in response to novel odors. A majority of SE neurons decreased firing to odor repetition and increased activity to novel odors. In contrast, DE neurons often showed suppressed activity in response to novel odors. Thus, neurons in LEnt and VS of male hamsters encode information that is critical for the identification and recognition of individual females by odor cues. This study reveals cellular mechanisms in LEnt and VS that may mediate a natural form of recognition memory in hamsters. These neuronal responses were similar to those observed in rats and monkeys during performance in standard recognition memory tasks. Consequently, the present data extend our understanding of the cellular basis for recognition memory and suggest that individual recognition requires similar neural mechanisms as those employed in laboratory tests of recognition memory.     

Respiratory responses to olfactory stimuli in Parkinson's disease

There are many reports of olfactory impairment in patients with Parkinson's disease (PD) and the impairment can be observed before the appearance of typical PD symptom. Accordingly, olfactory screening tests may predict disease onset and indicates a need for early treatment before classic signs of the disease. Olfaction is dependent on inspiration, and activation of olfactory limbic areas are synchronized with the natural breathing cycle in animals and humans. Subconscious changes in respiratory pattern occur in response to odor stimulation. The use of olfactory stimuli to investigate respiratory pattern could be used to assess olfactory perception and serve as an index for olfactory limbic activation. In this study, we tested olfactory acuity in normal subjects and in patients with PD and recorded V(O2) and respiratory variables during pleasant and unpleasant odor presentation. All subjects were able to detect the odorants; however patients with PD were assigned to one of two groups, group that could recognize odors or the group with impaired odor recognition. Respiratory response toward unpleasant and pleasant odor recognition were weak in PD groups who could recognize odors than normal subject as well as emotional response to odor stimuli. PD group with impaired odor recognition showed no respiratory response toward odor stimuli. PD may experience difficulty in feeling positive emotions toward pleasant odors prior to the unpleasant odor because respiratory responses to pleasant odors may also be related to higher processes including intentional control of breathing pattern as a result of olfactory cortex processing and perceptions or emotions.     

Influence of the odorization of the rearing environment on the development of odor-guided behavior in rat pups

The study describes a phenomenon in which attraction of rat pups to artificial odors disappeared after the first week of life. In experiment 1, pups were continually exposed to either: (1) the normal odors present in the litter or (2) the same odors enriched with one of four artificial odors present in the dam's food. Pups were tested daily with the odors of normal or adulterated soiled shavings from their nests. The results show that attraction to the normal test shavings lasted throughout the testing period (PN 1-7). However, pups raised on odorized shavings exhibited an attraction to the artificial odor until day 6 only, not on day 7. In experiment 2, pups were tested with dam's artificially adulterated food. The results show that the artificial odor, and not the food odor, was responsible for the lack of attraction on day 7. Experiment 3 was carried out to determine whether the date on which attraction to artificial odors changed might be specific to postnatal day 7 or whether the duration of odor exposure in test conditions was the important factor. The results suggest that the age of pup is the more important variable.     

Role of temporal order and odor intensity in taste-potentiated odor aversions

The role of the temporal order of odor and taste was studied in two experiments, and a third experiment studied the role of odor intensity in flavor-toxicosis conditioning with thirsty rats licking water spouts in a "wind tunnel." In all experiments, odors and tastes were presented for 2 min to rats, and 30 min later, a toxin (lithium chloride) was intubated. In Experiment 1, an odor was presented 90 s before, during, or 90 s after a taste to independent groups. Experiment 2 was a within-subjects partial replication of the first. Each rat was presented with one odor, then a taste, then a second odor with each stimulus separated by 45 s. The results of Experiments 1 and 2 indicated that (a) odor alone is not associated with illness under our conditions, (b) presenting an odor and a taste at the same time potentiates the odor component so that it is associated with illness, (c) 45-s and 90-s intervals between odor and taste eliminate potentiation, and (d) taste and odor interact asymetrically; that is, odor has little affect on the development of taste-illness associations. In Experiment 3, an odor and a taste were presented simultaneously, and odor intensity varied. As odor intensity increased, the strength of the taste-potentiated odor aversion increased, whereas the aversion to the taste remained constant. However, even at the highest intensity, odor presented in the absence of taste did not result in odor aversions.     

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.     

Dynamics of olfactory bulb input and output activity during odor stimulation in zebrafish

The processing of odor-evoked activity in the olfactory bulb (OB) of zebrafish was studied by extracellular single unit recordings from the input and output neurons, i.e., olfactory receptor neurons (ORNs) and mitral cells (MCs), respectively. A panel of 16 natural amino acid odors was used as stimuli. Responses of MCs, but not ORNs, changed profoundly during the first few hundred milliseconds after response onset. In MCs, but not ORNs, the total evoked excitatory activity in the population was initially odor-dependent but subsequently converged to a common level. Hence, the overall population activity is regulated by network interactions in the OB. The tuning widths of both ORN and MC response profiles were similar and, on average, stable over time. However, when analyzed for individual neurons, MC response profiles could sharpen (excitatory response to fewer odors) or broaden (excitatory response to more odors), whereas ORN response profiles remained nearly unchanged. Several observations indicate that dynamic inhibition plays an important role in this remodeling. Finally, the reliability of odor identification based on MC population activity patterns improved over time, whereas odor identification based on ORN activity patterns was most reliable early in the odor response. These results demonstrate that several properties of MC, but not ORN, activity change during the initial phase of the odor response with important consequences for odor-encoding activity patterns. Furthermore, our data indicate that inhibitory interactions in the OB are important in dynamically shaping the activity of OB output neurons.     

Odor-induced changes in taste perception

We investigated odor-induced changes in taste perception (OICTP), by examining the influence of strawberry and soy sauce odors on perceived sweetness (Experiment 1) and saltiness (Experiment 2). We explored whether taste-smell interactions occur at the central level, by delivering odorants (strawberry, soy sauce, odorless water) and tastants (sucrose, sodium chloride) separately, and whether effects of imagined odors are comparable to those of physically presented odors. We found specific taste-smell interactions: sweetness enhancement induced by strawberry odor and saltiness enhancement induced by soy sauce odor. These interactions were elicited with separate delivery of olfactory and gustatory stimuli. Secondly, we found a similar but rather limited effect with the imagined odors: imagined strawberry enhanced perceived sweetness of water solutions, and imagined soy sauce enhanced perceived saltiness of weak sodium chloride solutions. We concluded that OICTP is a centrally mediated phenomenon, and that imagined odors can to some extent induce changes in perceived taste intensity comparable to those elicited by perceived odors.