Olfactory Task Research Articles

Parkinson's Disease Affects Functional Connectivity within the Olfactory-Trigeminal Network.

Olfactory dysfunction (OD) is a frequent symptom of Parkinson's disease (PD) that appears years prior to diagnosis. Previous studies suggest that PD-related OD is different from non-parkinsonian forms of olfactory dysfunction (NPOD) as PD patients maintain trigeminal sensitivity as opposed to patients with NPOD who typically exhibit reduced trigeminal sensitivity. We hypothesize the presence of a specific alteration of functional connectivity between trigeminal and olfactory processing areas in PD. We aimed to assess potential differences in functional connectivity within the chemosensory network in 15 PD patients and compared them to 15 NPOD patients, and to 15 controls. Functional MRI scanning session included resting-state and task-related scans where participants carried out an olfactory and a trigeminal task. We compared functional connectivity, using a seed-based correlation approach, and brain network modularity of the chemosensory network. PD patients had impaired functional connectivity within the chemosensory network while no such changes were observed for NPOD patients. No group differences we found in modularity of the identified networks. Both patient groups exhibited impaired connectivity when executing an olfactory task, while network modularity was significantly weaker for PD patients than both other groups. When performing a trigeminal task, no changes were found for PD patients, but NPOD patients exhibited impaired connectivity. Conversely, PD patients exhibited a significantly higher network modularity than both other groups. In summary, the specific pattern of functional connectivity and chemosensory network recruitment in PD-related OD may explain distinct behavioral chemosensory features in PD when compared to NPOD patients and healthy controls.

Olfactory marker protein contributes to the evaluation of odour values by olfactory glomerular processing

Olfaction starts from olfactory receptor neurons (ORNs) that express olfactory marker protein (OMP). OMP deficit results in various behavioural phenotypes indicating olfactory dysfunction due to the impaired responses of ORNs. Recently, OMP was demonstrated to maintain strong olfaction by buffering olfactory cAMP signalling. However, the impact of OMP on olfaction behaviours, the assessment of which requires time to evaluate odour values, remains largely unexplained.Here, we examined the behaviour of heterozygous OMP+/GFP (HET) mice vs. homologous GFP-knock-in OMP-deficient OMP GFP/ GFP (KI) mice during the olfactory investigation of odours with different values. When a swab containing an organic odour was presented, both HET and KI mice swiftly approached and investigated the swab with gradual habituation over test sessions. However, when another similar odour was presented, KI mice investigated the new swab much less intensively than HET mice. Next, mice were placed in a chamber with an aversive odour source in one corner of a test chamber. KI mice more frequently approached the compartment containing the aversive odour source than HET mice. Finally, we trained mice to associate two odours with solutions by utilizing reward-penalty values. HET mice stayed close to the reward-associated odour, while KI mice initially approached the reward-associated odour, occasionally turned towards the penalty-associated odour source and eventually stayed in the reward-odour compartment. Histologically, c-Fos-expressing juxtaglomerular cells were fewer and more broadly distributed around glomeruli in KI mice than HET mice.In conclusion, OMP contributes to the evaluation of odour values by glomerular processing during an olfactory investigation task.

Differential Emergence and Stability of Sensory and Temporal Representations in Context-Specific Hippocampal Sequences

Hippocampal spiking sequences encode external stimuli and spatiotemporal intervals, linking sequential experiences in memory, but the dynamics controlling the emergence and stability of such diverse representations remain unclear. Using two-photon calcium imaging in CA1 while mice performed an olfactory working-memory task, we recorded stimulus-specific sequences of "odor-cells" encoding olfactory stimuli followed by "time-cells" encoding time points in the ensuing delay. Odor-cells were reliably activated and retained stable fields during changes in trial structure and across days. Time-cells exhibited sparse and dynamic fields that remapped in both cases. During task training, but not in untrained task exposure, time-cell ensembles increased in size, whereas odor-cell numbers remained stable. Over days, sequences drifted to new populations with cell activity progressively converging to a field and then diverging from it. Therefore, CA1 employs distinct regimes to encode external cues versus their variable temporal relationships, which may be necessary to construct maps of sequential experiences.

Context-dependent odor learning requires the anterior olfactory nucleus.

Learning to associate the context in which a stimulus occurs is an important aspect of animal learning. We propose that the association of an olfactory stimulus with its multisensory context is mediated by projections from ventral hippocampus (vHC) networks to the anterior olfactory nucleus (AON). Using a contextually cued olfactory discrimination task, rats were trained to associate 2 olfactory stimuli with different responses depending on visuospatial context. Temporary lesions of the AON or vHC impaired performance on this task. In contrast, such lesions did not impair performance on a noncontextual olfactory discrimination task. Moreover, vHC lesions also impaired performance on an analogous contextually cued texture discrimination task, whereas AON lesions affected only olfactory contextual associations. We describe a distinct role for the AON in olfactory processing and conclude that early olfactory networks such as the olfactory bulb and AON function as multimodal integration networks rather than processing olfactory signals exclusively. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

Smell-Based Memory Training: Evidence of Olfactory Learning and Transfer to the Visual Domain.

Human and non-human animal research converge to suggest that the sense of smell, olfaction, has a high level of plasticity and is intimately associated with visual-spatial orientation and memory encoding networks. We investigated whether olfactory memory (OM) training would lead to transfer to an untrained visual memory (VM) task, as well as untrained olfactory tasks. We devised a memory intervention to compare transfer effects generated by olfactory and non-olfactory (visual) memory training. Adult participants were randomly assigned to daily memory training for about 40 days with either olfactory or visual tasks that had a similar difficulty level. Results showed that while visual training did not produce transfer to the OM task, olfactory training produced transfer to the untrained VM task. Olfactory training also improved participants’ performance on odor discrimination and naming tasks, such that they reached the same performance level as a high-performing group of wine professionals. Our results indicate that the olfactory system is highly responsive to training, and we speculate that the sense of smell may facilitate transfer of learning to other sensory domains. Further research is however needed in order to replicate and extend our findings.

Collective olfactory search in a turbulent environment.

Finding the source of an odor dispersed by a turbulent flow is a vital task for many organisms. When many individuals concurrently perform the same olfactory search task, sharing information about other members' decisions can potentially boost the performance. But how much of this information is actually exploitable for the collective task? Here we show, in a model of a swarm of agents inspired by moth behavior, that there is an optimal way to blend the private information about odor and wind detections with the public information about other agents' heading direction. Our results suggest an efficient multiagent olfactory search algorithm that could prove useful in robotics, e.g., in the identification of sources of harmful volatile compounds.

Characterizing Olfactory Function in Children with Autism Spectrum Disorder and Children with Sensory Processing Dysfunction.

Abnormalities in olfactory function have been identified in a number of neurological and psychiatric disorders, including Parkinson’s disease and schizophrenia. However, little is known about olfactory function in autism spectrum disorder (ASD). The present study aims to assess the olfactory profiles of children with ASD, compared to an age- and sex-matched comparison group of typically developing children and a second clinical control group consisting of non-ASD children with sensory processing dysfunction (SPD). Participants completed a battery of sensory and behavioral assessments including olfactory tasks (Sniffin’ Sticks Threshold Test and self-reported valence ratings for two target odorants (phenylethyl alcohol and vanillin) and the University of Pennsylvania Smell Identification Test), and an autism evaluation (Autism Diagnostic Observation Schedule-2). Children with ASD showed intact odor detection with reduced odor identification ability. Poor odor identification was significantly correlated with autism symptom severity. Children with SPD demonstrated reduced odor detection and identification ability. These findings provide evidence for differential patterns of smell processing among ASD and non-ASD neurodevelopmental disorders. Future studies are needed to determine whether the association of impaired olfaction and increased autism symptoms is due to shared etiology.

The Basal Forebrain Modulates Neuronal Response in an Active Olfactory Discrimination Task.

Successful completion of sensory decision-making requires focusing on relevant stimuli, adequate signal/noise ratio for stimulus discrimination, and stimulus valence evaluation. Different brain regions are postulated to play a role in these computations; however, evidence suggests that sensory and decision-making circuits are required to interact through a common neuronal pathway to elicit a context-adequate behavioral response. Recently, the basal forebrain (BF) region has emerged as a good candidate, since its heterogeneous projecting neurons innervate most of the cortical mantle and sensory processing circuits modulating different aspects of the sensory decision-making process. Moreover, evidence indicates that the BF plays an important role in attention and in fast modulation of neuronal activity that enhance visual and olfactory sensory perception. Here, we study in awake mice the involvement of BF in initiation and completion of trials in a reward-driven olfactory detection task. Using tetrode recordings, we find that BF neurons (including cholinergics) are recruited during sensory discrimination, reward, and interestingly slightly before trial initiation in successful discrimination trials. The precue neuronal activity was correlated with animal performance, indicating that this circuit could play an important role in adaptive context-dependent behavioral responses.

The impact of learning on perceptual decisions and its implication for speed-accuracy tradeoffs

In standard models of perceptual decision-making, noisy sensory evidence is considered to be the primary source of choice errors and the accumulation of evidence needed to overcome this noise gives rise to speed-accuracy tradeoffs. Here, we investigated how the history of recent choices and their outcomes interact with these processes using a combination of theory and experiment. We found that the speed and accuracy of performance of rats on olfactory decision tasks could be best explained by a Bayesian model that combines reinforcement-based learning with accumulation of uncertain sensory evidence. This model predicted the specific pattern of trial history effects that were found in the data. The results suggest that learning is a critical factor contributing to speed-accuracy tradeoffs in decision-making, and that task history effects are not simply biases but rather the signatures of an optimal learning strategy.

Older, non-demented apolipoprotein ε4 carrier males show hyperactivation and structural differences in odor memory regions: a blood-oxygen-level-dependent and structural magnetic resonance imaging study

The current study sought to examine the interaction of sex and Apolipoprotein ε4 status on olfactory recognition memory within non-demented, older individuals. We separated 39 participants into groups based on ε4 status and sex. Each participant completed an olfactory memory recognition task during 2 functional magnetic resonance imaging scans and 1 structural scan. The ε4 carriers had greater functional recruitment of memory regions during false positives relative to ε4 non-carriers. During hits, the male ε4 carriers showed greater functional recruitment compared to female ε4 carriers. The ε4 carriers had larger bilateral putamen volumes relative to ε4 non-carriers. Neuroimaging data were significantly associated with Dementia Rating Scale scores solely in males. Results suggest differential olfactory memory processing in relation to sex and ε4 status. Male ε4 carriers in particular, demonstrated hyperactivation during recognition memory, which we suspect reflects neuronal compensation to maintain functional performance. Future studies should consider examining underlying mechanisms that contribute to these sex differences within ε4 carriers.

Lateralization of odor identification in right-handers

Background: Odor identification is related to odor naming, which is more of a verbal than an olfactory sensory task. Linguistic functions in right-handers are typically lateralized to the left hemisphere of the brain and the olfactory processing happens predominantly ipsilaterally to the stimulated side.Aims: Re-investigate side-related effect in healthy right-handed people with a larger sample size and investigate the influence of age or gender on the odor identification lateralization effect.Material and methods: The ‘Sniffin’ Sticks’ odor identification test on a single nostril (either left or right side) was conducted in four hundred and thirty-eight right-handed participants. Among those one hundred and ninety-nine participants were tested on the left-side nostril and two hundred and thirty-nine on the right-side nostril. They were divided into two groups based on the age (18 years) or sex, in the older group (18 years) and the younger group (18 years) we had subgroups based on the sex.Results: In adults (age >18 years), the left-nostril odor identification score was significantly higher than the right-nostril odor identification score (t256 = 2.21, p = .03), in the male participants, the left-nostril odor identification score was also significantly higher than the right-nostril odor identification score (t147 = 2.01, p = 0.04).Conclusions and significance: The present study found that the in adult group (age >18 years), the odor identification performed better on the left-side nostril than the right-side nostril compared to the younger group (age ≤18 years); The males performed better on the left-side nostril than the right-side nostril compared to the females. In the adults (age >18 years) group, the males subgroup played a more important role on the lateralization of odor identification. Gender and age seem to have a large influence on the lateralization of odor identification.

Transient Delay-Period Activity of Agranular Insular Cortex Controls Working Memory Maintenance in Learning Novel Tasks

Whether transient or sustained neuronal activity during the delay period underlies working memory (WM) has been debated. Here, we report that transient, but not sustained, delay-period activity in mouse anterior agranular insular cortex (aAIC) plays a dominant role in maintaining WM information during learning of novel olfactory tasks. By optogenetic screening over 12 brain regions, we found that suppressing aAIC activity markedly impaired olfactory WM maintenance during learning. Single-unit recording showed that odor-selective aAIC neurons with predominantly transient firing patterns encoded WM information. Both WM task performance and transient-neuron proportion were enhanced and reduced by activating and suppressing the delay-period activity of the projection from medial prefrontal cortex (mPFC) to aAIC. The ability of mice to resist delay-period distractors also correlated with an increased percentage of transient neurons. Therefore, transient, but not sustained, aAIC neuronal activity during the delay period is largely responsible for maintaining information while learning novel WM tasks.

Non-invasive recording from the human olfactory bulb

Current non-invasive neuroimaging methods can assess neural activity in all areas of the human brain but the olfactory bulb (OB). The OB has been suggested to fulfill a role comparable to that of V1 and the thalamus in the visual system and have been closely linked to a wide range of olfactory tasks and neuropathologies. Here we present a method for non-invasive recording of signals from the human OB with millisecond precision. We demonstrate that signals obtained via recordings from EEG electrodes at the nasal bridge represent responses from the human olfactory bulb - recordings we term Electrobulbogram (EBG). The EBG will aid future olfactory-related translational work but can also potentially be implemented as an everyday clinical tool to detect pathology-related changes in human central olfactory processing in neurodegenerative diseases. In conclusion, the EBG is localized to the OB, is reliable, and follows response patterns demonstrated in non-human animal models.

Prenatal fruit juice exposure enhances memory consolidation in male post-weanling Sprague-Dawley rats.

ObjectivesNutritional intake during gestation is known to impact health outcomes for progeny. Correlational evidence in humans suggests that increased fruit consumption of pregnant mothers enhances infant cognitive development. Moreover, wild-type Drosophila supplemented with a combination of orange and tomato juice showed robust enhancements in performance on an associative olfactory memory task. The current study aimed to experimentally test the effects of prenatal fruit juice exposure in a non-human, mammalian model of learning and memory.MethodsAcross three separate birth cohorts, pregnant rats were given access to diluted tomato and orange juice (N = 2 per cohort), with control rats (N = 2 per cohort) receiving only water, in addition to standard rodent chow, throughout the duration of gestation, ending at parturition. Following weaning, male offspring were tested for learning and memory in a spatial version of the circular water maze and an auditory-cued fear-conditioning task.ResultsAll pregnant rats increased fluid and food intake over the gestational period. Fruit juice-fed pregnant rats had increased fluid intake compared to control pregnant rats. When testing progeny, there were no effects of prenatal fruit juice on spatial learning, while it appeared to impair learning in fear conditioning relative to controls. However, we measured significant enhancements in both spatial memory and conditioned fear memory in the prenatal fruit-juice group compared to controls. Measures of vigilance, in response to the conditioned cue, were increased in prenatal fruit rats compared to controls, suggesting less generalized, and more adaptive, anxiety behaviours.DiscussionOur results corroborate the human and Drosophila findings of prenatal fruit effects on behaviour, specifically that prenatal fruit juice exposure may be beneficial for early-life memory consolidation in rats.

Roles of the medial prefrontal cortex, mediodorsal thalamus, and their combined circuit for performance of the odor span task in rats: analysis of memory capacity and foraging behavior.

Working memory (WM), the capacity for short-term storage of small quantities of information for immediate use, is thought to depend on activity within the prefrontal cortex. Recent evidence indicates that the prefrontal neuronal activity supporting WM is driven by thalamocortical connections arising in mediodorsal thalamus (mdThal). However, the role of these connections has not been studied using olfactory stimuli leaving open the question of whether this circuit extends to all sensory modalities. Additionally, manipulations of the mdThal in olfactory memory tasks have yielded mixed results. In the present experiment, we investigated the role of connections between the rat medial prefrontal cortex (mPFC) and mdThal in the odor span task (OST) using a pharmacological contralateral disconnection technique. Inactivation of either the mPFC or mdThal alone both significantly impaired memory performance in the OST, replicating previous findings with the mPFC and confirming that the mdThal plays an essential role in intact OST performance. Contralateral disconnection of the two structures impaired OST performance in support of the idea that the OST relies on mPFC-mdThal connections, but ipsilateral control infusions also impaired performance, complicating this interpretation. We also performed a detailed analysis of rats’ errors and foraging behavior and found a dissociation between mPFC and mdThal inactivation conditions. Inactivation of the mdThal and mPFC caused a significant reduction in the number of approaches rats made per odor, whereas only mdThal inactivation or mPFC-mdThal disconnection caused significant increases in choice latency. Our results confirm that the mdThal is necessary for performance of the OST and that it may critically interact with the mPFC to mediate OST performance. Additionally, we have provided evidence that the mPFC and mdThal play dissociable roles in mediating foraging behavior.

Fimbria-Fornix Volume Is Associated With Spatial Memory and Olfactory Identification in Humans.

White matter pathways that surround the hippocampus comprise its afferent and efferent connections, and are therefore crucial in mediating the function of the hippocampus. We recently demonstrated a role for the hippocampus in both spatial memory and olfactory identification in humans. In the current study, we focused our attention on the fimbria-fornix white matter bundle and investigated its relationship with spatial memory and olfactory identification. We administered a virtual navigation task and an olfactory identification task to 55 young healthy adults and measured the volume of the fimbria-fornix. We found that the volume of the right fimbria-fornix and its subdivisions is correlated with both navigational learning and olfactory identification in those who use hippocampus-based spatial memory strategies, and not in those who use caudate nucleus-based navigation strategies. These results are consistent with our recent finding that spatial memory and olfaction rely on similar neural networks and structures.

Honeybees fail to discriminate floral scents in a complex learning task after consuming a neonicotinoid pesticide.

ABSTRACTNeonicotinoids are pesticides used to protect crops but with known secondary influences at sublethal doses on bees. Honeybees use their sense of smell to identify the queen and nestmates, to signal danger and to distinguish flowers during foraging. Few behavioural studies to date have examined how neonicotinoid pesticides affect the ability of bees to distinguish odours. Here, we used a differential learning task to test how neonicotinoid exposure affects learning, memory and olfactory perception in foraging-age honeybees. Bees fed with thiamethoxam could not perform differential learning and could not distinguish odours during short- and long-term memory tests. Our data indicate that thiamethoxam directly impacts the cognitive processes involved in working memory required during differential olfactory learning. Using a combination of behavioural assays, we also identified that thiamethoxam has a direct impact on the olfactory perception of similar odours. Honeybees fed with other neonicotinoids (clothianidin, imidacloprid, dinotefuran) performed the differential learning task, but at a slower rate than the control. These bees could also distinguish the odours. Our data are the first to show that neonicotinoids have compound specific effects on the ability of bees to perform a complex olfactory learning task. Deficits in decision making caused by thiamethoxam exposure could mean that this is more harmful than other neonicotinoids, leading to inefficient foraging and a reduced ability to identify nestmates.

CREB in Mushroom Body Gates <i>Drosophila</i> Long-Term Memory

Long-term memory (LTM) requires learning-induced synthesis of new proteins allocated in specific neurons and synapses in a neural circuit. Not all learned information, however, becomes permanent memory. How the brain gates relevant information into LTM remains unclear. In Drosophila adults, a single training session in an olfactory aversive learning task is not sufficient to induce protein synthesis-dependent LTM. Instead, multiple spaced training sessions are required. Here, we report the surprising finding that a single training session induces the synthesis of new proteins in early α/β Kenyon cells of the mushroom body (MB), and output from these neurons inhibits LTM formation. CREBB expression, induced by spaced training, then appears to suppress this inhibitory effect. One training session can induce LTM formation when this inhibitory effect is relieved. We propose that learning-induced proteins and spaced training-induced CREBB protein act antagonistically to modulate neuron activity from early α/β MB neurons during LTM formation.

Hippocampal state transitions at the boundaries between trial epochs.

The hippocampus encodes distinct contexts with unique patterns of activity. Representational shifts with changes in context, referred to as remapping, have been extensively studied. However, less is known about transitions between representations. In this study, we leverage a large dataset of neuronal recordings taken while rats performed an olfactory memory task with a predictable temporal structure involving trials and intertrial intervals (ITIs), separated by salient boundaries at the trial start and trial end. We found that trial epochs were associated with stable hippocampal representations despite moment-to-moment variability in stimuli and behavior. Representations of trial and ITI epochs were far more distinct than spatial factors would predict and the transitions between the two were abrupt. The boundary was associated with a large spike in multiunit activity, with many individual cells specifically active at the start or end of each trial. Both epochs and boundaries were encoded by hippocampal populations, and these representations carried information on orthogonal axes readily identified using principal component analysis. We suggest that the hippocampus orthogonalizes representations of the trial and ITI epochs and the activity spike at trial boundaries might serve to drive hippocampal activity from one stable state to the other.

High beta rhythm amplitude in olfactory learning signs a well-consolidated and non-flexible behavioral state

Beta rhythm (15–30 Hz) is a major candidate underlying long-range communication in the brain. In olfactory tasks, beta activity is strongly modulated by learning but its condition of expression and the network(s) responsible for its generation are unclear. Here we analyzed the emergence of beta activity in local field potentials recorded from olfactory, sensorimotor and limbic structures of rats performing an olfactory task. Rats performed successively simple discrimination, rule transfer, memory recall tests and contingency reversal. Beta rhythm amplitude progressively increased over learning in most recorded areas. Beta amplitude reduced to baseline when new odors were introduced, but remained high during memory recall. Intra-session analysis showed that even expert rats required several trials to reach a good performance level, with beta rhythm amplitude increasing in parallel. Notably, at the beginning of the reversal task, beta amplitude remained high while performance was low and, in all tested animals, beta amplitude decreased before rats were able to learn the new contingencies. Connectivity analysis showed that beta activity was highly coherent between all structures where it was expressed. Overall, our results suggest that beta rhythm is expressed in a highly coherent network when context learning - including both odors and reward - is consolidated and signals behavioral inflexibility.