Conditioned Odor Research Articles

Odours Influence Visually Induced Emotion: Behavior and Neuroimaging

The present study was conducted to investigate the influence of olfaction on subjective valence intensity ratings of visual presentations. Pictures of five different categories (baby, flower, erotic, fear and disgust) were presented each being associated with five different odour conditions [no odour, low and high concentrations of phenylethyl alcohol (positive odour) and low and high concentrations of hydrogen sulphide (negative odour)]. Study participants had to rate the emotional content of each picture with respect to valence and intensity while brain activities were recorded with a whole-cortex magnetoencephalograph (MEG). A significant interaction between odour condition and picture category with respect to rating performance was found. In particular, positive valence intensity ratings related to flowers were increased in positive and negative odour conditions. Negative valence intensity ratings related to disgusting pictures were also increased in positive and negative odour conditions. The only decrease was found in the baby category in the high concentration negative odour condition. No behavioural effects were found for the categories erotic and fear. Around 300 ms after stimulus onset odour-related brain activity effects were found for all picture categories. On the other hand, around 700 ms after stimulus onset odour-related brain activity effects occurred only in the flower, fear and disgust picture categories. We interpret that early information processing demonstrates more pronounced olfactory and visually induced emotion interaction than later information processing. Since the early time window more likely reflects subconscious information processing we interpret that interaction between olfaction and visually induced emotion mostly occurs below the level of consciousness. Later, rather conscious information processing, seems to be differently influenced by simultaneous olfaction depending on the kind of emotion elicited through the sense of vision.

An implicit measure of olfactory performance for non-human primates reveals aversive and pleasant odor conditioning

We have little understanding of how odorants are processed in neural networks of the primate brain. Because chemo-stimuli are harder to control than physical stimuli (e.g. vision, audition), such research was limited by the temporal resolution, accuracy, and reliability of olfactometers (odor producing machines). Recent advances were able to create olfactometers that overcome these limitations, allowing their use together with neuroimaging techniques in humans. From the behavioral point of view, olfaction research requires a behavioral measure that can be used to quantify olfactory performance. This becomes a real problem when working with animals, where, unlike humans, explicit measures are harder to obtain. Furthermore, because odorants are powerful primitive reinforcers, such implicit measures can be beneficial to use in learning paradigms. Here we describe an olfactometer suitable for use in non-human primates, and an end-port design that allows the accurate measure of real-time respiratory modulations that are elicited in response to odor presentation. We demonstrate that this implicit measure is differentially modulated when experiencing pleasant or aversive odors. We then present an experimental paradigm in which monkeys learn to associate tones with odors, and show that the time delay from the conditioned stimuli to the next breath can be used to measure learning and memory expression in this paradigm. Using this construct, we reveal olfactory performance during acquisition and extinction of odor conditioning. These techniques can be used in electrophysiological recordings from relevant brain areas to shed light on neural networks involved in odor processing and reinforcement-learning.

Investigation of interactions between texture and ortho- and retronasal olfactory stimuli using psychophysical and electrophysiological approaches

Flavor is a result of the complex combination of olfactory, gustatory and trigeminal sensations perceived during oral processing of foods, including thermal, painful, tactile and/or kinesthetic effects. Aim of this study was to better understand interactions between synchronous tactile (texture) and olfactory (odor) sensations, using a psychophysical and an electrophysiological approach. Texture stimuli were aliquots of lean milk and thickened lean milk. A butter aroma was presented either orthonasally or retronasally after oral processing and before swallowing the oral stimulus or in the absence of an oral stimulus. Eighteen subjects (11 women, 7 men, mean age 24 years), naïve to the expected effects, rated both odor and texture intensity of each stimulus. Event-related potentials (ERP) were obtained from five recording positions. For the psychophysical data, the presence of an oral stimulus increased odor intensity, irrespective of odor presentation route. For the electrophysiological data, both early and late chemosensory ERPs were affected by odor conditions, texture conditions, and their respective interaction. In conclusion: (1) perceptual interactions occurred between food texture and odor, with cross-modal interactions being found for both orthonasal and retronasal odor administration, and (2) these interactions between texture and odor occur at both primary-sensory and cognitive evaluative levels of stimulus processing. The temporal dimension plays then a critical role in the investigation of odor–texture interactions.

Processing of disgusted faces is facilitated by odor primes: A functional MRI study

Facilitation of emotional face recognition is an established phenomenon for audiovisual crossmodal stimulation, but not for other sensory modalities. The present study used a crossmodal priming task to identify brain systems controlling olfactory–visual interactions during emotion processing. BOLD fMRI was acquired for 44 healthy subjects during an emotional face discrimination task preceded by an emotionally valenced odorant. Behavioral performance showed that recognition of disgusted faces was improved by the presentation of an olfactory stimulus irrespective of its emotional valence. No such facilitation was seen for other facial expressions. The neuroimaging data showed a selective default network responsivity to emotional faces which was modulated by odor condition. Among disgust faces, hypoactivations during trials preceded by odorants indicated the presence of priming effects. Consistent with studies investigating the brain systems associated with audiovisual emotional integration, activity modulations in clusters in fusiform gyrus, middle frontal and middle cingulate gyrus corresponded to the observed behavioral facilitation. Our study further shows modulation of signal in the anterior insula during trials combining negatively valenced odor and disgusted faces, suggesting a modality-specific mechanism for integration of the disgust response and olfaction. These results indicate the presence of a central network with modality-specific and -unspecific components modulating emotional face recognition.

Flavor preference learning increases olfactory and gustatory convergence onto single neurons in the basolateral amygdala but not in the insular cortex in rats.

The basolateral amygdala (BLA) and the insular cortex (IC) represent two major areas for odor-taste associations, i.e. flavor integration. This learning may require the development of convergent odor and taste neuronal activation allowing the memory representation of such association. Yet identification of neurons that respond to such coincident input and the effect of flavor experience on odor-taste convergence remain unclear. In the present study we used the compartmental analysis of temporal activity using fluorescence in situ hybridization for Arc (catFISH) to visualize odor-taste convergence onto single neurons in the BLA and in the IC to assess the number of cells that were co-activated by both stimuli after odor-taste association. We used a sucrose conditioned odor preference as a flavor experience in rats, in which 9 odor-sucrose pairings induce a reliable odor-taste association. The results show that flavor experience induced a four-fold increase in the percentage of cells activated by both taste and odor stimulations in the BLA, but not in the IC. Because conditioned odor preference did not modify the number of cells responding selectively to one stimulus, this greater odor-taste convergence into individual BLA neurons suggests the recruitment of a neuronal population that can be activated by both odor and taste only after the association. We conclude that the development of convergent activation in amygdala neurons after odor-taste associative learning may provide a cellular basis of flavor memory.

Reward sensitivity for a palatable food reward peaks during pubertal developmental in rats

Puberty is a critical period for the initiation of drug use and abuse. Because early drug use onset often accounts for a more severe progression of addiction, it is of importance to understand the underlying mechanisms and neurodevelopmental changes during puberty that are contributing to enhanced reward processing in teenagers. The present study investigated the progression of reward sensitivity toward a natural food reward over the whole course of adolescence in male rats (postnatal days 30–90) by monitoring consummatory, motivational behavior and neurobiological correlates of reward. Using a limited-free intake paradigm, consumption of sweetened condensed milk (SCM) was measured repeatedly in adolescent and adult rats. Additionally, early- and mid-pubertal animals were tested in Progressive Ratio responding for SCM and c-fos protein expression in reward-associated brain structures was examined after odor conditioning for SCM. We found a transient increase in SCM consumption and motivational incentive for SCM during puberty. This increased reward sensitivity was most pronounced around mid-puberty. The behavioral findings are paralleled by enhanced c-fos staining in reward-related structures revealing an intensified neuronal response after reward-cue presentation, distinctive for pubertal animals. Taken together, these data indicate an increase in reward sensitivity during adolescence accompanied by enhanced responsiveness of reward-associated brain structures to incentive stimuli, and it seems that both is strongly pronounced around mid-puberty. Therefore, higher reward sensitivity during pubertal maturation might contribute to the enhanced vulnerability of teenagers for the initiation of experimental drug use.

Is Liposuction with Shaving an Effective Treatment for Bromhidrosis

Background: Bromhidrosis is a troublesome problem that includes unpleasant odor and the occasional staining of clothing. Bromhidrosis patients are known to have more apocrine sweat glands than normal adults. Aim and Objectives: This study was conducted to evaluate the effectiveness of treating axillary bromhidrosis by subcutaneous liposuction with shaving according to histological examination of apocrine glands. Materials and Methods: From January of 2007 through December of 2007, 6 patients underwent subcutaneous liposuction with shaving for bromhidrosis. Pre- and post-operative skin samples were collected and histologically examined to evaluate the number of apocrine sweat glands. The wound and odor conditions were followed up clinically. Results: The average number of apocrine glands is obviously decreased from 46.83 to 2.33 after the operation. All six patients were satisfied with the clinical results of the operation. Conclusion: The operation decreased the number of apocrine glands found under histologic examination and the unpleasant odor improved clinically. Our study found subcutaneous liposuction with shaving an effective treatment for bromhidrosis.

Enhancement of spatial learning by predator odor in mice: Involvement of amygdala and hippocampus

Olfaction has particular links with learning and memory compared with other sensory cues, due to the interrelations between their neural circuitry. The present study deals with the effects of a putative stressor (i.e. a predator odor) on visuo-spatial learning in mice. Firstly, the results show that a predator odor spread during the Morris water maze task led to learning enhancement. In addition, a stereotaxic approach was used to investigate the involvement of the amygdala in this hippocampus-dependent type of learning. Thus, the performance of mice in visuo-spatial learning under predator odor conditions was dramatically reduced by an ibotenate bilateral amygdala lesion. The involvement of the amygdala was confirmed by a reduced expression of c-fos in the CA1 hippocampus of amygdala-lesioned mice at the end of the learning procedure. Mild exposure to a predator odor during hippocampus-dependent learning therefore leads to an enhancement of performance through the co-activation of the amygdala, probably by a stress mediated mechanism.

Social Facilitation of Long-Lasting Memory Retrieval in Drosophila

Recent studies demonstrate that social interactions can have a profound influence on Drosophila melanogaster behavior and cuticular pheromone patterns. Olfactory memory performance has mostly been investigated in groups, and previous studies have reported that grouped flies do not interact with each other and behave in the same way as individual flies during short-term memory retrieval. However, the influence of social effects on the two known forms of Drosophila long-lasting associative memory, anesthesia-resistant memory (ARM) and long-term memory (LTM), has never been reported. We show here that ARM is displayed by individual flies but is socially facilitated; flies trained for ARM interact within a group to improve their conditioned performance. In contrast, testing shows LTM improvement in individual flies rather than in a group. We show that the social facilitation of ARM during group testing is independent of the social context of training and does not involve nonspecific aggregation. Furthermore, we demonstrate that social interactions facilitate ARM retrieval. We also show that social interactions necessary for this facilitation are specifically generated by trained flies: when single flies trained for ARM are mixed with groups of naive flies, they display poor retrieval, whereas mixing with groups trained either for ARM or LTM enhances performance.

Influence de stimuli olfactifs dans une tâche d’évaluation hédonique de couleurs : les yeux voient ce que le nez sent

<titre>Résumé</titre> Ce travail s’intéresse à l’influence d’un couplage olfaction vision dans une tâche d’évaluation hédonique de pastilles de couleur. Les effets perceptifs des couleurs sur la perception des odeurs sont déjà connus. Toutefois ce travail se focalise sur l’effet intermodal inverse, du système olfactif sur le système visuel. Deux pré-expériences nous ont permis de sélectionner six couleurs (3 agréables/3 désagréables) et deux odeurs (1 agréable/1désagréable). Dans l’expérience, ces couleurs sont évaluées couplées à trois conditions odorantes (compatible/sans odeur/incompatible). Les résultats de la tâche d’évaluation des couleurs en condition odorante montrent un effet du facteur couleur ainsi qu’un effet d’interaction entre le facteur couleur et la condition de couplage olfactif. Les résultats sont discutés en faveur d’une approche de la perception considérée comme un simulateur intermodal.

Cat odor causes long-lasting contextual fear conditioning and increased pituitary-adrenal activation, without modifying anxiety

A single exposure to a cat or cat odors has been reported by some groups to induce contextual and auditory fear conditioning and long-lasting changes in anxiety-like behaviour, but there is no evidence for parallel changes in biological stress markers. In the present study we demonstrated in male rats that exposure to a novel environment containing a cloth impregnated with cat fur odor resulted in avoidance of the odor, lower levels of activity and higher pituitary-adrenal (PA) response as compared to those exposed to the novel environment containing a clean cloth, suggesting increased levels of stress in the former animals. When re-exposed 9 days later to the same environment with a clean cloth, previously cat fur exposed rats again showed avoidance of the cloth area and lower levels of activity, suggesting development of contextual fear conditioning, which again was associated with a higher PA activation. In contrast, unaltered both anxiety-like behaviour and PA responsiveness to an elevated plus-maze were found 7 days after cat odor exposure. It is concluded that: (i) PA activation is able to reflect both the stressful properties of cat fur odor and odor-induced contextual fear conditioning; (ii) development of cat odor-induced contextual fear conditioning is independent of the induction of long-lasting changes in anxiety-like behaviour; and (iii) greater PA activation during exposure to the odor context is not explained by non-specific sensitization of the PA axis caused by previous exposure to cat fur odor.

Olfactory learning in the rat immediately after birth: Unique salience of first odors.

An infant rat's chance of survival is increased when it remains close to the nest. Early olfactory learning supports such adaptive behavior. Previous experiments indicated that non-associative odor exposure immediately after birth promoted later attachment to a similarly scented artificial nipple. The goal of the current experiments was to extend these findings on olfactory learning in the hours after birth by: exposing pups to more than one odor exposure (Experiment 1), dissecting the role of timing versus order of odor exposure (Experiment 2), testing the odor specificity of these effects (Experiments 3 and 4), and evaluating associative odor conditioning soon after birth (Experiment 5). Without explicit prior odor experience, pups only hours old do not respond much to a novel odor. Prior non-associative odor experience increases later motor activity to that same odor and to novel odors. Furthermore, these findings may be specific to certain amodal dimensions of the (in our case) lemon odor exposure. Single odor non-associative and associative conditioning was equally effective immediately after birth and during the third postnatal hour. Nevertheless, pups given two mere odor exposures responded to the first one more than the second at test, regardless of whether the exposures began immediately or 2 hr after birth. Possible mechanisms for these findings concerning early olfactory learning are discussed.

Disruption of neuroendocrine stress responses to acute ferret odor by medial, but not central amygdala lesions in rats

Investigations of the neural pathways associated with responses to predators have implicated the medial amygdala (MeA) as an important region involved in defensive behaviors. To our knowledge, however, the involvement of the MeA in neuroendocrine responses to predator odor exposure has not been investigated. Therefore, the present study examined the effects of MeA disruption in rats exposed to ferret or control odor on hypothalamo-pituitary-adrenocortical (HPA) axis activation. Bilateral lesions of the MeA were made in Sprague–Dawley rats with the neurotoxin ibotenic acid (10 μg/μl; 0.3 μl / side). As a control for regional specificity, additional groups of rats were given lesions in the central amygdala (CeA). One week after recovery, the rats were exposed to ferret or strawberry control towels in small cages to examine HPA axis responses as determined by plasma corticosterone and adrenocorticotropin hormone (ACTH) levels. Rats with complete bilateral MeA but not CeA lesions displayed significantly less corticosterone and ACTH release compared to sham-operated control rats only in the ferret odor conditions. These results suggest that the MeA is an important structure involved in the HPA axis responses to predator odors, in support of previous studies investigating behavioral responses under similar conditions.

A gender difference related to the effect of a background odor: a magnetoencephalographic study

We measured brain activities with a whole head magnetoencephalograph (MEG) to investigate the influence of a background odor on alphabetical encoding of words in 20 healthy volunteers (10 females). Odor stimulation and control air stimulation were both accomplished with a computer-controlled olfactometer by providing permanent stimulation conditions. Behavioral data revealed significantly prolonged reaction times in men under the influence of phenylethyl alcohol (PEA) compared to the control condition. Women did not show a change in reaction time during stimulation with PEA. A comparison of men and women revealed significantly shorter reaction times in women for both the odor conditions, as well as for the control condition. Analysis of performance accuracy showed no significant differences between the odor and the control condition within and across gender. Analysis of grand averaged, event-related fields and localization of the underlying equivalent current dipoles revealed higher dipole strength in the odor, compared to the control condition in the right hemisphere, over the temporo-parietal brain areas, in the time range between 200 and 500 ms after word-onset only in male subjects. Within this time range, the gender-specific effect is interpreted to reflect odor-related modulation of word processing. The findings suggest gender-specific processing strategies in the present task with implications for differences in hemispheric laterality.

Unconscious odour conditioning 25 years later: Revisiting and extending ‘Kirk-Smith, Van Toller and Dodd’

The pioneering work by Kirk-Smith, Van Toller, and Dodd [Kirk-Smith, M. D., Van Toller, C., & Dodd, G. H. (1983). Unconscious odour conditioning in human subjects. Biological Psychology, 17, 221–231], established that an unnoticed odorant paired with an emotionally meaningful task can influence mood and attitudes when the odorant alone is re-encountered subsequently. This study was particularly important in highlighting unconscious odour learning processes as they may happen in everyday life. However, it was severely criticized by Black and Smith [Black, S. L., & Smith, D. G. (1994). Has odor conditioning been demonstrated? A critique of “Unconscious odour conditioning in human subjects”. Biological Psychology, 37, 265–267] on methodological grounds. In the present paper, we replicated and extended Kirk-Smith et al.’s investigation taking into account Black and Smith’s criticisms and carrying out additional controls to improve the validity of the study. The results confirm the initial findings of Kirk-Smith and colleagues by demonstrating the effectiveness of olfactory stimuli in inducing conditioned hedonic reactions even when presented below the level of awareness.

Long‐term effects of infant learning on adult conditioned odor aversion are determined by the last preweaning experience

We recently showed that odorizing mother's nipples from birth to weaning attenuated adult conditioned odor aversion (COA). The present study evaluated whether shorter durations of preweaning olfactory experiences could induce similar long-term effects. We first showed that late preweaning odorization (PN13-PN25) impaired adult COA similarly to odorization from birth to weaning (PN0-PN25) whereas early odorization (PN0-PN12) had no effect on adult COA. As early odorization was followed by an odorless suckling period, we evaluated whether this odorless suckling could have interfered with early associative learning. We therefore weaned the animals either immediately after early odorization or 7 days later. Early odorization (PN0-PN18) followed by late odorless suckling (PN19-PN25) had no effect on adult COA. However, pups with early odorization (PN0-PN18) but without late odorless suckling (weaned at PN18) showed attenuated COA. These results support the hypothesis that interference between early and late preweaning experiences with the mother determines the long-term impact on adult COA.

Critical role of insular cortex in taste but not odour aversion memory

Conditioned odour aversion (COA) and conditioned taste aversion (CTA) result from the association of a novel odour or a novel taste with delayed visceral illness. The insular cortex (IC) is crucial for CTA memory, and the present experiments sought to determine whether the IC is required for the formation and the retrieval of COA memory as it is for CTA. We first demonstrated that ingested odour is as effective as taste for single-trial aversion learning in rats conditioned in their home cage. COA, like CTA, tolerates long intervals between the ingested stimuli and the illness and is long-lasting. Transient inactivation of the IC during acquisition spared COA whereas it greatly impaired CTA. Similarly, blockade of protein synthesis in IC did not affect COA but prevented CTA consolidation. Moreover, IC inactivation before retrieval tests did not interfere with COA memory expression when performed either 2 days (recent memory) or 36 days after acquisition (remote memory). Similar IC inactivation impaired the retrieval of either recent or remote CTA memory. Altogether these findings indicate that the IC is not necessary for aversive odour memory whereas it is essential for acquisition, consolidation and retrieval of aversive taste memory. We propose that the chemosensory stimulations modulate IC recruitment during the formation and the retrieval of food aversive memory.

Olfactory learning and memory in the bumblebee Bombus occidentalis

In many respects, the behavior of bumblebees is similar to that of the closely related honeybees, a long-standing model system for learning and memory research. Living in smaller and less regulated colonies, bumblebees are physiologically more robust and thus have advantages in particular for indoor experiments. Here, we report results on Pavlovian odor conditioning of bumblebees using the proboscis extension reflex (PER) that has been successfully used in honeybee learning research. We examine the effect of age, body size, and experience on learning and memory performance. We find that age does not affect learning and memory ability, while body size positively correlates with memory performance. Foraging experience seems not to be necessary for learning to occur, but it may contribute to learning performance as bumblebees with more foraging experience on average were better learners. The PER represents a reliable tool for learning and memory research in bumblebees and allows examining interspecific similarities and differences of honeybee and bumblebee behavior, which we discuss in the context of social organization.

The basolateral amygdala is necessary for the encoding and the expression of odor memory

Conditioned odor avoidance (COA) results from the association between a novel odor and a delayed visceral illness. The present experiments investigated the role of the basolateral amygdala (BLA) in acquisition and retrieval of COA memory. To address this, we used the GABA(A) agonist muscimol to temporarily inactivate the BLA during COA acquisition or expression. BLA inactivation before odor-malaise pairing greatly impaired COA tested 3 d later. In contrast, muscimol microinfusion between odor and malaise spared retention. Moreover, inactivation of the BLA before pre-exposure to the odor prevented latent inhibition of COA. This suggests that neural activity in the BLA is essential for the formation of odor representation. BLA inactivation before the retrieval test also blocked COA memory expression when performed either 3 d (recent memory) or 28 d (remote memory) after acquisition. This effect was transitory as muscimol-treated animals were not different from controls during the subsequent extinction tests. Moreover, muscimol infusion in the BLA neither affected olfactory perception nor avoidance behavior, and it did not induce a state-dependent learning. Altogether, these findings suggest that neural activity in the BLA is required for the encoding and the retrieval of odor memory. Moreover, the BLA seems to play a permanent role in the expression of COA.

A phosphodiesterase inhibitor, cilomilast, enhances cAMP activity to restore conditioned odor preference memory after serotonergic depletion in the neonate rat

In various learning and memory models, preventing the breakdown of cyclic adenosine monophosphate (cAMP) by using a phosphodiesterase (PDE) inhibitor promotes memory. In the rat pup odor preference learning model serotonin, acting through 5-HT 2A/C receptors, has been shown to influence cAMP levels in the olfactory bulb initiated by β-adrenoceptor activation, as also seen in the neocortex. Since depletion of olfactory bulb serotonin prevents learning in the rat pup odor preference model, we ask whether a PDE inhibitor could restore that learning and also examined the influence of these manipulations on the temporal bulbar cAMP signal associated with successful learning. In this study, we found that a PDE4 inhibitor overcame learning deficits seen 24 h after a 10 min training trial on postnatal day 6 using the β-adrenoceptor agonist, isoproterenol as the unconditioned stimulus. We found in a previous study, that use of a PDE4 inhibitor during learning in normal pups extended memory to more than 48 h. However, in the present study the PDE4 treatment did not enable this memory extension in 5-HT depleted pups. An increase in the cAMP signal at the end of the 10 min training trial occurred in the presence of the PDE4 inhibitor. Such a cAMP increase has been associated with successful learning and is normally absent with bulbar 5-HT depletion. These results suggest PDE4 inhibitors may be useful therapeutically in disorders associated with reductions in serotonergic function.