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Current Opinion in Neurobiology Oct 2022Volatile chemicals in the environment provide ethologically important information to many animals. However, how animals learn to use this information is only beginning... (Review)
Review
Volatile chemicals in the environment provide ethologically important information to many animals. However, how animals learn to use this information is only beginning to be understood. This review highlights recent experimental advances elucidating olfactory learning in rodents, ranging from adaptations to the environment to task-dependent refinement and multisensory associations. The broad range of phenomena, mechanisms, and brain areas involved demonstrate the complex and multifaceted nature of olfactory learning.
Topics: Animals; Brain; Conditioning, Classical; Learning; Smell
PubMed: 35998474
DOI: 10.1016/j.conb.2022.102623 -
Neuron Sep 2004The olfactory nervous systems of insects and mammals exhibit many similarities, suggesting that the mechanisms for olfactory learning may be shared. Neural correlates of... (Review)
Review
The olfactory nervous systems of insects and mammals exhibit many similarities, suggesting that the mechanisms for olfactory learning may be shared. Neural correlates of olfactory memory are distributed among many neurons within the olfactory nervous system. Perceptual olfactory learning may be mediated by alterations in the odorant receptive fields of second and/or third order olfactory neurons, and by increases in the coherency of activity among ensembles of second order neurons. Operant olfactory conditioning is associated with an increase in the coherent population activity of these neurons. Olfactory classical conditioning increases the odor responsiveness and synaptic activity of second and perhaps third order neurons. Operant and classical conditioning both produce an increased responsiveness to conditioned odors in neurons of the basolateral amygdala. Molecular genetic studies of olfactory learning in Drosophila have revealed numerous molecules that function within the third order olfactory neurons for normal olfactory learning.
Topics: Action Potentials; Animals; Humans; Learning; Smell; Synapses
PubMed: 15450158
DOI: 10.1016/j.neuron.2004.09.008 -
Neuron Apr 2023The coincidence between conditioned stimulus (CS) and unconditioned stimulus (US) is essential for associative learning; however, the mechanism regulating the duration...
The coincidence between conditioned stimulus (CS) and unconditioned stimulus (US) is essential for associative learning; however, the mechanism regulating the duration of this temporal window remains unclear. Here, we found that serotonin (5-HT) bi-directionally regulates the coincidence time window of olfactory learning in Drosophila and affects synaptic plasticity of Kenyon cells (KCs) in the mushroom body (MB). Utilizing GPCR-activation-based (GRAB) neurotransmitter sensors, we found that KC-released acetylcholine (ACh) activates a serotonergic dorsal paired medial (DPM) neuron, which in turn provides inhibitory feedback to KCs. Physiological stimuli induce spatially heterogeneous 5-HT signals, which proportionally gate the intrinsic coincidence time windows of different MB compartments. Artificially reducing or increasing the DPM neuron-released 5-HT shortens or prolongs the coincidence window, respectively. In a sequential trace conditioning paradigm, this serotonergic neuromodulation helps to bridge the CS-US temporal gap. Altogether, we report a model circuitry for perceiving the temporal coincidence and determining the causal relationship between environmental events.
Topics: Animals; Smell; Serotonin; Drosophila; Conditioning, Classical; Neurons; Mushroom Bodies
PubMed: 36706757
DOI: 10.1016/j.neuron.2022.12.034 -
Scientific Reports Mar 2021Olfactory learning and conditioning in the fruit fly is typically modelled by correlation-based associative synaptic plasticity. It was shown that the conditioning of an...
Olfactory learning and conditioning in the fruit fly is typically modelled by correlation-based associative synaptic plasticity. It was shown that the conditioning of an odor-evoked response by a shock depends on the connections from Kenyon cells (KC) to mushroom body output neurons (MBONs). Although on the behavioral level conditioning is recognized to be predictive, it remains unclear how MBONs form predictions of aversive or appetitive values (valences) of odors on the circuit level. We present behavioral experiments that are not well explained by associative plasticity between conditioned and unconditioned stimuli, and we suggest two alternative models for how predictions can be formed. In error-driven predictive plasticity, dopaminergic neurons (DANs) represent the error between the predictive odor value and the shock strength. In target-driven predictive plasticity, the DANs represent the target for the predictive MBON activity. Predictive plasticity in KC-to-MBON synapses can also explain trace-conditioning, the valence-dependent sign switch in plasticity, and the observed novelty-familiarity representation. The model offers a framework to dissect MBON circuits and interpret DAN activity during olfactory learning.
Topics: Animals; Avoidance Learning; Dopaminergic Neurons; Drosophila; Models, Biological; Mushroom Bodies; Neuronal Plasticity; Smell; Stochastic Processes; Synapses
PubMed: 33762640
DOI: 10.1038/s41598-021-85841-y -
The Journal of Neuroscience : the... Oct 2018Localizing the sources of stimuli is essential. Most organisms cannot eat, mate, or escape without knowing where the relevant stimuli originate. For many, if not most,... (Review)
Review
Localizing the sources of stimuli is essential. Most organisms cannot eat, mate, or escape without knowing where the relevant stimuli originate. For many, if not most, animals, olfaction plays an essential role in search. While microorganismal chemotaxis is relatively well understood, in larger animals the algorithms and mechanisms of olfactory search remain mysterious. In this symposium, we will present recent advances in our understanding of olfactory search in flies and rodents. Despite their different sizes and behaviors, both species must solve similar problems, including meeting the challenges of turbulent airflow, sampling the environment to optimize olfactory information, and incorporating odor information into broader navigational systems.
Topics: Algorithms; Animals; Environment; Humans; Memory; Odorants; Smell; Species Specificity
PubMed: 30381430
DOI: 10.1523/JNEUROSCI.1668-18.2018 -
Behavioral Neuroscience Oct 2021Learning associations between sensory stimuli and outcomes, and generalizing these associations to novel stimuli, are a fundamental feature of adaptive behavior. Given a...
Learning associations between sensory stimuli and outcomes, and generalizing these associations to novel stimuli, are a fundamental feature of adaptive behavior. Given a noisy olfactory world, stimulus generalization holds unique relevance for the olfactory system. Recent studies suggest that aversive outcomes induce wider generalization curves by modulating discrimination thresholds, but evidence for similar processes in olfaction does not exist. Here, we use a novel olfactory discrimination learning paradigm to address the question of how outcome valence impacts associative learning and generalization in humans. Subjects underwent discrimination learning, where they learned to associate odor mixtures with either aversive (shock) or neutral (air puff) outcomes. We find better olfactory learning for odors associated with aversive compared to neutral outcomes. We further show that generalization gradients are also modulated by outcome valence, with the shock group exhibiting a steeper gradient. Computational modeling revealed that differences in generalization are driven by a narrower excitatory gradient in the shock group, indicating more discriminatory responses. These findings provide novel evidence that olfactory learning and generalization are strongly affected by the valence of outcomes. This adaptive mechanism allows for behavioral flexibility in novel situations with related stimuli and with outcomes of different valences. Because odor stimuli differ considerably from one encounter to the next, adaptive generalization may be especially important in the olfactory system. (PsycInfo Database Record (c) 2021 APA, all rights reserved).
Topics: Conditioning, Classical; Discrimination Learning; Generalization, Psychological; Humans; Odorants; Smell
PubMed: 34197137
DOI: 10.1037/bne0000476 -
Learning & Memory (Cold Spring Harbor,... 2004Olfactory perceptual learning is a relatively long-term, learned increase in perceptual acuity, and has been described in both humans and animals. Data from recent... (Review)
Review
Olfactory perceptual learning is a relatively long-term, learned increase in perceptual acuity, and has been described in both humans and animals. Data from recent electrophysiological studies have indicated that olfactory perceptual learning may be correlated with changes in odorant receptive fields of neurons in the olfactory bulb and piriform cortex. These changes include enhanced representation of the molecular features of familiar odors by mitral cells in the olfactory bulb, and synthetic coding of multiple coincident odorant features into odor objects by cortical neurons. In this paper, data are reviewed that show the critical role of acetylcholine (Ach) in olfactory system function and plasticity, and cholinergic modulation of olfactory perceptual learning at both the behavioral and cortical level.
Topics: Acetylcholine; Animals; Cerebral Cortex; Humans; Learning; Neuronal Plasticity; Odorants; Olfactory Bulb; Smell
PubMed: 14747514
DOI: 10.1101/lm.66404 -
Current Biology : CB Feb 2015Sensory cues that predict reward or punishment are fundamental drivers of animal behavior. For example, attractive odors of palatable food or a potential mate predict... (Review)
Review
Sensory cues that predict reward or punishment are fundamental drivers of animal behavior. For example, attractive odors of palatable food or a potential mate predict reward, while aversive odors of pathogen-laced food or a predator predict punishment. Aversive and attractive odors can be detected by intermingled sensory neurons that express highly related olfactory receptors and display similar central projections. These findings raise basic questions of how innate odor valence is extracted from olfactory circuits, how such circuits are developmentally endowed and modulated by state, and how innate and learned odor responses are related. Here, we review odors, receptors and neural circuits associated with stimulus valence, discussing salient principles derived from studies on nematodes, insects and vertebrates. Understanding the organization of neural circuitry that mediates odor aversion and attraction will provide key insights into how the brain functions.
Topics: Aedes; Animals; Avoidance Learning; Behavior, Animal; Caenorhabditis elegans; Cues; Discrimination Learning; Drosophila; Mice; Models, Neurological; Olfactory Pathways; Olfactory Receptor Neurons; Smell
PubMed: 25649823
DOI: 10.1016/j.cub.2014.11.044 -
Neuron Apr 2011Studies using functional cellular imaging of living flies have identified six memory traces that form in the olfactory nervous system after conditioning with odors.... (Review)
Review
Studies using functional cellular imaging of living flies have identified six memory traces that form in the olfactory nervous system after conditioning with odors. These traces occur in distinct nodes of the olfactory nervous system, form and disappear across different windows of time, and are detected in the imaged neurons as increased calcium influx or synaptic release in response to the conditioned odor. Three traces form at or near acquisition and coexist with short-term behavioral memory. One trace forms with a delay after learning and coexists with intermediate-term behavioral memory. Two traces form many hours after acquisition and coexist with long-term behavioral memory. The transient memory traces may support behavior across the time windows of their existence. The experimental approaches for dissecting memory formation in the fly, ranging from the molecular to the systems, make it an ideal system for elucidating the logic by which the nervous system organizes and stores different temporal forms of memory.
Topics: Animals; Drosophila; Humans; Memory; Mushroom Bodies; Odorants; Olfactory Pathways; Olfactory Perception; Smell
PubMed: 21482352
DOI: 10.1016/j.neuron.2011.03.012 -
Journal of Visualized Experiments : JoVE Mar 2018Olfaction is the predominant sensory modality in mice and influences many important behaviors, including foraging, predator detection, mating, and parenting....
Olfaction is the predominant sensory modality in mice and influences many important behaviors, including foraging, predator detection, mating, and parenting. Importantly, mice can be trained to associate novel odors with specific behavioral responses to provide insight into olfactory circuit function. This protocol details the procedure for training mice on a Go/No-Go operant learning task. In this approach, mice are trained on hundreds of automated trials daily for 2-4 weeks and can then be tested on novel Go/No-Go odor pairs to assess olfactory discrimination, or be used for studies on how odor learning alters the structure or function of the olfactory circuit. Additionally, the mouse olfactory bulb (OB) features ongoing integration of adult-born neurons. Interestingly, olfactory learning increases both the survival and synaptic connections of these adult-born neurons. Therefore, this protocol can be combined with other biochemical, electrophysiological, and imaging techniques to study learning and activity-dependent factors that mediate neuronal survival and plasticity.
Topics: Animals; Discrimination Learning; Female; Male; Mice; Reproducibility of Results; Smell
PubMed: 29630042
DOI: 10.3791/57142