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1.  Expanding the olfactory code by in silico decoding of odor-receptor chemical space 
eLife  2013;2:e01120.
Coding of information in the peripheral olfactory system depends on two fundamental factors: interaction of individual odors with subsets of the odorant receptor repertoire and mode of signaling that an individual receptor-odor interaction elicits, activation or inhibition. We develop a cheminformatics pipeline that predicts receptor–odorant interactions from a large collection of chemical structures (>240,000) for receptors that have been tested to a smaller panel of odorants (∼100). Using a computational approach, we first identify shared structural features from known ligands of individual receptors. We then use these features to screen in silico new candidate ligands from >240,000 potential volatiles for several Odorant receptors (Ors) in the Drosophila antenna. Functional experiments from 9 Ors support a high success rate (∼71%) for the screen, resulting in identification of numerous new activators and inhibitors. Such computational prediction of receptor–odor interactions has the potential to enable systems level analysis of olfactory receptor repertoires in organisms.
eLife digest
Although our sense of smell is regarded as inferior to that of many other species, we can nevertheless distinguish between roughly 10,000 different odors. These are made up of molecules called odorants, each of which activates a specific subset of odorant receptors in the nose. However, much of what we know about this process has come from studying the fruit fly, Drosophila, which detects odors using receptors located mainly on its antennae.
The number of potential odorants in nature is vast, and only a tiny fraction of the interactions between odorants and receptors can be physically tested. To address this challenge, Boyle et al. have used a computational approach to study in depth the interactions between a subset of 24 odorant receptors in Drosophila antennae and 109 odorants.
After developing a method to identify structural features shared by the odorants that activate each receptor, Boyle et al. used this information to perform a computational (in silico) screen of more than 240,000 different odorant-like volatile compounds. For each receptor, they compiled a list of the 500 odorants predicted to interact most strongly with it. They then tested their predictions for a subset of the receptors by performing experiments in living flies, and found that roughly 71% of predicted compounds did indeed activate or inhibit their receptors, compared to only 10% of a control sample.
In addition to providing new insights into the nature of the interactions between odorants and their receptors, the computational screen devised by Boyle et al. could aid the development of novel insect repellents, or compounds that mask the odors used by disease-causing insects to identify their hosts. It could also be used in the future to develop novel flavors and fragrances.
PMCID: PMC3787389  PMID: 24137542
odorant receptors; antenna; electrophysiology; cheminformatics; D. melanogaster
2.  A Large-Scale Analysis of Odor Coding in the Olfactory Epithelium 
The Journal of Neuroscience  2011;31(25):9179-9191.
Mammals can perceive and discriminate myriad volatile chemicals as having a distinct odor. Odorants are initially detected by odorant receptors (ORs) on olfactory sensory neurons (OSNs) in the nose. In the mouse, each OSN expresses one of ∼1000 different OR genes. Although OSNs and their expressed ORs constitute the fundamental units of sensory input to the brain, a comprehensive understanding of how they encode odor identities is still lacking. To gain a broader and more detailed understanding of odorant recognition and odor coding at this level, we tested the responses of 3000 mouse OSNs to 125 odorants with diverse structures and perceived odors. These studies revealed extraordinary diversity, but also bias, in odorant recognition by the OSN, and thus OR, repertoire. They indicate that most OSNs are narrowly tuned to detect a subset of odorants with related structures and often related odors, but that the repertoire also includes broadly tuned components. Strikingly, the vast majority of odorants activated a unique set of OSNs, usually two or more in combination. The resulting combinatorial codes varied in size among odorants and sometimes contained both narrowly and broadly tuned components. While many OSNs recognized multiple odorants, some appeared specific for a given pheromone or other animal-associated compound, or for one or more odorants with a particular odor quality, raising the possibility that signals derived from some OSNs and ORs might elicit an innate behavior or convey a specific odor quality.
PMCID: PMC3758579  PMID: 21697369
3.  A circuit supporting concentration-invariant odor perception in Drosophila 
Journal of Biology  2009;8(1):9.
Most odors are perceived to have the same quality over a large concentration range, but the neural mechanisms that permit concentration-invariant olfactory perception are unknown. In larvae of the vinegar fly Drosophila melanogaster, odors are sensed by an array of 25 odorant receptors expressed in 21 olfactory sensory neurons (OSNs). We investigated how subsets of larval OSNs with overlapping but distinct response properties cooperate to mediate perception of a given odorant across a range of concentrations.
Using calcium imaging, we found that ethyl butyrate, an ester perceived by humans as fruity, activated three OSNs with response thresholds that varied across three orders of magnitude. Whereas wild-type larvae were strongly attracted by this odor across a 500-fold range of concentration, individuals with only a single functional OSN showed attraction across a narrower concentration range corresponding to the sensitivity of each ethyl butyrate-tuned OSN. To clarify how the information carried by different OSNs is integrated by the olfactory system, we characterized the response properties of local inhibitory interneurons and projection neurons in the antennal lobe. Local interneurons only responded to high ethyl butyrate concentrations upon summed activation of at least two OSNs. Projection neurons showed a reduced response to odors when summed input from two OSNs impinged on the circuit compared to when there was only a single functional OSN.
Our results show that increasing odor concentrations induce progressive activation of concentration-tuned olfactory sensory neurons and concomitant recruitment of inhibitory local interneurons. We propose that the interplay of combinatorial OSN input and local interneuron activation allows animals to remain sensitive to odors across a large range of stimulus intensities.
PMCID: PMC2656214  PMID: 19171076
4.  Rapid Encoding and Perception of Novel Odors in the Rat 
PLoS Biology  2008;6(4):e82.
To gain insight into which parameters of neural activity are important in shaping the perception of odors, we combined a behavioral measure of odor perception with optical imaging of odor representations at the level of receptor neuron input to the rat olfactory bulb. Instead of the typical test of an animal's ability to discriminate two familiar odorants by exhibiting an operant response, we used a spontaneously expressed response to a novel odorant—exploratory sniffing—as a measure of odor perception. This assay allowed us to measure the speed with which rats perform spontaneous odor discriminations. With this paradigm, rats discriminated and began responding to a novel odorant in as little as 140 ms. This time is comparable to that measured in earlier studies using operant behavioral readouts after extensive training. In a subset of these trials, we simultaneously imaged receptor neuron input to the dorsal olfactory bulb with near-millisecond temporal resolution as the animal sampled and then responded to the novel odorant. The imaging data revealed that the bulk of the discrimination time can be attributed to the peripheral events underlying odorant detection: receptor input arrives at the olfactory bulb 100–150 ms after inhalation begins, leaving only 50–100 ms for central processing and response initiation. In most trials, odor discrimination had occurred even before the initial barrage of receptor neuron firing had ceased and before spatial maps of activity across glomeruli had fully developed. These results suggest a coding strategy in which the earliest-activated glomeruli play a major role in the initial perception of odor quality, and place constraints on coding and processing schemes based on simple changes in spike rate.
Author Summary
Olfactory stimuli elicit temporally complex patterns of activity across groups of receptor neurons as well as across central neurons. It remains unclear which parameters among these complex activity patterns are important in shaping odor perception. To address this issue, we imaged from the olfactory bulb of awake rats as they detected and responded to odorants. We used a spontaneously expressed response to novel odorants—exploratory sniffing—as a behavioral measure of odor perception. This assay allowed us to measure the speed with which rats perform simple odor discriminations by monitoring changes in respiration. Rats discriminated a novel odorant from a learned one in as little as 140 ms. Simultaneously imaging the sensory input to the olfactory bulb carried by receptor neurons revealed that the bulk of the response time is due to the peripheral events underlying odorant detection (inhalation and receptor neuron activation), leaving only 50–100 ms for central processing and response initiation. In most trials, responses to a novel odorant began before the initial barrage of input had ceased and before spatial patterns of input to the bulb had fully developed. These results suggest a coding strategy in which the earliest inputs play a major role in the initial perception of odor quality and place constraints on coding schemes based on simple changes in firing rate.
Imaging the olfactory bulb of awake rats reveals that odor discrimination occurs about 100 ms after sensory input reaches the brain, sharply limiting the role that spike rate and temporal integration can play in coding odor identity.
PMCID: PMC2288628  PMID: 18399719
5.  System identification of Drosophila olfactory sensory neurons 
The lack of a deeper understanding of how olfactory sensory neurons (OSNs) encode odors has hindered the progress in understanding the olfactory signal processing in higher brain centers. Here we employ methods of system identification to investigate the encoding of time-varying odor stimuli and their representation for further processing in the spike domain by Drosophila OSNs. In order to apply system identification techniques, we built a novel low-turbulence odor delivery system that allowed us to deliver airborne stimuli in a precise and reproducible fashion. The system provides a 1% tolerance in stimulus reproducibility and an exact control of odor concentration and concentration gradient on a millisecond time scale. Using this novel setup, we recorded and analyzed the in-vivo response of OSNs to a wide range of time-varying odor waveforms. We report for the first time that across trials the response of OR59b OSNs is very precise and reproducible. Further, we empirically show that the response of an OSN depends not only on the concentration, but also on the rate of change of the odor concentration. Moreover, we demonstrate that a two-dimensional (2D) Encoding Manifold in a concentration-concentration gradient space provides a quantitative description of the neuron’s response. We then use the white noise system identification methodology to construct one-dimensional (1D) and two-dimensional (2D) Linear-Nonlinear-Poisson (LNP) cascade models of the sensory neuron for a fixed mean odor concentration and fixed contrast. We show that in terms of predicting the intensity rate of the spike train, the 2D LNP model performs on par with the 1D LNP model, with a root mean-square error (RMSE) increase of about 5 to 10%. Surprisingly, we find that for a fixed contrast of the white noise odor waveforms, the nonlinear block of each of the two models changes with the mean input concentration. The shape of the nonlinearities of both the 1D and the 2D LNP model appears to be, for a fixed mean of the odor waveform, independent of the stimulus contrast. This suggests that white noise system identification of Or59b OSNs only depends on the first moment of the odor concentration. Finally, by comparing the 2D Encoding Manifold and the 2D LNP model, we demonstrate that the OSN identification results depend on the particular type of the employed test odor waveforms. This suggests an adaptive neural encoding model for Or59b OSNs that changes its nonlinearity in response to the odor concentration waveforms.
PMCID: PMC3736744  PMID: 20730480
System identification; Olfactory sensory neurons; White noise analysis; I/O modeling
6.  Modeling Peripheral Olfactory Coding in Drosophila Larvae 
PLoS ONE  2011;6(8):e22996.
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.
PMCID: PMC3153476  PMID: 21857978
7.  Friends and Foes from an Ant Brain's Point of View – Neuronal Correlates of Colony Odors in a Social Insect 
PLoS ONE  2011;6(6):e21383.
Successful cooperation depends on reliable identification of friends and foes. Social insects discriminate colony members (nestmates/friends) from foreign workers (non-nestmates/foes) by colony-specific, multi-component colony odors. Traditionally, complex processing in the brain has been regarded as crucial for colony recognition. Odor information is represented as spatial patterns of activity and processed in the primary olfactory neuropile, the antennal lobe (AL) of insects, which is analogous to the vertebrate olfactory bulb. Correlative evidence indicates that the spatial activity patterns reflect odor-quality, i.e., how an odor is perceived. For colony odors, alternatively, a sensory filter in the peripheral nervous system was suggested, causing specific anosmia to nestmate colony odors. Here, we investigate neuronal correlates of colony odors in the brain of a social insect to directly test whether they are anosmic to nestmate colony odors and whether spatial activity patterns in the AL can predict how odor qualities like “friend” and “foe” are attributed to colony odors.
Methodology/Principal Findings
Using ant dummies that mimic natural conditions, we presented colony odors and investigated their neuronal representation in the ant Camponotus floridanus. Nestmate and non-nestmate colony odors elicited neuronal activity: In the periphery, we recorded sensory responses of olfactory receptor neurons (electroantennography), and in the brain, we measured colony odor specific spatial activity patterns in the AL (calcium imaging). Surprisingly, upon repeated stimulation with the same colony odor, spatial activity patterns were variable, and as variable as activity patterns elicited by different colony odors.
Ants are not anosmic to nestmate colony odors. However, spatial activity patterns in the AL alone do not provide sufficient information for colony odor discrimination and this finding challenges the current notion of how odor quality is coded. Our result illustrates the enormous challenge for the nervous system to classify multi-component odors and indicates that other neuronal parameters, e.g., precise timing of neuronal activity, are likely necessary for attribution of odor quality to multi-component odors.
PMCID: PMC3121771  PMID: 21731724
8.  Complex and non-redundant signals from individual odor receptors that underlie chemotaxis behavior in Drosophila melanogaster larvae 
Biology Open  2014;3(10):947-957.
The rules by which odor receptors encode odors and allow behavior are still largely unexplored. Although large data sets of electrophysiological responses of receptors to odors have been generated, few hypotheses have been tested with behavioral assays. We use a data set on odor responses of Drosophila larval odor receptors coupled with chemotaxis behavioral assays to examine rules of odor coding. Using mutants of odor receptors, we have found that odor receptors with similar electrophysiological responses to odors across concentrations play non-redundant roles in odor coding at specific odor concentrations. We have also found that high affinity receptors for odors determine behavioral response thresholds, but the rules for determining peak behavioral responses are more complex. While receptor mutants typically show loss of attraction to odors, some receptor mutants result in increased attraction at specific odor concentrations. The odor receptor mutants were rescued using transgenic expression of odor receptors, validating assignment of phenotypes to the alleles. Vapor pressures alone cannot fully explain behavior in our assay. Finally, some odors that did not elicit strong electrophysiological responses are associated with behavioral phenotypes upon examination of odor receptor mutants. This result is consistent with the role of sensory neurons in lateral inhibition via local interneurons in the antennal lobe. Taken together, our results suggest a complexity of odor coding rules even in a simple olfactory sensory system.
PMCID: PMC4197443  PMID: 25238759
Odor receptors; Olfaction; Drosophila; Or42a; Or42b
9.  A Regulatory Code for Neuron-Specific Odor Receptor Expression 
PLoS Biology  2008;6(5):e125.
Olfactory receptor neurons (ORNs) must select—from a large repertoire—which odor receptors to express. In Drosophila, most ORNs express one of 60 Or genes, and most Or genes are expressed in a single ORN class in a process that produces a stereotyped receptor-to-neuron map. The construction of this map poses a problem of receptor gene regulation that is remarkable in its dimension and about which little is known. By using a phylogenetic approach and the genome sequences of 12 Drosophila species, we systematically identified regulatory elements that are evolutionarily conserved and specific for individual Or genes of the maxillary palp. Genetic analysis of these elements supports a model in which each receptor gene contains a zip code, consisting of elements that act positively to promote expression in a subset of ORN classes, and elements that restrict expression to a single ORN class. We identified a transcription factor, Scalloped, that mediates repression. Some elements are used in other chemosensory organs, and some are conserved upstream of axon-guidance genes. Surprisingly, the odor response spectra and organization of maxillary palp ORNs have been extremely well-conserved for tens of millions of years, even though the amino acid sequences of the receptors are not highly conserved. These results, taken together, define the logic by which individual ORNs in the maxillary palp select which odor receptors to express.
Author Summary
Odors are detected by olfactory receptor neurons (ORNs). Which odor an individual neuron detects is dictated by the odor receptors it expresses. Odor receptors are encoded by large families of genes, and an individual neuron must thus select the gene it expresses from among many possibilities. The mechanism underlying this choice is largely unknown. We have examined the problem of receptor gene choice in the fruit fly Drosophila, whose maxillary palp contains six functional classes of ORNs, each expressing different odor receptor genes. By comparing the DNA sequences flanking these genes in 12 different species of Drosophila, we have identified regulatory elements that are evolutionarily conserved and specific to each odor receptor. Genetic analysis of these elements showed that some act positively to dictate expression in a subset of ORNs, while others act negatively to restrict the expression of a receptor gene to a particular ORN class. We identified a transcription factor, Scalloped, that mediates repression. We were surprised to find that the odor response spectra of these neurons have been well-conserved for tens of millions of years, even though the amino acid sequences of their receptors have diverged considerably.
How does an olfactory receptor neuron select which odor receptor to express? A computational analysis of 12Drosophila genomes combined with mutational analysis identifies conservedcis elements and defines a regulatory code.
PMCID: PMC2430909  PMID: 18846726
10.  Long term functional plasticity of sensory inputs mediated by olfactory learning 
eLife  2014;3:e02109.
Sensory inputs are remarkably organized along all sensory pathways. While sensory representations are known to undergo plasticity at the higher levels of sensory pathways following peripheral lesions or sensory experience, less is known about the functional plasticity of peripheral inputs induced by learning. We addressed this question in the adult mouse olfactory system by combining odor discrimination studies with functional imaging of sensory input activity in awake mice. Here we show that associative learning, but not passive odor exposure, potentiates the strength of sensory inputs up to several weeks after the end of training. We conclude that experience-dependent plasticity can occur in the periphery of adult mouse olfactory system, which should improve odor detection and contribute towards accurate and fast odor discriminations.
eLife digest
The mammalian brain is not static, but instead retains a significant degree of plasticity throughout an animal’s life. It is this plasticity that enables adults to learn new things, adjust to new environments and, to some degree, regain functions they have lost as a result of brain damage.
However, information about the environment must first be detected and encoded by the senses. Odors, for example, activate specific receptors in the nose, and these in turn project to structures called glomeruli in a region of the brain known as the olfactory bulb. Each odor activates a unique combination of glomeruli, and the information contained within this ‘odor fingerprint’ is relayed via olfactory bulb neurons to the olfactory cortex.
Now, Abraham et al. have revealed that the earliest stages of odor processing also show plasticity in adult animals. Two groups of mice were exposed to the same two odors: however, the first group was trained to discriminate between the odors to obtain a reward, whereas the second group was passively exposed to them. When both groups of mice were subsequently re-exposed to the odors, the trained group activated more glomeruli, more strongly, than a control group that had never encountered the odors before. By contrast, the responses of mice in the passively exposed group did not differ from those of a control group.
Given that the response of glomeruli correlates with the ability of mice to discriminate between odors, these results suggest that trained animals would now be able to discriminate between the odors more easily than other mice. In other words, sensory plasticity ensures that stimuli that have been associatively learned with or without reward will be easier to detect should they be encountered again in the future.
PMCID: PMC3953949  PMID: 24642413
sensory perception; imaging; behavior; mouse
11.  Olfactory Bulb Mitral–Tufted Cell Plasticity: Odorant-Specific Tuning Reflects Previous Odorant Exposure 
Olfactory system second-order neurons, mitral–tufted cells, have odorant receptive fields (ORFs) (molecular receptive ranges in odorant space for carbon chain length in organic odorant molecules). This study quantified several dimensions of these excitatory odorant receptive fields to novel odorants in rats and then examined the effects of passive odorant exposure on the shape of the ORF-tuning curve. ORFs for carbon chain length of novel ethyl esters (pure odorants that the animals had not been exposed to previously) were determined before and after a 50 sec prolonged exposure to one of the odorants. In response to novel odorants, quantitative analysis of mitral–tufted cell excitatory ORFs revealed that the median ORF width spanned 3–4 carbons, generally with a single-most excitatory odorant. Exposure to either the most excitatory odorant (ON-PEAK) or an odorant that was two carbons longer (OFF-PEAK) for 50 sec produced whole ORF suppression immediately after the end of the prolonged exposure, with the ON-PEAK exposure producing the greatest suppression. These results are consistent with a feature-detecting function for mitral–tufted cells. Redetermination of the ORF 15 and 60 min after the exposure revealed that OFF-PEAK exposure produced a reduction in responsiveness to the best odorant and an increase in responsiveness to the exposed odorant. In contrast, exposure to the ON-PEAK odorant or no odorant did not affect ORFs. Given that mitral–tufted cells receive exclusive excitatory input from olfactory receptor neurons expressing identical receptor proteins, it is hypothesized that experience-induced mitral–tufted cell ORF changes reflect modulation of lateral and centrifugal olfactory bulb circuits.
PMCID: PMC2367229  PMID: 12890789
perceptual learning; olfactory memory; receptive field; odor coding; dynamic processing; mitral cell; habituation; adaptation; odorant receptive fields
12.  Profound Context-Dependent Plasticity of Mitral Cell Responses in Olfactory Bulb  
PLoS Biology  2008;6(10):e258.
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.
Author Summary
The way in which the brain represents and processes sensory information remains a fundamental question. One model posits that stable neural representation of a stimulus during early stages of stimulus processing allows for unbiased interpretation of incoming stimuli by higher order cortical centers. Alternately, early stimulus representation could be shaped by previous experience, thus providing a biased yet relevant interpretation of incoming stimuli. This study examines the activity of output cells, mitral cells, from the first stage of odor information processing in the olfactory bulb during an odor discrimination task. We found that odor responses changed during the task in a manner that increased the ability of the circuit to convey information necessary to discriminate among closely related odors. A switch between which of the two odors were rewarded caused mitral cells to switch the polarity of their divergent responses in behaviorally relevant ways. These results show that early neural representations of odor can be shaped by previously derived meaning, providing a simplified yet biased interpretation of the odor environment to higher cortical structures.
Early neural representation of odor can be shaped by previously derived meaning, providing a simplified yet biased interpretation of the odor environment to higher cortical structures.
PMCID: PMC2573932  PMID: 18959481
13.  Odor identity influences tracking of temporally patterned plumes in Drosophila 
BMC Neuroscience  2011;12:62.
Turbulent fluid landscapes impose temporal patterning upon chemical signals, and the dynamical neuronal responses to patterned input vary across the olfactory receptor repertoire in flies, moths, and locusts. Sensory transformations exhibit low pass filtering that ultimately results in perceptual fusion of temporally transient sensory signals. For example, humans perceive a sufficiently fast flickering light as continuous, but the frequency threshold at which this fusion occurs varies with wavelength. Although the summed frequency sensitivity of the fly antenna has been examined to a considerable extent, it is unknown how intermittent odor signals are integrated to influence plume tracking behavior independent of wind cues, and whether temporal fusion for behavioral tracking might vary according to the odor encountered.
Here we have adopted a virtual reality flight simulator to study the dynamics of plume tracking under different experimental conditions. Flies tethered in a magnetic field actively track continuous (non-intermittent) plumes of vinegar, banana, or ethyl butyrate with equal precision. However, pulsing these plumes at varying frequency reveals that the threshold rate, above which flies track the plume as if it were continuous, is unique for each odorant tested. Thus, the capability of a fly to navigate an intermittent plume depends on the particular odorant being tracked during flight. Finally, we measured antennal field potential responses to an intermittent plume, found that receptor dynamics track the temporal pattern of the odor stimulus and therefore do not limit the observed behavioral temporal fusion limits.
This study explores the flies' ability to track odor plumes that are temporally intermittent. We were surprised to find that the perceptual critical fusion limit, determined behaviorally, is strongly dependent on odor identity. Antennal field potential recordings indicate that peripheral processing of temporal cues faithfully follow rapid odor transients above the rates that can be resolved behaviorally. These results indicate that (1) higher order circuits create a perceptually continuous signal from an intermittent sensory one, and that (2) this transformation varies with odorant rather than being constrained by sensory-motor integration, thus (3) offering an entry point for examining the mechanisms of rapid olfactory decision making in an ecological context.
PMCID: PMC3145592  PMID: 21708035
14.  Decoding odor quality and intensity in the Drosophila brain 
eLife  null;3:e04147.
To internally reflect the sensory environment, animals create neural maps encoding the external stimulus space. From that primary neural code relevant information has to be extracted for accurate navigation. We analyzed how different odor features such as hedonic valence and intensity are functionally integrated in the lateral horn (LH) of the vinegar fly, Drosophila melanogaster. We characterized an olfactory-processing pathway, comprised of inhibitory projection neurons (iPNs) that target the LH exclusively, at morphological, functional and behavioral levels. We demonstrate that iPNs are subdivided into two morphological groups encoding positive hedonic valence or intensity information and conveying these features into separate domains in the LH. Silencing iPNs severely diminished flies' attraction behavior. Moreover, functional imaging disclosed a LH region tuned to repulsive odors comprised exclusively of third-order neurons. We provide evidence for a feature-based map in the LH, and elucidate its role as the center for integrating behaviorally relevant olfactory information.
eLife digest
Organisms need to sense and adapt to their environment in order to survive. Senses such as vision and smell allow an organism to absorb information about the external environment and translate it into a meaningful internal image. This internal image helps the organism to remember incidents and act accordingly when they encounter similar situations again. A typical example is when organisms are repeatedly attracted to odors that are essential for survival, such as food and pheromones, and are repulsed by odors that threaten survival.
Strutz et al. addressed how attractiveness or repulsiveness of a smell, and also the strength of a smell, are processed by a part of the olfactory system called the lateral horn in fruit flies. This involved mapping the neuronal patterns that were generated in the lateral horn when a fly was exposed to particular odors.
Strutz et al. found that a subset of neurons called inhibitory projection neurons processes information about whether the odor is attractive or repulsive, and that a second subset of these neurons process information about the intensity of the odor. Other insects, such as honey bees and hawk moths, have olfactory systems with a similar architecture and might also employ a similar spatial approach to encode information regarding the intensity and identity of odors. Locusts, on the other hand, employ a temporal approach to encoding information about odors.
The work of Strutz et al. shows that certain qualities of odors are contained in a spatial map in a specific brain region of the fly. This opens up the question of how the information in this spatial map influences decisions made by the fly.
PMCID: PMC4270039  PMID: 25512254
olfaction; neural circuit; lateral horn; antennal lobe; odor processing; functional imaging; D. melanogaster
15.  Learned odor discrimination in Drosophila without distinct combinatorial odor maps in the antennal lobe 
Current biology : CB  2008;18(21):1668-1674.
A unifying feature of mammalian and insect olfactory systems is that olfactory sensory neurons (OSNs) expressing the same unique odorant receptor gene converge onto the same glomeruli in the brain (1–7). Most odorants activate a combination of receptors and thus distinct patterns of glomeruli, forming a proposed combinatorial spatial code that could support discrimination between a large number of odorants (8–11). OSNs also exhibit odor-evoked responses with complex temporal dynamics (11), but the contribution of this activity to behavioral odor discrimination has received little attention (12). Here we investigated the importance of spatial encoding in the relatively simple Drosophila antennal lobe. We show that Drosophila can learn to discriminate between two odorants with one functional class of Or83b-expressing OSNs. Furthermore, these flies encode one odorant from a mixture, and cross-adapt to odorants that activate the relevant OSN class, demonstrating that they discriminate odorants using the same OSNs. Lastly, flies with a single class of Or83b-expressing OSNs recognize a specific odorant across a range of concentration indicating that they encode odorant identity. Therefore flies can distinguish odorants without discrete spatial codes in the antennal lobe, implying an important role for odorant-evoked temporal dynamics in behavioral odorant discrimination.
PMCID: PMC2602956  PMID: 18951022
16.  Regulators of AWC-Mediated Olfactory Plasticity in Caenorhabditis elegans 
PLoS Genetics  2009;5(12):e1000761.
While most sensory neurons will adapt to prolonged stimulation by down-regulating their responsiveness to the signal, it is not clear which events initiate long-lasting sensory adaptation. Likewise, we are just beginning to understand how the physiology of the adapted cell is altered. Caenorhabditis elegans is inherently attracted to specific odors that are sensed by the paired AWC olfactory sensory neurons. The attraction diminishes if the animal experiences these odors for a prolonged period of time in the absence of food. The AWC neuron responds acutely to odor-exposure by closing calcium channels. While odortaxis requires a Gα subunit protein, cGMP-gated channels, and guanylyl cyclases, adaptation to prolonged odor exposure requires nuclear entry of the cGMP-dependent protein kinase, EGL-4. We asked which candidate members of the olfactory signal transduction pathway promote nuclear entry of EGL-4 and which molecules might induce long-term adaptation downstream of EGL-4 nuclear entry. We found that initiation of long-term adaptation, as assessed by nuclear entry of EGL-4, is dependent on G-protein mediated signaling but is independent of fluxes in calcium levels. We show that long-term adaptation requires polyunsaturated fatty acids (PUFAs) that may act on the transient receptor potential (TRP) channel type V OSM-9 downstream of EGL-4 nuclear entry. We also present evidence that high diacylglycerol (DAG) levels block long-term adaptation without affecting EGL-4 nuclear entry. Our analysis provides a model for the process of long-term adaptation that occurs within the AWC neuron of C. elegans: G-protein signaling initiates long-lasting olfactory adaptation by promoting the nuclear entry of EGL-4, and once EGL-4 has entered the nucleus, processes such as PUFA activation of the TRP channel OSM-9 may dampen the output of the AWC neuron.
Author Summary
Caenorhabditis elegans is capable of sensing a variety of attractive volatile compounds. These odors are the worm's “best guesses” as to how to track down food. Employing calculated approximations underlies a foraging strategy that is open to failure. When C. elegans track an odor which proves unrewarding, they must modify their behavior based on this experience. They also need to prevent over-stimulating their neurons. To accomplish this, C. elegans olfactory sensory neurons adapt to odors after a sustained exposure to odor in the absence of food. Within the pair of primary odor-sensory neurons, termed the AWCs, adaptation requires the cGMP-dependent protein kinase G (PKG), EGL-4. Exposing animals to AWC–sensed odors for approximately 60 minutes results in a long-lasting (∼3 hour) adaptation that requires the nuclear translocation of EGL-4. To understand how sensory transduction and desensitization machinery converge to achieve olfactory adaptation, we asked whether odor-induced EGL-4 nuclear accumulation was affected by gene mutations that abrogate either odor sensation of or adaptation to AWC–sensed odors. We find that G-protein signaling represents the integration point where primary odor sensation and odor adaptation pathways diverge. PUFA signaling, calcium, and decreased diacylglycerol all dampen the response of the AWC neuron to odor downstream of this divergence.
PMCID: PMC2780698  PMID: 20011101
17.  Similar Odorants Elicit Different Behavioral and Physiological Responses, Some Supersustained 
An intriguing question in the field of olfaction is how animals distinguish among structurally similar odorants. We systematically analyzed olfactory responses elicited by a panel of 25 pyrazines. We found that structurally similar pyrazines elicit a wide range of behavioral responses from Drosophila larvae. Each pyrazine was tested against all functional receptors of the larval Odor receptor (Or) repertoire, yielding 525 odorant–receptor combinations. Different pyrazines vary markedly in the responses they elicit from the Or repertoire, with most strong responses deriving from two receptors, Or33b and Or59a. Surprisingly, 2-ethylpyrazine and 2-methylpyrazine, which elicit strikingly similar physiological responses across the receptor repertoire, elicit dramatically different behavioral responses. A small fraction of odorant-receptor combinations elicit remarkably long responses. These responses, which we term “supersustained” responses, are receptor specific and odorant specific, and can last for minutes. Such supersustained responses may prevent olfactory neurons from reporting contemporaneous information about the local odor environment. Odors that elicit such responses could provide a novel means of controlling insect pests and vectors of human disease by impairing the location of human hosts, food sources, and mates.
PMCID: PMC3116233  PMID: 21613503
18.  Effect of sniffing on the temporal structure of mitral/tufted cell output from the olfactory bulb 
Neural activity underlying odor representations in the mammalian olfactory system is strongly patterned by respiratory behavior; these dynamics are central to many models of olfactory information processing. We have previously found that sensory inputs to the olfactory bulb change both their magnitude and temporal structure as a function of sniff frequency. Here, we asked how sniff frequency affects responses of mitral/tufted (MT) cells – the principal olfactory bulb output neuron. We recorded from MT cells in anesthetized rats while reproducing sniffs recorded previously from awake animals and varying sniff frequency. The dynamics of a sniff-evoked response were consistent from sniff to sniff but varied across cells. Compared to the dynamics of receptor neuron activation by the same sniffs, the MT response was shorter and faster, reflecting a temporal sharpening of sensory inputs. Increasing sniff frequency led to moderate attenuation of MT response magnitude and significant changes in the temporal structure of the sniff-evoked MT cell response. Most MT cells responded with a shorter duration and shorter rise-time spike burst as sniff frequency increased, reflecting increased temporal sharpening of inputs by the olfactory bulb. These temporal changes were necessary and sufficient to maintain respiratory modulation in the MT cell population across the range of sniff frequencies expressed during behavior. These results suggest that the input-output relationship in the olfactory bulb varies dynamically as a function of sniff frequency, and that one function of the postsynaptic network is to maintain robust temporal encoding of odor information across different odor sampling strategies.
PMCID: PMC3159407  PMID: 21775605
19.  The activity-dependent histone variant H2BE modulates the life span of olfactory neurons 
eLife  2012;1:e00070.
We have identified a replication-independent histone variant, Hist2h2be (referred to herein as H2be), which is expressed exclusively by olfactory chemosensory neurons. Levels of H2BE are heterogeneous among olfactory neurons, but stereotyped according to the identity of the co-expressed olfactory receptor (OR). Gain- and loss-of-function experiments demonstrate that changes in H2be expression affect olfactory function and OR representation in the adult olfactory epithelium. We show that H2BE expression is reduced by sensory activity and that it promotes neuronal cell death, such that inactive olfactory neurons display higher levels of the variant and shorter life spans. Post-translational modifications (PTMs) of H2BE differ from those of the canonical H2B, consistent with a role for H2BE in altering transcription. We propose a physiological function for H2be in modulating olfactory neuron population dynamics to adapt the OR repertoire to the environment.
eLife digest
A hallmark of the nervous systems of all mammals is their capacity to undergo changes in function that are shaped by experience. This phenomenon underlies the ability of our brains to develop properly and to learn, and also enables various sensory systems—including the visual, auditory and olfactory systems—to perform optimally in diverse environments.
In most mammals, a high-functioning olfactory system is essential for carrying out tasks that are crucial for survival, such as finding food, avoiding predators and mating. In general, sensory systems have to decipher only a limited collection of stimuli, but the olfactory system must be able to process information from thousands of distinct odors that are found in a given environment and which may vary dramatically from one environment to the next. Each odor-sensing neuron in the nose of a mammal contains just one kind of odorant receptor protein, although mammalian genomes typically encode 1000 or so different kinds of receptor proteins. This suggests that it might be possible to ‘tune’ the olfactory system to a particular environment by changing the relative numbers of the different types of neurons. Indeed, it is known that the relative abundance of each type of odor-sensing neuron changes with age and experience, and that these changes might be caused by variations in the lifespans of the neurons.
Although our understanding of how these experience-dependent changes are orchestrated at the molecular level is far from complete, it is clear that adjustments in the levels of specific gene products is necessary. But how do experiences alter the levels of gene products to give rise to lasting changes in the brain? One hypothesis is that changes to a structure called chromatin are key to this process: chromatin is an assembly of DNA molecules, which are quite long, and organizing proteins, mostly proteins known as histones, that together form a compact structure that can fit inside the nucleus of a cell.
Santoro and Dulac have now discovered a previously uncharacterized protein called H2BE that is found only in the odor-sensing neurons of mice. H2BE is a variant of a protein called H2B, which is a well-known histone. They found that in odor-sensing neurons, H2BE replaces H2B to an extent that depends on the amount of activity experienced by the neuron: H2BE is nearly undetectable in highly active neurons, but almost completely replaces H2B in neurons that are inactive. Moreover, genetic manipulation showed that the deletion of H2BE significantly extended the lifespan of neurons, whereas elevated levels of H2BE shortened their lifespan. These findings reveal an extraordinary process that involves inactive odor-sensing neurons being depleted relative to active ones over time.
How does H2BE, which differs from H2B by just five amino acids, cause such dramatic changes in neuronal composition? One hint comes from evidence that these amino acids disrupt interactions between chromatin and ‘effector’ proteins, which modulate gene activity. Consistent with this, Santoro and Dulac have found that the replacement of H2B by H2BE strongly alters gene activity, although the precise mechanism by which these alterations regulate neuronal lifespans remains to be determined. Understanding this process in detail, and exploring if similar phenomena are involved in experience-dependent changes elsewhere in the nervous system, are fascinating areas of future research.
PMCID: PMC3510456  PMID: 23240083
histone; olfactory; epigenetics; Mouse
20.  The neuronal architecture of the mushroom body provides a logic for associative learning 
eLife  null;3:e04577.
We identified the neurons comprising the Drosophila mushroom body (MB), an associative center in invertebrate brains, and provide a comprehensive map describing their potential connections. Each of the 21 MB output neuron (MBON) types elaborates segregated dendritic arbors along the parallel axons of ∼2000 Kenyon cells, forming 15 compartments that collectively tile the MB lobes. MBON axons project to five discrete neuropils outside of the MB and three MBON types form a feedforward network in the lobes. Each of the 20 dopaminergic neuron (DAN) types projects axons to one, or at most two, of the MBON compartments. Convergence of DAN axons on compartmentalized Kenyon cell–MBON synapses creates a highly ordered unit that can support learning to impose valence on sensory representations. The elucidation of the complement of neurons of the MB provides a comprehensive anatomical substrate from which one can infer a functional logic of associative olfactory learning and memory.
eLife digest
One of the key goals of neuroscience is to understand how specific circuits of brain cells enable animals to respond optimally to the constantly changing world around them. Such processes are more easily studied in simpler brains, and the fruit fly—with its small size, short life cycle, and well-developed genetic toolkit—is widely used to study the genes and circuits that underlie learning and behavior.
Fruit flies can learn to approach odors that have previously been paired with food, and also to avoid any odors that have been paired with an electric shock, and a part of the brain called the mushroom body has a central role in this process. When odorant molecules bind to receptors on the fly's antennae, they activate neurons in the antennal lobe of the brain, which in turn activate cells called Kenyon cells within the mushroom body. The Kenyon cells then activate output neurons that convey signals to other parts of the brain.
It is known that relatively few Kenyon cells are activated by any given odor. Moreover, it seems that a given odor activates different sets of Kenyon cells in different flies. Because the association between an odor and the Kenyon cells it activates is unique to each fly, each fly needs to learn through its own experiences what a particular pattern of Kenyon cell activation means.
Aso et al. have now applied sophisticated molecular genetic and anatomical techniques to thousands of different transgenic flies to identify the neurons of the mushroom body. The resulting map reveals that the mushroom body contains roughly 2200 neurons, including seven types of Kenyon cells and 21 types of output cells, as well as 20 types of neurons that use the neurotransmitter dopamine. Moreover, this map provides insights into the circuits that support odor-based learning. It reveals, for example, that the mushroom body can be divided into 15 anatomical compartments that are each defined by the presence of a specific set of output and dopaminergic neuron cell types. Since the dopaminergic neurons help to shape a fly's response to odors on the basis of previous experience, this organization suggests that these compartments may be semi-autonomous information processing units.
In contrast to the rest of the insect brain, the mushroom body has a flexible organization that is similar to that of the mammalian brain. Elucidating the circuits that support associative learning in fruit flies should therefore make it easier to identify the equivalent mechanisms in vertebrate animals.
PMCID: PMC4273437  PMID: 25535793
mushroom body; olfactory learning; associative memory; neuronal circuits; dopamine; plasticity; D. melanogaster
21.  Experience Modifies Olfactory Acuity: Acetylcholine-Dependent Learning Decreases Behavioral Generalization between Similar Odorants 
Perceptual learning has been demonstrated in several thalamocortical sensory systems wherein experience enhances sensory acuity for trained stimuli. This perceptual learning is believed to be dependent on changes in sensory cortical receptive fields. Sensory experience and learning also modifies receptive fields and neural response patterns in the mammalian olfactory system; however, to date there has been little reported evidence of learned changes in behavioral olfactory acuity. The present report used a bradycardial orienting response and cross-habituation paradigm that allowed assessment of behavioral discrimination of nearly novel odorants, and then used the same paradigm to examine odorant discrimination after associative olfactory conditioning with similar or dissimilar odorants. The results demonstrate that associative conditioning can enhance olfactory acuity for odors that are the same as or similar to the learned odorant, but not for odors dissimilar to the learned odorant. Furthermore, scopolamine injected before associative conditioning can block the acquisition of this learned enhancement in olfactory acuity. These results could have important implications for mechanisms of olfactory perception and memory, as well as for correlating behavioral olfactory acuity with observed spatial representations of odorant features in the olfactory system.
PMCID: PMC2365514  PMID: 11784813
adaptation; perceptual learning; piriform cortex; olfaction; olfactory memory; scopolamine
22.  Evolution of Gene Expression in the Drosophila Olfactory System 
Molecular Biology and Evolution  2008;25(6):1081-1092.
Host plant shifts by phytophagous insects play a key role in insect evolution and plant ecology. Such shifts often involve major behavioral changes as the insects must acquire an attraction and/or lose the repulsion to the new host plant's odor and taste. The evolution of chemotactic behavior may be due, in part, to gene expression changes in the peripheral sensory system. To test this hypothesis, we compared gene expression in the olfactory organs of Drosophila sechellia, a narrow ecological specialist that feeds on the fruit of Morinda citrifolia, with its close relatives Drosophila simulans and Drosophila melanogaster, which feed on a wide variety of decaying plant matter. Using whole-genome microarrays and quantitative polymerase chain reaction, we surveyed the entire repertoire of Drosophila odorant receptors (ORs) and odorant-binding proteins (OBPs) expressed in the antennae. We found that the evolution of OR and OBP expression was accelerated in D. sechellia compared both with the genome average in that species and with the rate of OR and OBP evolution in the other species. However, some of the gene expression changes that correlate with D. sechellia’s increased sensitivity to Morinda odorants may predate its divergence from D. simulans. Interspecific divergence of olfactory gene expression cannot be fully explained by changes in the relative abundance of different sensilla as some ORs and OBPs have evolved independently of other genes expressed in the same sensilla. A number of OR and OBP genes are upregulated in D. sechellia compared with its generalist relatives. These genes include Or22a, which likely responds to a key odorant of M. citrifolia, and several genes that are yet to be characterized in detail. Increased expression of these genes in D. sechellia may have contributed to the evolution of its unique chemotactic behavior.
PMCID: PMC3299402  PMID: 18296696
olfactory receptors; Drosophila sechellia; gene expression; microarrays; regulatory evolution; host plant preferences
23.  Understanding Odor Information Segregation in the Olfactory Bulb by Means of Mitral and Tufted Cells 
PLoS ONE  2014;9(10):e109716.
Odor identification is one of the main tasks of the olfactory system. It is performed almost independently from the concentration of the odor providing a robust recognition. This capacity to ignore concentration information does not preclude the olfactory system from estimating concentration itself. Significant experimental evidence has indicated that the olfactory system is able to infer simultaneously odor identity and intensity. However, it is still unclear at what level or levels of the olfactory pathway this segregation of information occurs. In this work, we study whether this odor information segregation is performed at the input stage of the olfactory bulb: the glomerular layer. To this end, we built a detailed neural model of the glomerular layer based on its known anatomical connections and conducted two simulated odor experiments. In the first experiment, the model was exposed to an odor stimulus dataset composed of six different odorants, each one dosed at six different concentrations. In the second experiment, we conducted an odor morphing experiment where a sequence of binary mixtures going from one odor to another through intermediate mixtures was presented to the model. The results of the experiments were visualized using principal components analysis and analyzed with hierarchical clustering to unveil the structure of the high-dimensional output space. Additionally, Fisher's discriminant ratio and Pearson's correlation coefficient were used to quantify odor identity and odor concentration information respectively. Our results showed that the architecture of the glomerular layer was able to mediate the segregation of odor information obtaining output spiking sequences of the principal neurons, namely the mitral and external tufted cells, strongly correlated with odor identity and concentration, respectively. An important conclusion is also that the morphological difference between the principal neurons is not key to achieve odor information segregation.
PMCID: PMC4214673  PMID: 25356586
24.  Synaptic Learning Rules and Sparse Coding in a Model Sensory System 
PLoS Computational Biology  2008;4(4):e1000062.
Neural circuits exploit numerous strategies for encoding information. Although the functional significance of individual coding mechanisms has been investigated, ways in which multiple mechanisms interact and integrate are not well understood. The locust olfactory system, in which dense, transiently synchronized spike trains across ensembles of antenna lobe (AL) neurons are transformed into a sparse representation in the mushroom body (MB; a region associated with memory), provides a well-studied preparation for investigating the interaction of multiple coding mechanisms. Recordings made in vivo from the insect MB demonstrated highly specific responses to odors in Kenyon cells (KCs). Typically, only a few KCs from the recorded population of neurons responded reliably when a specific odor was presented. Different odors induced responses in different KCs. Here, we explored with a biologically plausible model the possibility that a form of plasticity may control and tune synaptic weights of inputs to the mushroom body to ensure the specificity of KCs' responses to familiar or meaningful odors. We found that plasticity at the synapses between the AL and the MB efficiently regulated the delicate tuning necessary to selectively filter the intense AL oscillatory output and condense it to a sparse representation in the MB. Activity-dependent plasticity drove the observed specificity, reliability, and expected persistence of odor representations, suggesting a role for plasticity in information processing and making a testable prediction about synaptic plasticity at AL-MB synapses.
Author Summary
The way in which the brain encodes, processes, transforms, and stores sensory information is a fundamental question in systems neuroscience. One challenge is to understand how neural oscillations, synchrony, population coding, and sparseness interact in the process of transforming and transferring information. Another question is how synaptic plasticity, the ability of synapses to change their strength, interacts efficiently with these different coding strategies to support learning and information storage. We approached these questions, rarely accessible to direct experimental investigation, in the olfactory system of the locust, a well-studied example. Here, the neurons in the antennal lobe carry neural representations of odor identity using dense, spatially distributed, oscillatory synchronized patterns of neural activity. Odor information cannot be interpreted by considering their activity independently. On the contrary, in the mushroom body—the next processing region, involved in the storage and retrieval of olfactory memories and analogous to the olfactory cortex—odor representations are sparse and carried by more selective neurons. Sparse information coding by ensembles of neurons provides several important advantages including high memory capacity, low overlap between stored objects, and easy information retrieval. How is this sparseness achieved? Here, with a rigorous computational model of the olfactory system, we demonstrate that plasticity at the input afferents to the mushroom body can efficiently mediate the delicate tuning necessary to selectively filter intense sensory input, condensing it to the sparse responses observed in the mushroom body. Our results suggest a general mechanism for plasticity-enabled sparse representations in other sensory systems, such as the visual system. Overall, we illustrate a potential central role for plasticity in the transfer of information across different coding strategies within neural systems.
PMCID: PMC2278376  PMID: 18421373
25.  A spiking neural network model of self-organized pattern recognition in the early mammalian olfactory system 
Olfactory sensory information passes through several processing stages before an odor percept emerges. The question how the olfactory system learns to create odor representations linking those different levels and how it learns to connect and discriminate between them is largely unresolved. We present a large-scale network model with single and multi-compartmental Hodgkin–Huxley type model neurons representing olfactory receptor neurons (ORNs) in the epithelium, periglomerular cells, mitral/tufted cells and granule cells in the olfactory bulb (OB), and three types of cortical cells in the piriform cortex (PC). Odor patterns are calculated based on affinities between ORNs and odor stimuli derived from physico-chemical descriptors of behaviorally relevant real-world odorants. The properties of ORNs were tuned to show saturated response curves with increasing concentration as seen in experiments. On the level of the OB we explored the possibility of using a fuzzy concentration interval code, which was implemented through dendro-dendritic inhibition leading to winner-take-all like dynamics between mitral/tufted cells belonging to the same glomerulus. The connectivity from mitral/tufted cells to PC neurons was self-organized from a mutual information measure and by using a competitive Hebbian–Bayesian learning algorithm based on the response patterns of mitral/tufted cells to different odors yielding a distributed feed-forward projection to the PC. The PC was implemented as a modular attractor network with a recurrent connectivity that was likewise organized through Hebbian–Bayesian learning. We demonstrate the functionality of the model in a one-sniff-learning and recognition task on a set of 50 odorants. Furthermore, we study its robustness against noise on the receptor level and its ability to perform concentration invariant odor recognition. Moreover, we investigate the pattern completion capabilities of the system and rivalry dynamics for odor mixtures.
PMCID: PMC3916767  PMID: 24570657
pattern recognition; olfactory bulb; piriform cortex; large-scale neuromorphic systems; spiking neural network; BCPNN; concentration invariance; pattern rivalry

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