Odor similarity does not influence the time needed for odor processing

The brain's link between perception and action involves several steps, which include stimulus transduction, neuronal coding of the stimulus, comparison to a memory template and choice of an appropriate behavioral response. All of these need time, and many studies report that the time needed to compare two stimuli correlates inversely with the perceived distance between them. We developed a behavioral assay in which we tested the time that a honeybee needs to discriminate between odors consisting of mixtures of two components, and included both very similar and very different stimuli spanning four log-concentration ranges. Bees learned to discriminate all odors, including very similar odors and the same odor at different concentrations. Even though discriminating two very similar odors appears to be a more difficult task than discriminating two very distinct substances, we found that the time needed to make a choice for or against an odor was independent of odor similarity. Our data suggest that, irrespective of the nature of the olfactory code, the bee olfactory system evaluates odor quality after a constant interval. This may ensure that odors are only assessed after the olfactory network has optimized its representation.     

Odor representations in olfactory cortex: distributed rate coding and decorrelated population activity

How information encoded in neuronal spike trains is used to guide sensory decisions is a fundamental question. In olfaction, a single sniff is sufficient for fine odor discrimination but the neural representations on which olfactory decisions are based are unclear. Here, we recorded neural ensemble activity in the anterior piriform cortex (aPC) of rats performing an odor mixture categorization task. We show that odors evoke transient bursts locked to sniff onset and that odor identity can be better decoded using burst spike counts than by spike latencies or temporal patterns. Surprisingly, aPC ensembles also exhibited near-zero noise correlations during odor stimulation. Consequently, fewer than 100 aPC neurons provided sufficient information to account for behavioral speed and accuracy, suggesting that behavioral performance limits arise downstream of aPC. These findings demonstrate profound transformations in the dynamics of odor representations from the olfactory bulb to cortex and reveal likely substrates for odor-guided decisions. VIDEO ABSTRACT:     

Modeling peripheral olfactory coding in Drosophila larvae

The Drosophila larva possesses just 21 unique and identifiable pairs of olfactory sensory neurons (OSNs), enabling investigation of the contribution of individual OSN classes to the peripheral olfactory code. We combined electrophysiological and computational modeling to explore the nature of the peripheral olfactory code in situ. We recorded firing responses of 19/21 OSNs to a panel of 19 odors. This was achieved by creating larvae expressing just one functioning class of odorant receptor, and hence OSN. Odor response profiles of each OSN class were highly specific and unique. However many OSN-odor pairs yielded variable responses, some of which were statistically indistinguishable from background activity. We used these electrophysiological data, incorporating both responses and spontaneous firing activity, to develop a bayesian decoding model of olfactory processing. The model was able to accurately predict odor identity from raw OSN responses; prediction accuracy ranged from 12%-77% (mean for all odors 45.2%) but was always significantly above chance (5.6%). However, there was no correlation between prediction accuracy for a given odor and the strength of responses of wild-type larvae to the same odor in a behavioral assay. We also used the model to predict the ability of the code to discriminate between pairs of odors. Some of these predictions were supported in a behavioral discrimination (masking) assay but others were not. We conclude that our model of the peripheral code represents basic features of odor detection and discrimination, yielding insights into the information available to higher processing structures in the brain.     

Olfactory predator recognition in the brown mouse lemur (Microcebus rufus) in Ranomafana National Park,Madagascar

Predator odors such as urine and feces are known to elicit antipredator behaviors in prey including avoidance, fear, and curiosity. We measured how wild brown mouse lemurs (Microcebus rufus) responded to odors of mammalian, avian, and snake predators as well as nonpredator controls. The first experiment took place under controlled conditions in a laboratory where we recorded the occurrence of four behavioral categories (ignore, curiosity, alert, and fear) in response to a single odor. Subjects exhibited behavioral change significantly more often in response to the predator than to control stimuli, but did not distinguish between familiar and unfamiliar predators. Mammalian predator urine and feces were most likely to elicit behavioral change. The owl was the only predator to never elicit behavioral change, possibly because owls do not provide relevant odor cues. A second experiment employing live traps in the forest found that neither predator nor control odors affected the likelihood of capture. Due to their longevity, odors do not provide accurate information of spatial and temporal risk, and while mouse lemurs may have initially hesitated to enter a trap, in the absence of additional information about risk, they may have eventually ignored the stimuli. This study found that brown mouse lemurs are able to distinguish between predator and nonpredator odors, and that risk assessment may be affected by the experience, as well as predator and sensory stimulus quality.     

Different thresholds for detection and discrimination of odors in the honey bee (Apis mellifera)

Naturally occurring odors used by animals for mate recognition, food identification and other purposes must be detected at concentrations that vary across several orders of magnitude. Olfactory systems must therefore have the capacity to represent odors over a large range of concentrations regardless of dramatic changes in the salience, or perceived intensity, of a stimulus. The stability of the representation of an odor relative to other odors across concentration has not been extensively evaluated. We tested the ability of honey bees to discriminate pure odorants across a range of concentrations at and above their detection threshold. Our study showed that pure odorant compounds became progressively easier for honey bees to discriminate with increasing concentration. Discrimination is, therefore, a function of odorant concentration. We hypothesize that the recruitment of sensory cell populations across a range of concentrations may be important for odor coding, perhaps by changing its perceptual qualities or by increasing its salience against background stimuli, and that this mechanism is a general property of olfactory systems.     

Changes in odor quality discrimination following recovery from olfactory nerve transection

Following recovery from olfactory nerve transection, animals regain their ability to discriminate between odors. Odor discrimination is restored after new neurons establish connections with the olfactory bulb. However, it is not known if the new connections alter odor quality perception. To address this question, 20 adult hamsters were first trained to discriminate between cinnamon and strawberry odors. After reaching criterion (> or = 90% correct response), half of the animals received a bilateral nerve transection (BTX) and half a surgical sham procedure. Animals were not tested again until day 40, a point in recovery when connections are re-established with the bulb. When BTX animals were tested without food reinforcement, they could not perform the odor discrimination task. Sham animals, however, could discriminate, demonstrating that the behavioral response had not been extinguished during the 40 day period. When reinforcement was resumed, BTX animals were able to discriminate between cinnamon and strawberry after four test sessions. In addition, their ability to discriminate between these two familiar odors was no different than that of BTX and sham animals tested with two novel odors, baby powder and coffee. These findings suggest that, after recovery from nerve transection, there are alterations in sensory perception and that restoration of odor quality discrimination requires that the animal must again learn to associate individual odor sensations with a behavioral response.      

High-content behavioral analysis of Caenorhabditis elegans in precise spatiotemporal chemical environments

To quantitatively understand chemosensory behaviors, it is desirable to present many animals with repeatable, well-defined chemical stimuli. To that end, we describe a microfluidic system to analyze Caenorhabditis elegans behavior in defined temporal and spatial stimulus patterns. A 2 cm × 2 cm structured arena allowed C. elegans to perform crawling locomotion in a controlled liquid environment. We characterized behavioral responses to attractive odors with three stimulus patterns: temporal pulses, spatial stripes and a linear concentration gradient, all delivered in the fluid phase to eliminate variability associated with air-fluid transitions. Different stimulus configurations preferentially revealed turning dynamics in a biased random walk, directed orientation into an odor stripe and speed regulation by odor. We identified both expected and unexpected responses in wild-type worms and sensory mutants by quantifying dozens of behavioral parameters. The devices are inexpensive, easy to fabricate, reusable and suitable for delivering any liquid-borne stimulus.     

Profound context-dependent plasticity of mitral cell responses in olfactory bulb

On the basis of its primary circuit it has been postulated that the olfactory bulb (OB) is analogous to the retina in mammals. In retina, repeated exposure to the same visual stimulus results in a neural representation that remains relatively stable over time, even as the meaning of that stimulus to the animal changes. Stability of stimulus representation at early stages of processing allows for unbiased interpretation of incoming stimuli by higher order cortical centers. The alternative is that early stimulus representation is shaped by previously derived meaning, which could allow more efficient sampling of odor space providing a simplified yet biased interpretation of incoming stimuli. This study helps place the olfactory system on this continuum of subjective versus objective early sensory representation. Here we show that odor responses of the output cells of the OB, mitral cells, change transiently during a go–no-go odor discrimination task. The response changes occur in a manner that increases the ability of the circuit to convey information necessary to discriminate among closely related odors. Remarkably, a switch between which of the two odors is rewarded causes mitral cells to switch the polarity of their divergent responses. Taken together these results redefine the function of the OB as a transiently modifiable (active) filter, shaping early odor representations in behaviorally meaningful ways.     

Complex mixture discrimination and the role of contaminants

Rats were trained in a 2-alternative odor choice task to discriminate between a 10-component odor mixture and the same mixture with one component removed and replaced with 1 of 3 concentrations of a different monomolecular odor (contaminant). All stimuli were presented within a training session, thus the rat essentially had to learn to discriminate the 10-component mixture from "not" the 10-component mixture. Rats performed most poorly discriminating the complete mixture from the mixture with one component removed and no contaminant added. As the concentration of the contaminant increased from 10 ppm to a concentration equal to the other components (100 ppm), discrimination improved linearly. In analyses of individual differences, rats that spent more time in the sampling port (sampling and making a decision) were more accurate than rats that spent less time. Together, these results emphasize the balance between perceptual stability and perceptual discrimination expressed by the olfactory system dealing with dynamic mixtures and the robust effects of contamination on those processes. In addition, they provide further support that modification of sampling/decision time is a strategy used by rats to deal with difficult discriminations of complex odors.     

Odor Detection in Manduca sexta Is Optimized when Odor Stimuli Are Pulsed at a Frequency Matching the Wing Beat during Flight

Sensory systems sample the external world actively, within the context of self-motion induced disturbances. Mammals sample olfactory cues within the context of respiratory cycles and have adapted to process olfactory information within the time frame of a single sniff cycle. In plume tracking insects, it remains unknown whether olfactory processing is adapted to wing beating, which causes similar physical effects as sniffing. To explore this we first characterized the physical properties of our odor delivery system using hotwire anemometry and photo ionization detection, which confirmed that odor stimuli were temporally structured. Electroantennograms confirmed that pulse trains were tracked physiologically. Next, we quantified odor detection in moths in a series of psychophysical experiments to determine whether pulsing odor affected acuity. Moths were first conditioned to respond to a target odorant using Pavlovian olfactory conditioning. At 24 and 48 h after conditioning, moths were tested with a dilution series of the conditioned odor. On separate days odor was presented either continuously or as 20 Hz pulse trains to simulate wing beating effects. We varied pulse train duty cycle, olfactometer outflow velocity, pulsing method, and odor. Results of these studies, established that detection was enhanced when odors were pulsed. Higher velocity and briefer pulses also enhanced detection. Post hoc analysis indicated enhanced detection was the result of a significantly lower behavioral response to blank stimuli when presented as pulse trains. Since blank responses are a measure of false positive responses, this suggests that the olfactory system makes fewer errors (i.e. is more reliable) when odors are experienced as pulse trains. We therefore postulate that the olfactory system of Manduca sexta may have evolved mechanisms to enhance odor detection during flight, where the effects of wing beating represent the norm. This system may even exploit temporal structure in a manner similar to sniffing.     

Experience-dependent adult cortical plasticity requires cognitive association between sensation and reward

We tested the involvement of cognition in adult experience-dependent neuroplasticity using primate cortical implants. In a prior study, learning an operant sensory discrimination increased cortical excitability and target selectivity. Here, the prior task was separated into three behavioral phases. First, naive animals were exposed to stimulus-reward pairings from the prior study. These yoked animals did not have to discriminate to be rewarded and did not learn the discrimination. The plasticity observed in the prior study did not occur. Second, the animals were classically conditioned to discriminate the same stimuli in a simplified format. Learning was accompanied by increased sensory response strength and an increased range of sensory inputs eliciting responses. The third study recreated the original operant discrimination, and selectivity for task targets increased. These studies demonstrate that cognitive association between sensory stimuli and reinforcers accompanies adult experience-dependent cortical plasticity and suggest that selectivity in representation and action are linked.     

Translation of sensory input into behavioral output via an olfactory system

We investigate the logic by which sensory input is translated into behavioral output. First we provide a functional analysis of the entire odor receptor repertoire of an olfactory system. We construct tuning curves for the 21 functional odor receptors of the Drosophila larva and show that they sharpen at lower odor doses. We construct a 21-dimensional odor space from the responses of the receptors and find that the distance between two odors correlates with the extent to which one odor masks the other. Mutational analysis shows that different receptors mediate the responses to different concentrations of an odorant. The summed response of the entire receptor repertoire correlates with the strength of the behavioral response. The activity of a small number of receptors is a surprisingly powerful predictor of behavior. Odors that inhibit more receptors are more likely to be repellents. Odor space is largely conserved between two dissimilar olfactory systems.     

Divergence of odorant signals within and between the two European subspecies of the house mouse

The olfactory acuity of mice allows them to discriminate odorsof conspecifics differing by a few genes. This acuity is usedin habituation procedures where investigation of novel odorsby the mouse can be translated into relative difference or similaritybetween the stimuli. This study adapts these behavioral proceduresto address suprapopulation divergence among urinary odors inthe house mouse. Specifically, we investigate geographical patternsof odor divergence within and between 2 subspecies of the housemouse, Mus musculus musculus and Mus musculus domesticus, whichdiverged in allopatry and met secondarily in Europe where theyhybridize. Based on M. m. musculus perception, our study suggeststhat odors of the 2 subspecies differ in both allopatric andcontact zone populations and that divergence is more markedin the latter. Our earlier studies documented mate preferenceand signal divergence between the 2 subspecies. Hence, we considerthe role of the urinary odors as mating signals. We discusshow signal divergence between the 2 subspecies may relate toreproductive character displacement. This study validates theuse of habituation procedures to reconstruct geographical patternsof odorant signal divergence, providing a strong methodologicalplatform to address reproductive character displacement affectingcryptic mating signals in mammals.     

Attractiveness of host volatiles combined with background visual cues to the tea leafhopper,Empoasca vitis

The tea green leafhopper, Empoasca vitis (Göthe) (Hemiptera: Cicadellidae), is a serious pest of tea plants. We examined the behavioral responses of E. vitis adults to odors from the shoots of three host plants in a Y‐tube olfactometer with background visual cues. The host plants were tea [Camellia sinensis (L.) Kuntze (Theaceae)], peach [Prunus persica (L.) Siebold & Zucc. (Rosaceae)], and grapevine [Vitis vinifera L. (Vitaceae)]. Volatiles from the shoots were analyzed. Both yellow‐green and gold backgrounds enhanced the olfactory responses of E. vitis adults to tea plant odors, and this enhancement was stronger under a high light intensity. On the yellow‐green background, E. vitis adults significantly preferred the odors from shoots of the three host plants compared with clean air. Moreover, E. vitis adults preferred grapevine odor over the tea plant odor. The volatile blends of the three plant species were distinctly different. Peach plant shoots emitted the greatest amount of volatiles, whereas grapevine shoots released the greatest diversity of compounds. These results provide evidence that background visual cues could enhance the response of E. vitis adults to host‐plant volatiles. The leafhoppers can discern different host odors, suggesting the possibility of using peach plant and grapevine odors to monitor and manage this pest in tea plantations.     

Effects of olfactory stimuli on arm-reaching duration

The aim of the present study was to investigate the effects of olfactory stimuli on visually guided reaching. In Experiment 1, participants reached toward and grasped either a small (almond/strawberry) or a large (apple/orange) visual target. Any 1 of 4 odors corresponding to the visual stimuli or odorless air was administered before movement initiation. Within the same block of trials, participants smelled 1) an odor associated with an object of a different size than the target, 2) an odor associated with an object of a size equal to that of the target, or 3) odorless air. Results indicated that reaching duration was longer for trials in which the odor "size" and the visual target did not match than when they matched. In Experiment 2, the same procedures were applied but the "no-odor" trials were administered in a separate block to the "odor" trials. Similar results as for Experiment 1 were found. However, in contrast to Experiment 1, the presence of an odor increased the level of alertness resulting in a shortening of reaching duration. We contend that olfactory stimuli have the capacity to elicit motor plans interfering with those programmed for a movement toward a visual stimulus.     

Olfactory Coding in Antennal Neurons of the Malaria Mosquito, Anopheles gambiae

Olfactory receptor neurons (ORNs) in the antenna of insects serve to encode odors in action potential activity conducted to the olfactory lobe of the deuterocerebrum. We performed an analysis of the electrophysiological responses of olfactory neurons in the antennae of the female malaria mosquito Anopheles gambiae s.s. and investigated the effect of blood feeding on responsiveness. Forty-four chemicals that are known to be present in human volatile emanations were used as odor stimuli. We identified 6 functional types of trichoid sensilla and 5 functional types of grooved-peg sensilla (GP) based on a hierarchical cluster analysis. Generalist ORNs, tuned to a broad range of odors, moderate specialist ORNs and 2 ORNs tuned to only one odor were identified in different sensilla types. Neurons in GP were tuned to more polar compounds including the important behavioral attractant ammonia and its synergist L-lactic acid, responses to which were found only in GP. Combinatorial coding is the most plausible principle operating in the olfactory system of this mosquito species. We document for the first time both up- and downregulation of ORN responsiveness after blood feeding. Modulation of host-seeking and oviposition behavior is associated with both qualitative and quantitative changes in the peripheral sensory system.     

Affected by smells? Environmental chemical responsivity predicts odor perception

Strong negative reactions, physical symptoms, and behavioral disruptions due to environmental odors are common in the adult population. We investigated relationships among such environmental chemosensory responsivity (CR), personality traits, affective states, and odor perception. Study 1 showed that CR and neuroticism were positively correlated in a sample of young adults (n = 101), suggesting that persons high in neuroticism respond more negatively to environmental odors. Study 2 explored the relationships among CR, noise responsivity (NR), neuroticism, and odor perception (i.e., pleasantness and intensity) in a subset of participants (n = 40). High CR was associated with high NR. Regression analyses indicated that high CR predicted higher odor intensity ratings and low olfactory threshold (high sensitivity) predicted lower pleasantness ratings. However, neuroticism was not directly associated with odor ratings or thresholds. Overall, the results suggest that CR and odor thresholds predict perceptual ratings of odors and that high CR is associated with nonchemosensory affective traits.     

Temporal integration of olfactory perceptual evidence in human orbitofrontal cortex

Given a noisy sensory world, the nervous system integrates perceptual evidence over time to optimize decision-making. Neurophysiological accumulation of sensory information is well-documented in the animal visual system, but how such mechanisms are instantiated in the human brain remains poorly understood. Here we combined psychophysical techniques, drift-diffusion modeling, and functional magnetic resonance imaging (fMRI) to establish that odor evidence integration in the human olfactory system enhances discrimination on a two-alternative forced-choice task. Model-based measures of fMRI brain activity highlighted a ramp-like increase in orbitofrontal cortex (OFC) that peaked at the time of decision, conforming to predictions derived from an integrator model. Combined behavioral and fMRI data further suggest that decision bounds are not fixed but collapse over time, facilitating choice behavior in the presence of low-quality evidence. These data highlight a key role for the orbitofrontal cortex in resolving sensory uncertainty and provide substantiation for accumulator models of human perceptual decision-making.     

The signal function of thematically (In)congruent ambient scents in a retail environment

An odor emitted by an object signals the presence of that object and may draw attention to it. Can odors that are not actually emitted by an object also function as a signal? We investigated whether the degree of thematic congruency between an ambient odor and a magazine affected magazine sales in a retail store. We selected two odors: a grass odor, congruent with soccer, animal/nature and gardening magazines; and a sunflower odor, congruent with personal care and women's magazines. In a field study in three bookstores, the ambient odors did not increase sales for thematically congruent magazines, nor did they decrease sales for incongruent magazines. Several explanations for these unexpected findings are discussed.