Odor Context Research Articles

Olfactory-to-visual facilitation in the infant brain declines gradually from 4 to 12 months.

During infancy, intersensory facilitation declines gradually as unisensory perception develops. However, this trade-off was mainly investigated using audiovisual stimulations. Here, fifty 4- to 12-month-old infants (26 females, predominately White) were tested in 2017-2020 to determine whether the facilitating effect of their mother's body odor on neural face categorization, as previously observed at 4 months, decreases with age. In a baseline odor context, the results revealed a face-selective electroencephalographic response that increases and changes qualitatively between 4 and 12 months, marking improved face categorization. At the same time, the benefit of adding maternal odor fades with age (R2 = .31), indicating an inverse relation with the amplitude of the visual response, and generalizing to olfactory-visual interactions previous evidence from the audiovisual domain.

A configural context signal simultaneously but separably drives positioning and orientation of hippocampal place fields.

Effective self-localization requires that the brain can resolve ambiguities in incoming sensory information arising from self-similarities (symmetries) in the environment structure. We investigated how place cells use environmental cues to resolve the ambiguity of a rotationally symmetric environment, by recording from hippocampal CA1 in rats exploring a "2-box." This apparatus comprises two adjacent rectangular compartments, identical but with directionally opposed layouts (cue card at one end and central connecting doorway) and distinguished by their odor contexts (lemon vs. vanilla). Despite the structural and visual rotational symmetry of the boxes, no place cells rotated their place fields. The majority changed their firing fields (remapped) between boxes but some repeated them, maintaining a translational symmetry and thus adopting a relationship to the layout that was conditional on the odor. In general, the place field ensemble maintained a stable relationship to environment orientation as defined by the odors, but sometimes the whole ensemble rotated its firing en bloc, decoupling from the odor context cues. While the individual elements of these observations-odor remapping, place field repetition, ensemble rotation, and decoupling from context-have been reported in isolation, the combination in the one experiment is incompletely explained within current models. We redress this by proposing a model in which odor cues enter into a three-way association with layout cues and head direction, creating a configural context signal that facilitates two separate processes: place field orientation and place field positioning. This configuration can subsequently still function in the absence of one of its components, explaining the ensemble decoupling from odor. We speculate that these interactions occur in retrosplenial cortex, because it has previously been implicated in context processing, and all the relevant signals converge here.

Descending neuron population dynamics during odor-evoked and spontaneous limb-dependent behaviors.

Deciphering how the brain regulates motor circuits to control complex behaviors is an important, long-standing challenge in neuroscience. In the fly, Drosophila melanogaster, this is coordinated by a population of ~ 1100 descending neurons (DNs). Activating only a few DNs is known to be sufficient to drive complex behaviors like walking and grooming. However, what additional role the larger population of DNs plays during natural behaviors remains largely unknown. For example, they may modulate core behavioral commands or comprise parallel pathways that are engaged depending on sensory context. We evaluated these possibilities by recording populations of nearly 100 DNs in individual tethered flies while they generated limb-dependent behaviors, including walking and grooming. We found that the largest fraction of recorded DNs encode walking while fewer are active during head grooming and resting. A large fraction of walk-encoding DNs encode turning and far fewer weakly encode speed. Although odor context does not determine which behavior-encoding DNs are recruited, a few DNs encode odors rather than behaviors. Lastly, we illustrate how one can identify individual neurons from DN population recordings by using their spatial, functional, and morphological properties. These results set the stage for a comprehensive, population-level understanding of how the brain's descending signals regulate complex motor actions.

Investigating the neuroinflammatory regulation of social stress‐induced anxiety and opioid seeking between the sexes

Exposure to social stress leads to psychiatric conditions such as substance abuse, anxiety, and post‐traumatic stress disorder in susceptible individuals. Importantly, these conditions disproportionately affect females as compared to males, yet studies conducted in females are lacking. Further, neuroinflammation has been identified as a possible mechanism underlying this susceptibility and may link stress exposure to increased drug intake, especially for opioids. Thus, these experiments seek to further identify if ethologically relevant models of social stress that increase anxiety‐like behavior in male and female rodents also increase susceptibility to substance abuse. Our lab has characterized the witness stress paradigm in rats, where a female observes the sensory aspect of social defeat stress between two males. Previous work indicates that females are especially sensitive to the physiological and behavioral effects of this stressor due to lasting increases in neuroinflammation. The current study was completed to determine if we can predict susceptibility to social stress induced neuropsychiatric disorders by measuring behavioral responses to predator odor and if we can identify distinct physiological and neuronal markers related to stress susceptibility that are linked to increased drug seeking behavior. Specifically, adult male and female rats were first exposed to ferret odor and freezing behaviors were quantified to separate animals into high and low freezing clusters using a K‐means cluster analysis. Males were then exposed to 5 daily social defeat episodes while females observed from within the cage. To measure anxiety‐like responses to fear related cues, all rats were subsequently exposed to the ferret odor context and, 24‐hours later, the social stress context to determine the behavioral and physiological effects of these cues. These experiments found that exposure to the predator odor delineates two separate phenotypes – high and low freezing groups – for both male and female rats. Further, this behavioral phenotype predicts the level of anxiety‐like behavior that is exhibited in response to the presentation of fear‐related cues. Blood samples collected following the initial predator odor exposure and after fear cue presentation are being analyzed to determine corticosterone levels while brain tissue collected after fear cue exposure will allow us to identify the extent of the neuroinflammatory response. Current experiments using opioid conditioned place preference testing in stressed animals along with the administration of an anti‐inflammatory agent are being completed to identify the role of this stress‐induced neuroinflammation in opioid abuse. These results will ultimately allow us to elucidate the behavioral, physiological, and neuronal impact of stress exposure that contributes to increased substance abuse and will identify novel anti‐inflammatory therapeutics that can be used for the clinical prevention and treatment of these disorders.

Odor-based context-dependent memory: influence of olfactory cues on declarative and nondeclarative memory indices.

Reinstating the olfactory learning context can increase access to memory information, but it is not fully clear which memory functions are subject to an enhancing odor context reinstatement effect. Here, we tested whether congruent odor context during encoding and recall positively affected declarative and nondeclarative memory scores using a novel method for manipulation of an odorous environment; namely, intranasal Nosa plugs. Recall of a text and a complex figure as well as performance in a priming task were assessed immediately and 1 wk after encoding. We found that congruent odor exposure at encoding and recall aided free retrieval of a story at delayed testing but had no significant effect on a complex figure recall or a word completion task. Differences between the assessed memory indices suggest that olfactory environmental cues may be primarily efficient in free verbal recall tasks.

Smell what you hardly see: Odors assist visual categorization in the human brain

Visual categorization is the brain ability to rapidly and automatically respond to a certain category of inputs. Whether category-selective neural responses are purely visual or can be influenced by other sensory modalities remains unclear. Here, we test whether odors modulate visual categorization, expecting that odors facilitate the neural categorization of congruent visual objects, especially when the visual category is ambiguous. Scalp electroencephalogram (EEG) was recorded while natural images depicting various objects were displayed in rapid 12-Hz streams (i.e., 12 images / second) and variable exemplars of a target category (either human faces, cars, or facelike objects in dedicated sequences) were interleaved every 9th stimulus to tag category-selective responses at 12/9 = 1.33 Hz in the EEG frequency spectrum. During visual stimulation, participants (N = 26) were implicitly exposed to odor contexts (either body, gasoline or baseline odors) and performed an orthogonal cross-detection task. We identify clear category-selective responses to every category over the occipito-temporal cortex, with the largest response for human faces and the lowest for facelike objects. Critically, body odor boosts the response to the ambiguous facelike objects (i.e., either perceived as nonface objects or faces) over the right hemisphere, especially for participants reporting their presence post-stimulation. By contrast, odors do not significantly modulate other category-selective responses, nor the general visual response recorded at 12 Hz, revealing a specific influence on the categorization of congruent ambiguous stimuli. Overall, these findings support the view that the brain actively uses cues from the different senses to readily categorize visual inputs, and that olfaction, which has long been considered as poorly functional in humans, is well placed to disambiguate visual information.

Are male meadow voles (Microtus pennsylvanicus) influenced by social odor context with regard to scent marking behaviors?

AbstractMeadow voles (Microtus pennsylvanicus) rely on olfactory communication, such as scent marking, to find and secure mating opportunities during the breeding season. Scent marks, and odors in general, provide information about the donors and persist in the environment for extended periods, allowing a wide audience. Whether a vole responds to another scent mark(s), or odor(s), depends on the social context and the information the odor provides about the donor(s). Therefore, we examined if male scent marking toward a social odor or female meadow voles is influenced by information present or previously encountered based on contextual differences in the social odor. We presented males with two odor associations of a male with a female with contextual differences in the age of the rival. We tested male scent marking under two conditions: one with two social odors present, current information, and a second with the females present from previously encountered social information, prior information. It was found that rival male age did not affect the scent marking behavior of males toward a social odor or female voles. Rival male age also did not affect preference as males did not show a preference for either female. The lack of an effect may lie in the properties of scent marks and the natural history of meadow voles during the breeding season. The odor of an individual rival may not represent a strong enough competitive threat to influence a signaler's decisions, but the association could still provide the signaler with valuable information about which females are considered high quality.

Can ambient odors influence the recognition of emotional words? A behavioral and event-related potentials study

Odor context can affect the recognition of facial expressions. However, there is no evidence to date that odor can regulate the processing of emotional words conveyed by visual words. An emotional word recognition task was combined with event-related potential technology. Briefly, 49 adults were randomly divided into three odor contexts (pleasant odor, unpleasant odor, and no odor) to judge the valence of emotional words (positive, negative, and neutral). Both behavioral and Electroencephalography (EEG) data were collected. Both the pleasant odor and unpleasant odor contexts shortened the response time of the subjects to emotional words. In addition, negative words induced greater amplitudes of early posterior negativity (EPN) and late positive potential (LPP) than the positive and neutral words. However, the neutral words induced a larger N400 amplitude than the positive and negative words. More importantly, the processing of emotional words was found to be modulated by external odor contexts. For example, during the earlier (P2) processing stages, pleasant and unpleasant odor contexts induced greater P2 amplitudes than the no odor context. In the unpleasant odor context, negative words with the same odor valence induced greater P2 amplitudes than the positive words. During the later (N400) stages, various regions of the brain regions exhibited different results. For example, in the left and right frontal areas of the brain, exposure to positive words in a pleasant odor context resulted in a smaller N400 amplitude than exposure to neutral words in the same context. Meanwhile, in the left and right central regions, emotional words with the same valence as pleasant or unpleasant odor contexts elicited the minimum N400 amplitude. Individuals are very sensitive to emotional information. With deeper processing, different cognitive processes are reflected and they can be modulated by external odors. In the early and late stages of word processing, both pleasant and unpleasant odor contexts exhibited an undifferentiated dominance effect and could specifically modulate affectively congruent words.

Avoidance of the Plant Hormone Cis-Jasmone by Aedes aegypti Depends On Mosquito Age in Both Plant and Human Odor Backgrounds

Adults of many mosquito species feed on plants to obtain metabolic energy and to enhance reproduction. Mosquitoes primarily rely on olfaction to locate plants and are known to respond to a range of plant volatiles. We studied the olfactory response of the yellow fever mosquito Aedes aegypti to methyl jasmonate (MeJA) and cis-jasmone (CiJA), volatile compounds originating from the octadecanoid signaling pathway that plays a key role in plant defense against herbivores. Specifically, we investigated how Ae. aegypti of different ages responded to elevated levels of CiJA in two attractive odor contexts, either derived from Lima bean plants or human skin. Aedes aegypti females landed significantly less often on a surface with CiJA and MeJA compared to the solvent control, CiJA exerting a stronger reduction in landing than MeJA. Odor context (plant or human) had no significant main effect on the olfactory responses of Ae. aegypti females to CiJA. Mosquito age significantly affected the olfactory response, older females (7–9 d) responding more strongly to elevated levels of CiJA than young females (1–3 d) in either odor context. Our results show that avoidance of CiJA by Ae. aegypti is independent of odor background, suggesting that jasmonates are inherently aversive cues to these mosquitoes. We propose that avoidance of plants with elevated levels of jasmonates is adaptive to mosquitoes to reduce the risk of encountering predators that is higher on these plants, i.e. by avoiding ‘enemy-dense-space’.

The processing characteristics of bodily expressions under the odor context: An ERP study

The recognition of facial expressions has been shown to be influenced by contextual odors. The aims of this study were (1) to investigate whether odor has a similar effect on the recognition of bodily expressions, and (2) to analyze the time-course of such effects. Sixty-nine adults were randomized into three groups to identify bodily expressions (happy, fearful, and neutral) in three odor environments (pleasant odor, unpleasant odor, and no odor). Event-related potentials (ERPs) induced by the viewing bodily expressions were analyzed. Behaviorally, the unpleasant odor context promoted the recognition of bodily expressions. The ERP results showed odor influences on bodily expression recognition in two phases. In a middle stage phase (150–200 ms post-stimulus onset), VPP amplitudes induced by bodily expressions were greater in an unpleasant odor context than in a pleasant odor context. In a mid-late stage phase (beyond 200 ms), an interaction between contextual odor and bodily expression type was observed. When exposed to an unpleasant contextual odor, N2 and LPP amplitudes related to fearful bodily expressions were smaller than when exposed to other odor contexts, showing the promoting effect of mood coherence effect. Behavioral and ERP evidence confirmed that contextual odor can modulate the visual processing of bodily expressions, with an overall promoting effect of an unpleasant odor on bodily expression processing (phase one) and a specific modulating influence of odors on affectively congruent/incongruent bodily expressions (phase two).

Odor-driven face-like categorization in the human infant brain

Understanding how the young infant brain starts to categorize the flurry of ambiguous sensory inputs coming in from its complex environment is of primary scientific interest. Here, we test the hypothesis that senses other than vision play a key role in initiating complex visual categorizations in 20 4-mo-old infants exposed either to a baseline odor or to their mother's odor while their electroencephalogram (EEG) is recorded. Various natural images of objects are presented at a 6-Hz rate (six images/second), with face-like object configurations of the same object categories (i.e., eliciting face pareidolia in adults) interleaved every sixth stimulus (i.e., 1 Hz). In the baseline odor context, a weak neural categorization response to face-like stimuli appears at 1 Hz in the EEG frequency spectrum over bilateral occipitotemporal regions. Critically, this face-like-selective response is magnified and becomes right lateralized in the presence of maternal body odor. This reveals that nonvisual cues systematically associated with human faces in the infant's experience shape the interpretation of face-like configurations as faces in the right hemisphere, dominant for face categorization. At the individual level, this intersensory influence is particularly effective when there is no trace of face-like categorization in the baseline odor context. These observations provide evidence for the early tuning of face-(like)-selective activity from multisensory inputs in the developing brain, suggesting that perceptual development integrates information across the senses for efficient category acquisition, with early maturing systems such as olfaction driving the acquisition of categories in later-developing systems such as vision.

Odor-evoked hedonic contexts influence the discrimination of facial expressions in the human brain

The influence of odor valence on expressive-face perception remains unclear. Here, three “valenced” odor contexts (pleasant, unpleasant, control) were diffused while scalp electroencephalogram (EEG) was recorded in 18 participants presented with expressive faces alternating at a 6-Hz rate. One facial expression (happiness, disgust or neutrality) repeatedly arose every 6 face pictures to isolate its discrimination from other expressions at 1 Hz and harmonics in the EEG spectrum. The amplitude of the brain response to neutrality was larger in the pleasant vs. control odor context, and fewer electrodes responded in the unpleasant odor context. The number of responding electrodes was reduced for disgust in both odor contexts. The response to happiness was unchanged between odor conditions. Overall, these observations suggest that valenced odors influence the neural discrimination of facial expressions depending on both face and odor hedonic valence, especially for the emotionally ambiguous neutral expression.

The effect of social odour context on the amount of time male meadow voles, Microtus pennsylvanicus, self-groom

Abstract Communicational behaviours by individuals provide information for not only the intended target(s) of the signal but any non-target individual(s) that may be nearby. For terrestrial mammals a major form of communication and social information is through odours via scent marking and self-grooming. Self-grooming is a ubiquitous behaviour in mammals with the function thought to primarily be centred on personal care. But it has been found in rodents that self-grooming will occur in the presence of social odours thus potentially serving a communicative role. For example, male meadow voles (Microtus pennsylvanicus) self-groom in the presence of a female conspecific odour but not a male conspecific odour. Most studies examining self-grooming as a form of olfactory communication have used single odour donors but in a natural environment individuals will come across complex social odour situations. Therefore, we examined how male meadow voles respond to complex social odours with regards to their self-grooming behaviour. We tested the hypothesis that self-grooming can act as a form of olfactory communication and that male meadow voles will control this behaviour measured by differences in self-grooming rates based on social contexts. Male meadow voles did not show differences in the amount of time spent self-grooming to social odours that contained a female and varying number of rival males (0, 1, 3, or 5) or if the social odour contained an acquainted or novel male. Male meadow voles did self-groom more to a social odour that contained a female and a younger male compared to when the social odour contained a female and older male. Male meadow voles appear to adjust their self-grooming behaviour based on the context of the social information. This may be a strategy that can maximize that individual’s fitness by adjusting how much information is provided to potential rivals and mates.

Categorization of objects and faces in the infant brain and its sensitivity to maternal odor: further evidence for the role of intersensory congruency in perceptual development

According to recent evidence, rapid categorization of natural face images in the infant brain is enhanced by concomitant maternal odor (Leleu et al., 2020). To test whether this effect is selective to faces, we recorded scalp electroencephalogram (EEG) in 4-month-old infants presented with variable exemplars of a nonface visual category - cars - appearing every 6 stimuli in 6-Hz streams of natural object images. At the same time, infants were exposed to the maternal or to a control odor context. A relatively weak neural categorization response to cars (i.e., a differential response to cars that generalizes across exemplars) was observed at 1 Hz over the right occipital cortex in both odor conditions, revealing rapid categorization of an unfamiliar object in the infant brain. However, the car categorization response was not modulated by maternal odor, suggesting that odors selectively prime neural activity in the infant visual cortex to categorize congruent incoming inputs.

Unpleasant Food Odors Modulate the Processing of Facial Expressions: An Event-Related Potential Study.

In real-life situations, emotional information is often expressed through multiple sensory channels, with cross-talk between channels. Previous research has established that odor environments regulate the recognition of facial expressions. Therefore, this study combined event-related potentials (ERPs) with a facial emotion recognition task to investigate the effect of food odor context on the recognition of facial expressions and its time course. Fifty-four participants were asked to identify happy, fearful, and neutral faces in an odor context (pleasant, unpleasant or neutral). Electroencephalography (EEG) was performed to extract event-related potentials (ERPs). Behaviorally, unpleasant food odors triggered faster recognition of facial expressions, especially fearful ones. ERP results found that in the early stage, unpleasant food odors within 80–110 ms evoked a larger P100 amplitude than pleasant food odors and no odors, which showed that the unpleasant odor environment promoted the rapid processing of facial expressions. Next, the interaction between odor environment and facial expressions occurred during the middle stage, and the fearful expression evoked a smaller VPP (vertex positive potential) amplitude than the happy and neutral expressions when exposed to the unpleasant food odor environment. This result indicates that unpleasant odor environment consumed fewer cognitive resources when judging fearful expression, showing the promoting effect of mood coherence effect. These findings provided evidence for how people chose odor environments to facilitate the recognition of facial expressions, and highlighted the advantages of unpleasant food odors in communicating emotional information across the olfactory and visual pathways.

An Evolutionarily Threat-Relevant Odor Strengthens Human Fear Memory.

Olfaction is an evolutionary ancient sense, but it remains unclear to what extent it can influence routine human behavior. We examined whether a threat-relevant predator odor (2-methyl-2-thiazoline) would contextually enhance the formation of human fear memory associations. Participants who learned to associate visual stimuli with electric shock in this predator odor context later showed stronger fear responses to the visual stimuli than participants who learned in an aversiveness-matched control odor context. This effect generalized to testing in another odor context, even after extinction training. Results of a separate experiment indicate that a possible biological mechanism for this effect may be increased cortisol levels in a predator odor context. These results suggest that innate olfactory processes can play an important role in human fear learning. Modulatory influences of odor contexts may partly explain the sometimes maladaptive persistence of human fear memory, e.g., in post-traumatic stress disorders.

Maternal odor shapes rapid face categorization in the infant brain.

To successfully interact with a rich and ambiguous visual environment, the human brain learns to differentiate visual stimuli and to produce the same response to subsets of these stimuli despite their physical difference. Although this visual categorization function is traditionally investigated from a unisensory perspective, its early development is inherently constrained by multisensory inputs. In particular, an early-maturing sensory system such as olfaction is ideally suited to support the immature visual system in infancy by providing stability and familiarity to a rapidly changing visual environment. Here, we test the hypothesis that rapid visual categorization of salient visual signals for the young infant brain, human faces, is shaped by another highly relevant human-related input from the olfactory system, the mother's body odor. We observe that a right-hemispheric neural signature of single-glance face categorization from natural images is significantly enhanced in the maternal versus a control odor context in individual 4-month-old infant brains. A lack of difference between odor conditions for the common brain response elicited by both face and non-face images rules out a mere enhancement of arousal or visual attention in the maternal odor context. These observations show that face-selective neural activity in infancy is mediated by the presence of a (maternal) body odor, providing strong support for multisensory inputs driving category acquisition in the developing human brain and having important implications for our understanding of human perceptual development.

Background odors affect behavior in a dot-probe task with emotionally expressive faces

Odors affect perception of social cues in visual environments. Although often underestimated, people use their sense of smell to guide approach or avoidance behavior in social contexts. However, underlying psychological mechanisms are not well known. Prior work suggested olfactory effects are due to increased attention or arousal, or depend on the congruency between olfactory and visual cues. Our aim was to assess how odors influence attentional processes using a dot-probe task with odor-congruent and odor-incongruent facial expressions (happy, disgusted and neutral expressions paired with pleasant odor, unpleasant odor and no-odor). In a preregistered analysis plan, we hypothesized either faster reaction times attributed to arousal from odors in general, or to faces that were emotionally congruent with the odors. We also hypothesized time-on-task effects specific to the odor compared to the control condition. Using Bayesian linear models, we found strong evidence that the faces were rated as more arousing and emotional in odor contexts. However, the dot-probe task did in fact not provide an effective cue to selective visual attention, and odors did not modulate overall attention to the faces. However, we found a time-on-task effect such that in the unpleasant odor condition, response times decreased over time, whereas in the no-odor and pleasant condition there was a slight increase in response times. We conclude that time-on-task effects is an interesting venue for odor-visual interaction research, and such effects might explain inconsistent findings in the prior research literature.

When to collect resting-state data: The influence of odor on post-task resting-state connectivity

The human brain networks at rest represent spontaneous activity that is highly correlated between different brain regions. Previous studies have shown that these resting-state networks are flexible and dynamic, and they can be affected by performance of different types of tasks. Moreover, it has been suggested that the re-activation of a task-related brain network during rest promotes learning and improves the expertise on that task. However, it is still unclear whether the presence of different sensory information in the on-task state affects functional connectivity in subsequent resting-state fMRI even though the perception of the sensory information did not induce significant behavioral effects. To clarify this issue, we compared pre- and post-task resting-state fMRI of two groups of participants performing the same task either with an odor context (ODOR group) or without an odor context (AIR group). Seed-based functional connectivity analyses were performed with orbitofrontal cortex, piriform cortex and working-memory core network as seeds. The results showed that an odor context presented during an encoding task induced significant changes in the functional connectivity only within the olfactory network of the post-task resting-state compared to the same post-task situation without previous odor context. No significant difference in functional connectivity were found for the working-memory core network. This evidence emphasizes how the sensory context, in which a task is performed, is relevant for understanding the observed changes of functional connectivity during rest.

The discriminative stimulus effects of nicotine & ethanol with two distinct olfactory contexts in male and female rats

Odor cues and interoceptive cues can combine in promoting drug seeking behavior. Drug discrimination methodology was combined with odor-context conditioning in 8 male and 8 female rats. One drug (nicotine or EtOH) plus odorant (peppermint or anise) compound functioned as setting the occasion for sessions of food-reinforced nose poke responses (i.e., the SD) that were maintained on a variable interval 30 s schedule (VI-30), whereas the opposite drug (EtOH or nicotine) plus odorant (anise or peppermint) compound predicted intermixed sessions of non-reinforcement of nose poking (i.e., the SΔ). During brief non-reinforcement tests conducted with each condition there was significantly greater responding under the SD drug plus odor compound compared to the SΔ drug plus odor compound. Discriminative control was evident and there was a sex by stimulus role interaction with greater SΔ responding in females. The odor contexts and drug contexts alone also sustained strong stimulus control but to a lesser extent compared to the full drug-odor compounds. These data suggest configural learning among drug and odor cues.