Odour Retrieval Processing in Mice: Cholinergic Modulation of Oscillatory Coupling in Olfactory Bulb-Piriform Networks

2021 ◽  
pp. 1-19
Author(s):  
Abdallah Ahnaou ◽  
Lucile Chave ◽  
Nikolay V. Manyakov ◽  
Wilhelmus H.I.M. Drinkenburg
Keyword(s):  
Olfactory Bulb ◽  
Piriform Cortex ◽  
Field Potential ◽  
Reference Memory ◽  
Valuable Insight ◽  
Olfactory Pathway ◽  
Cholinergic Modulation ◽  
Coupling Index ◽  
Phase Amplitude

<b><i>Background/Aims:</i></b> Olfactory dysfunction can provide valuable insight into early pathophysiological processes of brain disorders. Olfactory processing of chemosensory and odour sensitivity relies on segregating salient odours from background odours cues. Odour-evoked fast oscillations in the olfactory bulb (OB) are hypothesized to be an important index of odour quality coding. The present preclinical work aimed at better understanding connectivity associated with odour coding and behavioural odour discrimination. <b><i>Methods:</i></b> Network oscillations and functional connectivity (FC) were measured in C57BL/6 mice performing the olfactory associative odour learning (OL) test, using multichannel local field potential recordings in key olfactory networks. Cholinergic modulation of odour processing was investigated using the muscarinic antagonist scopolamine. <b><i>Results:</i></b> At the behavioural level, olfactory memory, which refers to the acquisition and recollection of a reference odour by reduced exploration time, was observed in animals that correctly learned the task. Significant decrease in mean investigation and retrieval time of the associated odour-food reward was observed between trials. At the network level, the associated odour during sniffing behaviour was associated with enhanced coherence in the β and γ frequency oscillations across the olfactory pathway, with marked changes observed between the OB and anterior piriform cortex (PC). The enhanced phase-amplitude cross-frequency coupling in the OB and the weak coupling index in the hippocampal CA1 suggests a role of the OB network in olfaction encoding and processing. Scopolamine impaired behavioural and FC underlying recall and retrieval of the associated odour. <b><i>Conclusion:</i></b> The results suggest that the acquisition and formation of odour reference memory rely primarily on FC at the OB-PC network and confirm the role of muscarinic receptors in olfactory retrieval processing.

Chemical Factors Determine Olfactory System Beta Oscillations in Waking Rats

2007 ◽  
Vol 98 (1) ◽  
pp. 394-404 ◽  
Author(s):  
Catherine A. Lowry ◽  
Leslie M. Kay
Keyword(s):  
Olfactory Bulb ◽  
Vapor Pressure ◽  
Vapor Phase ◽  
Local Field ◽  
Olfactory System ◽  
Piriform Cortex ◽  
Field Potential ◽  
Gamma Oscillations ◽  
Beta Oscillations ◽  
Phase Concentration

Recent studies have pointed to olfactory system beta oscillations of the local field potential (15–30 Hz) and their roles both in learning and as specific responses to predator odors. To describe odorant physical properties, resultant behavioral responses and changes in the central olfactory system that may induce these oscillations without associative learning, we tested rats with 26 monomolecular odorants spanning 6 log units of theoretical vapor pressure (estimate of relative vapor phase concentration) and 10 different odor mixtures. We found odorant vapor phase concentration to be inversely correlated with investigation time on the first presentation, after which investigation times were brief and not different across odorants. Analysis of local field potentials from the olfactory bulb and anterior piriform cortex shows that beta oscillations in waking rats occur specifically in response to the class of volatile organic compounds with vapor pressures of 1–120 mmHg. Beta oscillations develop over the first three to four presentations and are weakly present for some odorants in anesthetized rats. Gamma oscillations show a smaller effect that is not restricted to the same range of odorants. Olfactory bulb theta oscillations were also examined as a measure of effective afferent input strength, and the power of these oscillations did not vary systematically with vapor pressure, suggesting that it is not olfactory bulb drive strength that determines the presence of beta oscillations. Theta band coherence analysis shows that coupling strength between the olfactory bulb and piriform cortex increases linearly with vapor phase concentration, which may facilitate beta oscillations above a threshold.

scholarly journals Perturbation of in vivo neural activity following α-Synuclein seeding in the olfactory bulb

2020 ◽  
Author(s):  
Aishwarya S. Kulkarni ◽  
Maria del Mar Cortijo ◽  
Elizabeth R. Roberts ◽  
Tamara L. Suggs ◽  
Heather B. Stover ◽  
...  
Keyword(s):  
Olfactory Bulb ◽  
Neural Activity ◽  
Olfactory System ◽  
Piriform Cortex ◽  
Field Potential ◽  
Dopamine Neurons ◽  
Motor Deficits ◽  
Wild Type ◽  
Evoked Activity

AbstractBACKGROUNDParkinson’s disease (PD) neuropathology is characterized by intraneuronal protein aggregates composed of misfolded α-Synuclein (α-Syn), as well as degeneration of substantia nigra dopamine neurons. Deficits in olfactory perception and aggregation of α-Syn in the olfactory bulb (OB) are observed during early stages of PD, and have been associated with the PD prodrome, before onset of the classic motor deficits. α-Syn fibrils injected into the OB of mice cause progressive propagation of α-Syn pathology throughout the olfactory system and are coupled to olfactory perceptual deficits.OBJECTIVEWe hypothesized that accumulation of pathogenic α-Syn in the OB impairs neural activity in the olfactory system.METHODSTo address this, we monitored spontaneous and odor-evoked local field potential dynamics in awake wild type mice simultaneously in the OB and piriform cortex (PCX) one, two, and three months following injection of pathogenic preformed α-Syn fibrils in the OB.RESULTSWe detected α-Syn pathology in both the OB and PCX. We also observed that α-Syn fibril injections influenced odor-evoked activity in the OB. In particular, α-Syn fibril-injected mice displayed aberrantly high odor-evoked power in the beta spectral range. A similar change in activity was not detected in the PCX, despite high levels of α-Syn pathology.CONCLUSIONSTogether, this work provides evidence that synucleinopathy impacts in vivo neural activity in the olfactory system at the network-level.

scholarly journals Perturbation of in vivo Neural Activity Following α-Synuclein Seeding in the Olfactory Bulb

2020 ◽  
Vol 10 (4) ◽  
pp. 1411-1427
Author(s):  
Aishwarya S. Kulkarni ◽  
Maria del Mar Cortijo ◽  
Elizabeth R. Roberts ◽  
Tamara L. Suggs ◽  
Heather B. Stover ◽  
...  
Keyword(s):  
Olfactory Bulb ◽  
Neural Activity ◽  
Olfactory System ◽  
Piriform Cortex ◽  
Field Potential ◽  
Dopamine Neurons ◽  
Motor Deficits ◽  
Wild Type ◽  
Evoked Activity

Background: Parkinson’s disease (PD) neuropathology is characterized by intraneuronal protein aggregates composed of misfolded α-Synuclein (α-Syn), as well as degeneration of substantia nigra dopamine neurons. Deficits in olfactory perception and aggregation of α-Syn in the olfactory bulb (OB) are observed during early stages of PD, and have been associated with the PD prodrome, before onset of the classic motor deficits. α-Syn fibrils injected into the OB of mice cause progressive propagation of α-Syn pathology throughout the olfactory system and are coupled to olfactory perceptual deficits. Objective: We hypothesized that accumulation of pathogenic α-Syn in the OB impairs neural activity in the olfactory system. Methods: To address this, we monitored spontaneous and odor-evoked local field potential dynamics in awake wild type mice simultaneously in the OB and piriform cortex (PCX) one, two, and three months following injection of pathogenic preformed α-Syn fibrils in the OB. Results: We detected α-Syn pathology in both the OB and PCX. We also observed that α-Syn fibril injections influenced odor-evoked activity in the OB. In particular, α-Syn fibril-injected mice displayed aberrantly high odor-evoked power in the beta spectral range. A similar change in activity was not detected in the PCX, despite high levels of α-Syn pathology. Conclusion: Together, this work provides evidence that synucleinopathy impacts in vivo neural activity in the olfactory system at the network-level.

scholarly journals Thalamic olfaction: characterizing odor processing in the mediodorsal thalamus of the rat

2014 ◽  
Vol 111 (6) ◽  
pp. 1274-1285 ◽  
Author(s):  
Emmanuelle Courtiol ◽  
Donald A. Wilson
Keyword(s):  
Local Field ◽  
Local Field Potential ◽  
Piriform Cortex ◽  
Field Potential ◽  
Olfactory Perception ◽  
Olfactory Pathway ◽  
Odor Processing ◽  
State Dependent ◽  
Beta Frequency Band ◽  
Beta Frequency

Thalamus is a key crossroad structure involved in various functions relative to visual, auditory, gustatory, and somatosensory senses. Because of the specific organization of the olfactory pathway (i.e., no direct thalamic relay between sensory neurons and primary cortex), relatively little attention has been directed toward the thalamus in olfaction. However, an olfactory thalamus exists: the mediodorsal nucleus of the thalamus (MDT) receives input from various olfactory structures including the piriform cortex. How the MDT contributes to olfactory perception remains unanswered. The present study is a first step to gain insight into the function of the MDT in olfactory processing. Spontaneous and odor-evoked activities were recorded in both the MDT (single unit and local field potential) and the piriform cortex (local field potential) of urethane-anesthetized rats. We demonstrate that: 1) odorant presentation induces a conjoint, coherent emergence of beta-frequency-band oscillations in both the MDT and the piriform cortex; 2) 51% of MDT single units were odor-responsive with narrow-tuning characteristics across an odorant set, which included biological, monomolecular, and mixture stimuli. In fact, a majority of MDT units responded to only one odor within the set; 3) the MDT and the piriform cortex showed tightly related activities with, for example, nearly 20% of MDT firing in phase with piriform cortical beta-frequency oscillations; and 4) MDT-piriform cortex coherence was state-dependent with enhanced coupling during slow-wave activity. These data are discussed in the context of the hypothesized role of MDT in olfactory perception and attention.

scholarly journals Pharmacological manipulation of olfactory bulb granule cell excitability modulates beta oscillations: Testing a model

2017 ◽  
Author(s):  
Boleslaw L. Osinski ◽  
Alex Kim ◽  
Wenxi Xiao ◽  
Nisarg Mehta ◽  
Leslie M. Kay
Keyword(s):  
Olfactory Bulb ◽  
Granule Cell ◽  
Piriform Cortex ◽  
Field Potential ◽  
Gamma Oscillations ◽  
List Type ◽  
Muscarinic Agonist ◽  
Beta Oscillations ◽  
Cell Excitability ◽  
Beta Power

AbstractThe mammalian olfactory bulb (OB) generates gamma (40 – 100 Hz) and beta (15 – 30 Hz) oscillations of the local field potential (LFP). Gamma oscillations arise at the peak of inhalation supported by dendrodendritic interactions between glutamatergic mitral cells (MCs) and GABAergic granule cells (GCs). Beta oscillations occur in response to odorants in learning or odor sensitization paradigms, but their generation mechanism and function are still poorly understood. When centrifugal inputs to the OB are blocked, beta oscillations disappear, but gamma oscillations persist. Centrifugal input targets primarily GABAergic interneurons in the GC layer (GCL) and regulates GC excitability, which suggests a causal link between beta oscillations and GC excitability. Previous modeling work from our laboratory predicted that convergence of excitatory/inhibitory inputs onto MCs and centrifugal inputs onto GCs can increase GC excitability sufficiently to drive beta oscillations primarily through voltage dependent calcium channel (VDCC) mediated GABA release, independently of NMDA channels. We test this model by examining the influence of NMDA and muscarinic acetylcholine receptors on GC excitability and beta oscillations. Intrabulbar scopolamine (muscarinic antagonist) infusion decreased or completely suppressed odor-evoked beta in response to a strong stimulus, but increased beta power in response to a weak stimulus, as predicted by our model. Piriform cortex (PC) beta power was unchanged. Oxotremorine (muscarinic agonist) tended to suppress all oscillations, probably from over-inhibition. APV, an NMDA receptor antagonist, suppressed gamma oscillations selectively (in OB and PC), lending support to the model’s prediction that beta oscillations can be supported by VDCC mediated currents.New and Noteworthy:Olfactory bulb beta oscillations rely on granule cell excitability.Reducing granule cell excitability with scopolamine reduces high volatilityinduced beta power but increases low volatility-induced beta power.Piriform cortex beta oscillations maintain power when olfactory bulb beta power is low, and the system maintains beta band coherence.

scholarly journals Learning improves decoding of odor identity with phase-referenced oscillations in the olfactory bulb

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Justin Losacco ◽  
Daniel Ramirez-Gordillo ◽  
Jesse Gilmer ◽  
Diego Restrepo
Keyword(s):  
Olfactory Bulb ◽  
Field Potential ◽  
Brain Regions ◽  
Spike Timing ◽  
Potential Oscillations ◽  
Neuronal Ensembles ◽  
Beta Power ◽  
High Gamma ◽  
Theta Phase ◽  
Phase Amplitude

Local field potential oscillations reflect temporally coordinated neuronal ensembles—coupling distant brain regions, gating processing windows, and providing a reference for spike timing-based codes. In phase amplitude coupling (PAC), the amplitude of the envelope of a faster oscillation is larger within a phase window of a slower carrier wave. Here, we characterized PAC, and the related theta phase-referenced high gamma and beta power (PRP), in the olfactory bulb of mice learning to discriminate odorants. PAC changes throughout learning, and odorant-elicited changes in PRP increase for rewarded and decrease for unrewarded odorants. Contextual odorant identity (is the odorant rewarded?) can be decoded from peak PRP in animals proficient in odorant discrimination, but not in naïve mice. As the animal learns to discriminate the odorants the dimensionality of PRP decreases. Therefore, modulation of phase-referenced chunking of information in the course of learning plays a role in early sensory processing in olfaction.

scholarly journals Enhancing GABAergic signaling ameliorates aberrant gamma oscillations of olfactory bulb in AD mouse models

2021 ◽  
Vol 16 (1) ◽  
Author(s):  
Ming Chen ◽  
Yunan Chen ◽  
Qingwei Huo ◽  
Lei Wang ◽  
Shuyi Tan ◽  
...  
Keyword(s):  
T Cells ◽  
Olfactory Bulb ◽  
Field Potential ◽  
Gamma Oscillations ◽  
Synaptic Function ◽  
Gaba Uptake ◽  
Olfactory Behavior ◽  
Olfactory Pathway

Abstract Background Before the deposition of amyloid-beta plaques and the onset of learning memory deficits, patients with Alzheimer’s disease (AD) experience olfactory dysfunction, typified by a reduced ability to detect, discriminate, and identify odors. Rodent models of AD, such as the Tg2576 and APP/PS1 mice, also display impaired olfaction, accompanied by aberrant in vivo or in vitro gamma rhythms in the olfactory pathway. However, the mechanistic relationships between the electrophysiological, biochemical and behavioral phenomena remain unclear. Methods To address the above issues in AD models, we conducted in vivo measurement of local field potential (LFP) with a combination of in vitro electro-olfactogram (EOG), whole-cell patch and field recordings to evaluate oscillatory and synaptic function and pharmacological regulation in the olfactory pathway, particularly in the olfactory bulb (OB). Levels of protein involved in excitation and inhibition of the OB were investigated by western blotting and fluorescence staining, while behavioral studies assessed olfaction and memory function. Results LFP measurements demonstrated an increase in gamma oscillations in the OB accompanied by altered olfactory behavior in both APP/PS1 and 3xTg mice at 3–5 months old, i.e. an age before the onset of plaque formation. Fewer olfactory sensory neurons (OSNs) and a reduced EOG contributed to a decrease in the excitatory responses of M/T cells, suggesting a decreased ability of M/T cells to trigger interneuron GABA release indicated by altered paired-pulse ratio (PPR), a presynaptic parameter. Postsynaptically, there was a compensatory increase in levels of GABAAR α1 and β3 subunits and subsequent higher amplitude of inhibitory responses. Strikingly, the GABA uptake inhibitor tiagabine (TGB) ameliorated abnormal gamma oscillations and levels of GABAAR subunits, suggesting a potential therapeutic strategy for early AD symptoms. These findings reveal increased gamma oscillations in the OB as a core indicator prior to onset of AD and uncover mechanisms underlying aberrant gamma activity in the OB. Conclusions This study suggests that the concomitant dysfunction of both olfactory behavior and gamma oscillations have important implications for early AD diagnosis: in particular, awareness of aberrant GABAergic signaling mechanisms might both aid diagnosis and suggest therapeutic strategies for olfactory damage in AD.

scholarly journals 50 years of decoding olfaction

2018 ◽  
Vol 2 ◽  
pp. 239821281881749 ◽  
Author(s):  
Peter A Brennan
Keyword(s):  
Olfactory Bulb ◽  
Olfactory System ◽  
Piriform Cortex ◽  
Vomeronasal System ◽  
Main Olfactory Bulb ◽  
Late 20Th Century ◽  
Fundamental Insight ◽  
Main Olfactory System ◽  
G Protein Coupled

The identification, in the late 20th century, of unexpectedly large families of G-protein-coupled chemosensory receptors revolutionised our understanding of the olfactory system. The discovery that non-selective olfactory sensory neurons express a single olfactory receptor type and project to a specific glomerulus in the main olfactory bulb provided fundamental insight into the spatial pattern of odour representation in the main olfactory bulb. Studies using head-fixed awake mice and optogenetics have revealed the importance of the timing of glomerular input in relation to the sniff cycle and the role of piriform cortex in odour object recognition. What in the 1970s had appeared to be a relatively simple dichotomy between odour detection by the main olfactory system and pheromone detection by the vomeronasal system has been found to consist of multiple subsystems. These mediate innate responses to odours and pheromones and to substances as diverse as O2, volatile urinary constituents, peptides and proteins.

scholarly journals Basolateral amygdala to posterior piriform cortex connectivity ensures precision in learned odor threat

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Brett S. East ◽  
Gloria Fleming ◽  
Samantha Vervoordt ◽  
Prachi Shah ◽  
Regina M. Sullivan ◽  
...  
Keyword(s):  
Functional Connectivity ◽  
Stimulus Control ◽  
Local Field ◽  
Basolateral Amygdala ◽  
Piriform Cortex ◽  
Field Potential ◽  
Emotional States ◽  
Odor Perception ◽  
High Gamma

AbstractOdor perception can both evoke emotional states and be shaped by emotional or hedonic states. The amygdala complex plays an important role in recognition of, and response to, hedonically valenced stimuli, and has strong, reciprocal connectivity with the primary olfactory (piriform) cortex. Here, we used differential odor-threat conditioning in rats to test the role of basolateral amygdala (BLA) input to the piriform cortex in acquisition and expression of learned olfactory threat responses. Using local field potential recordings, we demonstrated that functional connectivity (high gamma band coherence) between the BLA and posterior piriform cortex (pPCX) is enhanced after differential threat conditioning. Optogenetic suppression of activity within the BLA prevents learned threat acquisition, as do lesions of the pPCX prior to threat conditioning (without inducing anosmia), suggesting that both regions are critical for acquisition of learned odor threat responses. However, optogenetic BLA suppression during testing did not impair threat response to the CS+ , but did induce generalization to the CS−. A similar loss of stimulus control and threat generalization was induced by selective optogenetic suppression of BLA input to pPCX. These results suggest an important role for amygdala-sensory cortical connectivity in shaping responses to threatening stimuli.

scholarly journals Network and synaptic mechanisms underlying high frequency oscillations in the rat and cat olfactory bulb under ketamine-xylazine anesthesia

2020 ◽  
Author(s):  
Władysław Średniawa ◽  
Jacek Wróbel ◽  
Ewa Kublik ◽  
Daniel Krzysztof Wójcik ◽  
Miles Adrian Whittington ◽  
...  
Keyword(s):  
Olfactory Bulb ◽  
High Frequency ◽  
Piriform Cortex ◽  
Field Potential ◽  
Gamma Oscillations ◽  
Synaptic Activity ◽  
Surgical Removal ◽  
Nasal Airflow ◽  
High Frequency Oscillations ◽  
Subcortical Regions

AbstractHigh frequency oscillations (HFO) are receiving increased attention for their role in health and disease. Ketamine-dependent HFO have been identified in cortical and subcortical regions in rodents, however, the mechanisms underlying their generation and whether they occur in higher mammals is unclear. Here, we show under ketamine-xylazine anesthesia, classical gamma oscillations diminish and a prominent > 80 Hz oscillation emerges in the olfactory bulb of rats and cats. In cats negligible HFO was observed in the thamalus and visual cortex indicating the OB was a suitable site for further investigation. Simultaneous local field potential and thermocouple recordings demonstrated HFO was dependent on nasal airflow. Silicon probe mapping studies spanning almost the entire dorsal ventral aspect of the OB revealed this rhythm was strongest in ventral areas of the bulb and associated with microcurrent sources about the mitral layer. Pharmacological microinfusion studies revealed HFO was dependent on excitatory-inhibitory synaptic activity, but not gap junctions. Finally, we showed HFO was preserved despite surgical removal of the piriform cortex. We conclude that ketamine-dependent HFO in the OB are driven by nasal airflow and local dendrodendritic interactions. The relevance of our findings to ketamine’s model of psychosis in awake state are also discussed.

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