Olfactory Environment Research Articles

High Precision of Spike Timing across Olfactory Receptor Neurons Allows Rapid Odor Coding in Drosophila

SummaryIn recent years, it has become evident that olfaction is a fast sense, and millisecond short differences in stimulus onsets are used by animals to analyze their olfactory environment. In contrast, olfactory receptor neurons are thought to be relatively slow and temporally imprecise. These observations have led to a conundrum: how, then, can an animal resolve fast stimulus dynamics and smell with high temporal acuity? Using parallel recordings from olfactory receptor neurons in Drosophila, we found hitherto unknown fast and temporally precise odorant-evoked spike responses, with first spike latencies (relative to odorant arrival) down to 3 ms and with a SD below 1 ms. These data provide new upper bounds for the speed of olfactory processing and suggest that the insect olfactory system could use the precise spike timing for olfactory coding and computation, which can explain insects' rapid processing of temporal stimuli when encountering turbulent odor plumes.

Differential effects of adaptation on odor discrimination.

Adaptation of neural responses is ubiquitous in sensory systems and can potentially facilitate many important computational functions. Here we examined this issue with a well-constrained computational model of the early olfactory circuits. In the insect olfactory system, the responses of olfactory receptor neurons (ORNs) on the antennae adapt over time. We found that strong adaptation of sensory input is important for rapidly detecting a fresher stimulus encountered in the presence of other background cues and for faithfully representing its identity. However, when the overlapping odorants were chemically similar, we found that adaptation could alter the representation of these odorants to emphasize only distinguishing features. This work demonstrates novel roles for peripheral neurons during olfactory processing in complex environments. NEW & NOTEWORTHY Olfactory systems face the problem of distinguishing salient information from a complex olfactory environment. The neural representations of specific odor sources should be consistent regardless of the background. How are olfactory representations robust to varying environmental interference? We show that in locusts the extraction of salient information begins in the periphery. Olfactory receptor neurons adapt in response to odorants. Adaptation can provide a computational mechanism allowing novel odorant components to be highlighted during complex stimuli.

Binding properties of four antennae-expressed chemosensory proteins (CSPs) with insecticides indicates the adaption of Spodoptera litura to environment

Insects receive a variety of chemical signals from the environment. Chemosensory protein (CSP) is one of the olfactory proteins that can accommodate a variety of small molecules and have the ability to bind to lipophilic compounds, transmitting nonvolatile odor molecules and chemical stimuli to target cells. To understand the correlation between the insect olfactory system and environment, we identified four antennae-expressed SlituCSP genes and investigated their expression profiles after treatment with different temperatures, starvation and three commonly used pesticides: chlorpyrifos, emamectin benzoate and fipronil. The transcriptions of four SlituCSP genes are affected by pesticide treatment and less affected by starvation and different temperatures. To further understand the molecular function of CSPs and their correlation with pesticides, we expressed and purified four SlituCSPs and assayed their binding ability with pesticides. The binding of four SlituCSPs with three pesticides were determined using a fluorescence competitive binding assay. We found direct binding between CSPs and pesticides, especially between SlituCSP18 and chlorpyrifos/fipronil and between SlituCSP6 and all three pesticides. The high binding affinity with pesticides and the significant down-regulation of SlituCSP18 by chlorpyrifos suggests that SlituCSP18 is more sensitive to pesticide treatment and may play an important role in mediating the interaction of the olfactory system and the pesticide. This study can help us understand the role of CSP proteins in the adaption of S. litura to the environment.

Effects of diversity in olfactory environment on children\u2019s sense of smell

Diversity in children’s everyday olfactory environment may affect the development of their olfactory abilities and odor awareness. To test this, we collected data on olfactory abilities using the Sniffin’ Sticks and odor awareness with Children’s Olfactory Behaviors in Everyday Life Questionnaire in 153 preschool children and retested them one and a half year later. Parents completed an inventory on children’s exposure to a variety of odors and on their own odor awareness using the Odor Awareness Scale. We controlled for the effects of age and verbal fluency on the children’s performance. We found that the children’s odor identification and discrimination scores differed as a function of parental odor awareness. Although these effects were rather small, they were commensurate in size with those of gender and age. To the best of our knowledge, this study is the first to present evidence that diversity in children’s olfactory environment affects variation in their olfactory abilities and odor awareness. We suggest that future studies consider the long-term impact of perceptual learning out of the laboratory and its consequences for olfactory development.

Odor-Driven Spike Synchrony Across Olfactory Receptor Neurons Allows Rapid Odor Identification in Drosophila

In recent years, it has become evident that olfaction is a fast sense, and millisecond short differences in stimulus onsets are used by animals to analyze their olfactory environment. In contrast, olfactory receptor neurons are thought to be relatively slow and temporally imprecise. These observations have led to a conundrum: How, then, can an animal resolve fast stimulus dynamics and smell with high temporal acuity? Using parallel recordings from olfactory receptor neurons in Drosophila, we found hitherto unknown fast and temporally precise odorant‐evoked spike responses, with first spike latencies as short as 3 ms and with a standard deviation (jitter) well below 1 ms. These data provide new upper bounds for the speed of olfactory processing and suggest that the insect olfactory system can use the precise spike timing for olfactory coding and computation, which can explain insects’ rapid processing of temporal stimuli when encountering turbulent odor plumes.

Analysis of Fos expression in the rat olfactory neurogenic region following single exposure to maternal separation during different neonatal stages.

Accumulating evidence confirms that the exposure of neonatal rats to maternal separation can significantly alter individual processes of postnatal neurogenesis in the olfactory neurogenic region - the subventricular zone (SVZ) and the rostral migratory stream (RMS). To establish the stressful influence of MS on postnatal neurogenesis we have investigated whether altered olfactory environment caused by short-term MS induces expression of Fos protein in the SVZ/RMS and in the olfactory cortical area - anterior olfactory nucleus (AON) of neonatal rats. Pups were separated from mothers for 2 hours at the postnatal days 7, 14 and 21. Immunohistochemically labeled Fos protein was assessed. Our results revealed that single exposure to MS is a stressful event that selectively and in age-dependent manner stimulates cellular activity in the SVZ and AON. A few Fos+ cells were found in the SVZ of P21 control animals and MS significantly increased their number. This suggests that some SVZ cells are included in the circuitry, which is activated by MS and that these cells have complete equipment for the Fos signal transduction. MS significantly increased the number of Fos+ cells in the AON in all age stages examined suggesting that its effect is mediated by olfaction.

Stimulation of the Locus Ceruleus Modulates Signal-to-Noise Ratio in the Olfactory Bulb.

Norepinephrine (NE) has been shown to influence sensory, and specifically olfactory processing at the behavioral and physiological levels, potentially by regulating signal-to-noise ratio (S/N). The present study is the first to look at NE modulation of olfactory bulb (OB) in regards to S/N in vivo We show, in male rats, that locus ceruleus stimulation and pharmacological infusions of NE into the OB modulate both spontaneous and odor-evoked neural responses. NE in the OB generated a non-monotonic dose-response relationship, suppressing mitral cell activity at high and low, but not intermediate, NE levels. We propose that NE enhances odor responses not through direct potentiation of the afferent signal per se, but rather by reducing the intrinsic noise of the system. This has important implications for the ways in which an animal interacts with its olfactory environment, particularly as the animal shifts from a relaxed to an alert behavioral state.SIGNIFICANCE STATEMENT Sensory perception can be modulated by behavioral states such as hunger, fear, stress, or a change in environmental context. Behavioral state often affects neural processing via the release of circulating neurochemicals such as hormones or neuromodulators. We here show that the neuromodulator norepinephrine modulates olfactory bulb spontaneous activity and odor responses so as to generate an increased signal-to-noise ratio at the output of the olfactory bulb. Our results help interpret and improve existing ideas for neural network mechanisms underlying behaviorally observed improvements in near-threshold odor detection and discrimination.

Development and Refinement of Functional Properties of Adult-Born Neurons

New neurons appear only in a few regions of the adult mammalian brain and become integrated into existing circuits. Little is known about the functional development of individual neurons invivo. We examined the functional life history of adult-born granule cells (abGCs) in the olfactory bulb using multiphoton imaging in awake and anesthetized mice. We found that abGCs can become responsive to odorants soon after they arrive in the olfactory bulb. Tracking identified abGCs over weeks revealed that the robust and broadly tuned responses of most newly arrived abGCs gradually become more selective over a period of ∼3weeks, but a small fraction achieves broader tuning with maturation. Enriching the olfactory environment of mice prolonged the period over which abGCs were strongly and broadly responsive to odorants. Our data offer direct support for rapid integration of adult-born neurons into existing circuits, followed by experience-dependent refinement of their functional connectivity.

Odorant-odorant metabolic interaction, a novel actor in olfactory perception and behavioral responsiveness

In the nasal olfactory epithelium, olfactory metabolic enzymes ensure odorant clearance from the olfactory receptor environment. This biotransformation of odorants into deactivated polar metabolites is critical to maintaining peripheral sensitivity and perception. Olfactory stimuli consist of complex mixtures of odorants, so binding interactions likely occur at the enzyme level and may impact odor processing. Here, we used the well-described model of mammary pheromone-induced sucking-related behavior in rabbit neonates. It allowed to demonstrate how the presence of different aldehydic odorants efficiently affects the olfactory metabolism of this pheromone (an aldehyde too: 2-methylbut-2-enal). Indeed, according to in vitro and ex vivo measures, this metabolic interaction enhances the pheromone availability in the epithelium. Furthermore, in vivo presentation of the mammary pheromone at subthreshold concentrations efficiently triggers behavioral responsiveness in neonates when the pheromone is in mixture with a metabolic challenger odorant. These findings reveal that the periphery of the olfactory system is the place of metabolic interaction between odorants that may lead, in the context of odor mixture processing, to pertinent signal detection and corresponding behavioral effect.

Spontaneous Rapid Odor Source Localization Behavior Requires Interhemispheric Communication

Navigation, finding food sources, and avoiding danger critically depend on the identification and spatial localization of airborne chemicals. When monitoring the olfactory environment, rodents spontaneously engage in active olfactory sampling behavior, also referred to as exploratory sniffing [1]. Exploratory sniffing is characterized by stereotypical high-frequency respiration, which is also reliably evoked by novel odorant stimuli [2, 3]. Tostudy novelty-induced exploratory sniffing, wedeveloped a novel, non-contact method for measuring respiration by infrared (IR) thermography in a behavioral paradigm in which novel andfamiliar stimuli are presented to head-restrained mice. We validated the method by simultaneously performing nasal pressure measurements, a commonly used invasive approach [2, 4], and confirmed highly reliable detection of inhalation onsets. We further discovered that mice actively orient their nostrils toward novel, previously unexperienced, smells. In line with the remarkable speed of olfactory processing reported previously [3, 5, 6], we find that mice initiate their response already within the first sniff after odor onset. Moreover, transecting the anterior commissure (AC) disrupted orienting, indicating that the orienting response requires interhemispheric transfer ofinformation. This suggests that mice compare odorant information obtained from the two bilaterally symmetric nostrils to locate the source of the novel odorant. We further demonstrate that asymmetric activation of the anterior olfactory nucleus (AON) is both necessary and sufficient for eliciting orienting responses. These findings support the view that the AON plays an important role in the internostril difference comparison underlying rapid odor source localization.

Mice Lacking M1 and M3 Muscarinic Acetylcholine Receptors Have Impaired Odor Discrimination and Learning.

The cholinergic system has extensive projections to the olfactory bulb (OB) where it produces a state-dependent regulation of sensory gating. Previous work has shown a prominent role of muscarinic acetylcholine (ACh) receptors (mAChRs) in regulating the excitability of OB neurons, in particular the M1 receptor. Here, we examined the contribution of M1 and M3 mAChR subtypes to olfactory processing using mice with a genetic deletion of these receptors, the M1−/− and the M1/M3−/− knockout (KO) mice. Genetic ablation of the M1 and M3 mAChRs resulted in a significant deficit in odor discrimination of closely related molecules, including stereoisomers. However, the discrimination of dissimilar molecules, social odors (e.g., urine) and novel object recognition was not affected. In addition the KO mice showed impaired learning in an associative odor-learning task, learning to discriminate odors at a slower rate, indicating that both short and long-term memory is disrupted by mAChR dysfunction. Interestingly, the KO mice exhibited decreased olfactory neurogenesis at younger ages, a deficit that was not maintained in older animals. In older animals, the olfactory deficit could be restored by increasing the number of new born neurons integrated into the OB after exposing them to an olfactory enriched environment, suggesting that muscarinic modulation and adult neurogenesis could be two different mechanism used by the olfactory system to improve olfactory processing.

Impact of sensory design interventions on image quality, patient anxiety and overall patient experience at MRI.

This study aimed to assess the effect of sensory stimulation on patient MRI experience and to assess whether sensory stimulation has a significant effect on MR image quality. A case-control study was conducted over 4 months, involving patients undergoing MRI brain, cervical spine, breast and prostate. The study involved 106 patients, 64 cases and 42 controls. Cases underwent sensory stimulation during the scan in the form of a scented cotton pad placed in the scanner near their head and/or calming bird noises were played over headphones. Post-scan, participants completed a questionnaire regarding their experience of MRI. Scanning radiographers completed a questionnaire regarding patient tolerance of the scan. All studies were evaluated by two radiologists for the presence of movement artefact. 39% of cases and 38% of controls reported anxiety in the days preceding MRI. 6.2% of cases required coaching during image acquisition, while 9.7% of controls required coaching. 4.7% of cases and 4.8% controls required sequence repetition owing to movement artefact. Mean patient experience score (as graded by the patient) for controls was 1.74 ± 0.63 standard deviation (SD) and for cases, it was 1.67 ± 0.60 SD. (Lower assigned scores equated to a better experience). Mean patient experience score based on comments on a 5-point scale as graded by two observers was 2.81 ± 0.70 SD for controls, 2.42 + 0.94 SD for sound intervention and 2.46 ± 1.01 SD for scent intervention. Mean motion artefact score graded by the two radiologists was 1.13 ± 0.53 SD for controls and 1.08 ± 0.36 SD for cases. (A lower score equated to less movement artefact). We demonstrated a trend towards a relaxing experience in those patients undergoing MRI for the first time who underwent sensory intervention. Participant positive ratings of the smell pleasantness were associated with a reduced likelihood of experiencing anxiety (p = 0.13). Results were not statistically significant. This study demonstrated a subjectively improved experience of MRI for some patients with the intervention of sound and smell. The study failed to show a significant decrease in patient movement during MRI investigations. This may relate to the small study size and a low level of patient movement in the case group. Advances in knowledge: Sound and olfactory sensory environment interventions at MRI can improve the patient experience. These low-cost interventions are well tolerated, may improve acceptance of MRI in patients with anxiety and offer a competitive advantage to imaging centres.

Olfactory variation in mouse husbandry and its implications for refinement and standardization: UK survey of non-animal scents.

With their highly sensitive olfactory system, the behaviour and physiology of mice are not only influenced by the scents of conspecifics and other species, but also by many other chemicals in the environment. The constraints of laboratory housing limit a mouse's capacity to avoid aversive odours that could be present in the environment. Potentially odorous items routinely used for husbandry procedures, such as sanitizing products and gloves, could be perceived by mice as aversive or attractive, and affect their behaviour, physiology and experimental results. A survey was sent to research institutions in the UK to enquire about husbandry practices that could impact on the olfactory environment of the mouse. Responses were obtained from 80 individuals working in 51 institutions. Husbandry practices varied considerably. Seventy percent of respondents reported always wearing gloves for handling mice, with nitrile being the most common glove material (94%) followed by latex (23%) and vinyl (14%). Over six different products were listed for cleaning surfaces, floors, anaesthesia and euthanasia chambers and behavioural apparatus. In all cases Trigene™ (now called Anistel™) was the most common cleaning product used (43, 41, 40 and 49%, respectively). Depending on the attribute considered, between 7 and 19% of respondents thought that cleaning products definitely, or were likely to, have strong effects on standardization, mouse health, physiology or behaviour. Understanding whether and how these odours affect mouse welfare will help to refine mouse husbandry and experimental procedures through practical recommendations, to improve the quality of life of laboratory animals and the experimental data obtained.

Significance of sniffing pattern during the acquisition of an olfactory discrimination task

Active sampling of olfactory environment consists of sniffing in rodents. The importance of sniffing dynamics is well established at the neuronal and behavioral levels. Patterns of sniffing have been shown to be modulated by the physicochemical properties of odorants, particularly concentration and sorption. Sniffing is also heavily impacted by higher processing related to the behavioral context, emotion and attentional demand. However, how the pattern of sniffing evolves over the course of learning of an experimental olfactory conditioning is still poorly understood. We tested this question by monitoring sniffing activity, using a whole-body plethysmograph, on rats performing a two-alternative choice odor discrimination task. We followed sniff variations at different learning stages (naïve, well-trained, expert). We found that during the acquisition of an odor discrimination task, rats acquired a global sniffing pattern, independent of the odor pair used. This pattern consists of a longer sampling duration, a higher sniffing frequency, and a larger amplitude. In parallel, subtle differences of sniffing between the two odors of a pair were also observed. This sniffing behavior was not only associated with a better and faster acquisition of the discrimination task but was also transferred to other odor sets and refined after a long-term pause so as to reduce the sampling duration and maintain a specific sniffing frequency. Our results provide additional arguments that sniffing is a complex sensorimotor act that is strongly affected by olfactory learning.

Olfactory modulation of affective touch processing — A neurophysiological investigation

Touch can be highly emotional, and depending on the environment, it can be perceived as pleasant and comforting or disgusting and dangerous. Here, we studied the impact of context on the processing of tactile stimuli using a functional magnetic resonance imaging (fMRI) paradigm. This was achieved by embedding tactile stimulation in a variable olfactory environment.Twenty people were scanned with BOLD fMRI while receiving the following stimulus blocks: Slow stroking Touch, Civette odor (feces like), Rose odor, Touch+Civette, and Touch+Rose. Ratings of pleasantness and intensity of tactile stimuli and ratings of disgust and intensity of olfactory stimuli were collected. The impact of the olfactory context on the processing of touch was studied using covariance analyses. Coupling between olfactory processing and somatosensory processing areas was assessed with psychophysiological interaction analysis (PPI).A subjectively disgusting olfactory environment significantly reduced the perceived pleasantness of touch. The touch fMRI activation in the secondary somatosensory cortex, operculum 1 (OP1), was positively correlated with the disgust towards the odors. Decreased pleasantness of touch was related to decreased posterior insula activity. PPI analysis revealed a significant interaction between the OP1, posterior insula, and regions processing the disgust of odors (orbitofrontal cortex and amygdala).We conclude that the disgust evaluation of the olfactory environment moderates neural reactivity in somatosensory regions by upregulation of the OP1 and downregulation of the posterior insula. This adaptive regulation of affective touch processing may facilitate adaptive reaction to a potentially harmful stimulus.

A Functionally Conserved Gene Regulatory Network Module Governing Olfactory Neuron Diversity.

Sensory neuron diversity is required for organisms to decipher complex environmental cues. In Drosophila, the olfactory environment is detected by 50 different olfactory receptor neuron (ORN) classes that are clustered in combinations within distinct sensilla subtypes. Each sensilla subtype houses stereotypically clustered 1–4 ORN identities that arise through asymmetric divisions from a single multipotent sensory organ precursor (SOP). How each class of SOPs acquires a unique differentiation potential that accounts for ORN diversity is unknown. Previously, we reported a critical component of SOP diversification program, Rotund (Rn), increases ORN diversity by generating novel developmental trajectories from existing precursors within each independent sensilla type lineages. Here, we show that Rn, along with BarH1/H2 (Bar), Bric-à-brac (Bab), Apterous (Ap) and Dachshund (Dac), constitutes a transcription factor (TF) network that patterns the developing olfactory tissue. This network was previously shown to pattern the segmentation of the leg, which suggests that this network is functionally conserved. In antennal imaginal discs, precursors with diverse ORN differentiation potentials are selected from concentric rings defined by unique combinations of these TFs along the proximodistal axis of the developing antennal disc. The combinatorial code that demarcates each precursor field is set up by cross-regulatory interactions among different factors within the network. Modifications of this network lead to predictable changes in the diversity of sensilla subtypes and ORN pools. In light of our data, we propose a molecular map that defines each unique SOP fate. Our results highlight the importance of the early prepatterning gene regulatory network as a modulator of SOP and terminally differentiated ORN diversity. Finally, our model illustrates how conserved developmental strategies are used to generate neuronal diversity.

Pigeons home faster through polluted air.

Air pollution, especially haze pollution, is creating health issues for both humans and other animals. However, remarkably little is known about how animals behaviourally respond to air pollution. We used multiple linear regression to analyse 415 pigeon races in the North China Plain, an area with considerable air pollution, and found that while the proportion of pigeons successfully homed was not influenced by air pollution, pigeons homed faster when the air was especially polluted. Our results may be explained by an enhanced homing motivation and possibly an enriched olfactory environment that facilitates homing. Our study provides a unique example of animals’ response to haze pollution; future studies are needed to identify proposed mechanisms underlying this effect.

Dynamical sensory representations establish a rapid odor code in a spiking model of the insect olfactory system

In their natural environment, animals sense and evaluate olfactory cues of time-varying composition and concentration. Their olfactory pathways are adapted to the natural stimulus statistics, thus it is not surprising that odor processing is fast [1]. Honey bees, for example, learn to discriminate odors presented as short as 200 ms [2]. The neural odor code in these animals emerges within 50ms after stimulus onset and neural representation changes dynamically during and after an odorant is present [1,3]. How is the insect olfactory system optimized to reliably estimate spatial and temporal aspects of the olfactory environment and what are the mechanisms behind rapid odor processing? To investigate odor encoding at the Antennal Lobe (AL) and the Mushroom Body (MB) level, we employ a simple phenomenological spiking network model of the honeybee olfactory system. The model implements a transformation from a low dimensional dense odorant representation in the AL to a high dimensional sparse representation in the MB. We demonstrate how information about the stimulus is present in both encoding schemes, by time resolved classification of neural activity. Our model displays sparse and robust odor representation in the Mushroom Body [4]. Typically, less than 10% of the Kenyon Cell population is activated by an odor, with only 2-3 spikes at the odor onset (Figure ​(Figure1A).1A). KC spikes establish a rapid odor identity code at stimulus onset, while intrinsic adaptation currents provide a persistent and prolonged odor trace (Figure ​(Figure1B).1B). Our approach allows us to investigate dynamical changes in odor representations and predict odor after images. Figure 1 (A) Kenyon Cell spike raster plot. Stimulation is indicated by gray shading (B) Top: Decoding Accuracy given two odors (chance level: 0.5) as a function of time based on spike count estimates in 50ms time bins. Bottom: Decoding accuracy based on KC adaptation ...

Changes in Olfactory Sensory Neuron Physiology and Olfactory Perceptual Learning After Odorant Exposure in Adult Mice

The adult olfactory system undergoes experience-dependent plasticity to adapt to the olfactory environment. This plasticity may be accompanied by perceptual changes, including improved olfactory discrimination. Here, we assessed experience-dependent changes in the perception of a homologous aldehyde pair by testing mice in a cross-habituation/dishabituation behavioral paradigm before and after a week-long ester-odorant exposure protocol. In a parallel experiment, we used optical neurophysiology to observe neurotransmitter release from olfactory sensory neuron (OSN) terminals in vivo, and thus compared primary sensory representations of the aldehydes before and after the week-long ester-odorant exposure in individual animals. Mice could not discriminate between the aldehydes during pre-exposure testing, but ester-exposed subjects spontaneously discriminated between the homologous pair after exposure, whereas home cage control mice cross-habituated. Ester exposure did not alter the spatial pattern, peak magnitude, or odorant-selectivity of aldehyde-evoked OSN input to olfactory bulb glomeruli, but did alter the temporal dynamics of that input to make the time course of OSN input more dissimilar between odorants. Together, these findings demonstrate that odor exposure can induce both physiological and perceptual changes in odor processing, and suggest that changes in the temporal patterns of OSN input to olfactory bulb glomeruli could induce differences in odor quality.

Olfactory signal coding in an odor background

Insects communicating with pheromones are confronted with an olfactory environment featuring a diversity of volatile organic compounds from plant origin. These volatiles constitute a rich and fluctuant background from which the information carried by the pheromone signal must be extracted. Thus, the pheromone receptor neurons must encode into spike trains the quality, intensity and temporal characteristics of the signal that are determinant to the recognition and localization of a conspecific female. We recorded and analyzed the responses of the pheromone olfactory receptor neurons of male moths to sex pheromone in different odor background conditions. We show that in spite of the narrow chemical tuning of the pheromone receptor neurons, the sensory input can be altered by odorant background.