Cortical feedback and gating in odor discrimination and generalization

A central question in neuroscience is how context changes perception. In the olfactory system, for example, experiments show that task demands can drive divergence and convergence of cortical odor responses, likely underpinning olfactory discrimination and generalization. Here, we propose a simple statistical mechanism for this effect based on unstructured feedback from the central brain to the olfactory bulb, which represents the context associated with an odor, and sufficiently selective cortical gating of sensory inputs. Strikingly, the model predicts that both convergence and divergence of cortical odor patterns should increase when odors are initially more similar, an effect reported in recent experiments. The theory in turn predicts reversals of these trends following experimental manipulations and in neurological conditions that increase cortical excitability.

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Cortical feedback and gating in olfactory pattern completion and separation

10.1101/2020.11.05.370494 ◽

2020 ◽

Author(s):

Gaia Tavoni ◽

David E. Chen Kersen ◽

Vijay Balasubramanian

Keyword(s):

Olfactory System ◽

Cortical Excitability ◽

Task Demands ◽

Pattern Separation ◽

Central Question ◽

Sensory Stimuli ◽

Sensory Inputs ◽

Central Brain ◽

Statistical Mechanism ◽

Neurological Conditions

A central question in neuroscience is how context changes perception of sensory stimuli. In the olfactory system, for example, experiments show that task demands can drive merging and separation of cortical odor responses, which underpin olfactory generalization and discrimination. Here, we propose a simple statistical mechanism for this effect, based on unstructured feedback from the central brain to the olfactory bulb, representing the context associated with an odor, and sufficiently selective cortical gating of sensory inputs. Strikingly, the model predicts that both pattern separation and completion should increase when odors are initially more similar, an effect reported in recent experiments. The theory predicts reversals of these trends following experimental manipulations and neurological conditions such as Alzheimer’s disease that increase cortical excitability.

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Extinction reverses olfactory fear-conditioned increases in neuron number and glomerular size

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1505068112 ◽

2015 ◽

Vol 112 (41) ◽

pp. 12846-12851 ◽

Cited By ~ 24

Author(s):

Filomene G. Morrison ◽

Brian G. Dias ◽

Kerry J. Ressler

Keyword(s):

Olfactory Bulb ◽

Learning And Memory ◽

Olfactory Epithelium ◽

Olfactory System ◽

Structural Changes ◽

Freezing Behavior ◽

Extinction Training ◽

Odor Stimulus ◽

Main Olfactory Epithelium ◽

Odor Learning

Although much work has investigated the contribution of brain regions such as the amygdala, hippocampus, and prefrontal cortex to the processing of fear learning and memory, fewer studies have examined the role of sensory systems, in particular the olfactory system, in the detection and perception of cues involved in learning and memory. The primary sensory receptive field maps of the olfactory system are exquisitely organized and respond dynamically to cues in the environment, remaining plastic from development through adulthood. We have previously demonstrated that olfactory fear conditioning leads to increased odorant-specific receptor representation in the main olfactory epithelium and in glomeruli within the olfactory bulb. We now demonstrate that olfactory extinction training specific to the conditioned odor stimulus reverses the conditioning-associated freezing behavior and odor learning-induced structural changes in the olfactory epithelium and olfactory bulb in an odorant ligand-specific manner. These data suggest that learning-induced freezing behavior, structural alterations, and enhanced neural sensory representation can be reversed in adult mice following extinction training.

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Region-specific amyloid-β accumulation in the olfactory system influences olfactory sensory neuronal dysfunction in 5xFAD mice

Alzheimer s Research & Therapy ◽

10.1186/s13195-020-00730-2 ◽

2021 ◽

Vol 13 (1) ◽

Author(s):

Gowoon Son ◽

Seung-Jun Yoo ◽

Shinwoo Kang ◽

Ameer Rasheed ◽

Da Hae Jung ◽

...

Keyword(s):

Olfactory Bulb ◽

Sensory Neurons ◽

Olfactory System ◽

Amyloid Β ◽

Olfactory Sensory Neurons ◽

Basal Cells ◽

Irreversible Damage ◽

5Xfad Mouse ◽

Peripheral Areas ◽

5Xfad Mice

Abstract Background Hyposmia in Alzheimer’s disease (AD) is a typical early symptom according to numerous previous clinical studies. Although amyloid-β (Aβ), which is one of the toxic factors upregulated early in AD, has been identified in many studies, even in the peripheral areas of the olfactory system, the pathology involving olfactory sensory neurons (OSNs) remains poorly understood. Methods Here, we focused on peripheral olfactory sensory neurons (OSNs) and delved deeper into the direct relationship between pathophysiological and behavioral results using odorants. We also confirmed histologically the pathological changes in 3-month-old 5xFAD mouse models, which recapitulates AD pathology. We introduced a numeric scale histologically to compare physiological phenomenon and local tissue lesions regardless of the anatomical plane. Results We observed the odorant group that the 5xFAD mice showed reduced responses to odorants. These also did not physiologically activate OSNs that propagate their axons to the ventral olfactory bulb. Interestingly, the amount of accumulated amyloid-β (Aβ) was high in the OSNs located in the olfactory epithelial ectoturbinate and the ventral olfactory bulb glomeruli. We also observed irreversible damage to the ectoturbinate of the olfactory epithelium by measuring the impaired neuronal turnover ratio from the basal cells to the matured OSNs. Conclusions Our results showed that partial and asymmetrical accumulation of Aβ coincided with physiologically and structurally damaged areas in the peripheral olfactory system, which evoked hyporeactivity to some odorants. Taken together, partial olfactory dysfunction closely associated with peripheral OSN’s loss could be a leading cause of AD-related hyposmia, a characteristic of early AD.

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A Mathematical Model of the Olfactory Bulb for the Selective Adaptation Mechanism in the Rodent Olfactory System

PLoS ONE ◽

10.1371/journal.pone.0165230 ◽

2016 ◽

Vol 11 (12) ◽

pp. e0165230

Author(s):

Zu Soh ◽

Shinya Nishikawa ◽

Yuichi Kurita ◽

Noboru Takiguchi ◽

Toshio Tsuji

Keyword(s):

Mathematical Model ◽

Olfactory Bulb ◽

Olfactory System ◽

Selective Adaptation ◽

Adaptation Mechanism

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Single Cell Spike Activity in the Olfactory Bulb

American Journal of Physiology-Legacy Content ◽

10.1152/ajplegacy.1956.186.2.255 ◽

1956 ◽

Vol 186 (2) ◽

pp. 255-257 ◽

Cited By ~ 60

Author(s):

Raymond R. Walsh

Keyword(s):

Olfactory Bulb ◽

Single Cell ◽

Spike Activity ◽

Olfactory System ◽

Olfactory Receptors ◽

Class I ◽

Olfactory Stimulation ◽

Fundamental Characteristic ◽

Class Iii ◽

Discharge Patterns

Studies of single-cell spike discharges in the olfactory bulb of the rabbit indicate the presence of three classes of neurons as characterized by their discharge patterns. Cells of class I discharge continuously and spontaneously; class II cells discharge intermittently in bursts, in synchrony with the passage of air through the nose. Cells of classes I and II are unmodified during olfactory stimulation. It appears there are many cells in the olfactory bulb whose discharge patterns are unrelated to excitation of the olfactory receptors by odors. Cells of class III respond to appropriate odors; the response of such cells to some odors and not others indicates that odor specificity is a fundamental characteristic of the olfactory system.

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Functional recovery of odor representations in regenerated sensory inputs to the olfactory bulb

Frontiers in Neural Circuits ◽

10.3389/fncir.2013.00207 ◽

2014 ◽

Vol 7 ◽

Cited By ~ 3

Author(s):

Man C. Cheung ◽

Woochan Jang ◽

James E. Schwob ◽

Matt Wachowiak

Keyword(s):

Olfactory Bulb ◽

Functional Recovery ◽

Sensory Inputs

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Circuit Properties Generating Gamma Oscillations in a Network Model of the Olfactory Bulb

Journal of Neurophysiology ◽

10.1152/jn.01141.2005 ◽

2006 ◽

Vol 95 (4) ◽

pp. 2678-2691 ◽

Cited By ~ 71

Author(s):

Brice Bathellier ◽

Samuel Lagier ◽

Philippe Faure ◽

Pierre-Marie Lledo

Keyword(s):

Olfactory Bulb ◽

Firing Rate ◽

Lateral Inhibition ◽

Temporal Structure ◽

Gamma Oscillations ◽

Synaptic Organization ◽

Neural Basis ◽

Sensory Inputs ◽

Model Based

The study of the neural basis of olfaction is important both for understanding the sense of smell and for understanding the mechanisms of neural computation. In the olfactory bulb (OB), the spatial patterning of both sensory inputs and synaptic interactions is crucial for processing odor information, although this patterning alone is not sufficient. Recent studies have suggested that representations of odor may already be distributed and dynamic in the first olfactory relay. The growing evidence demonstrating a functional role for the temporal structure of bulbar neuronal activity supports this assumption. However, the detailed mechanisms underlying this temporal structure have never been thoroughly studied. Our study focused on gamma (40–100 Hz) network oscillations in the mammalian OB, which is a form of temporal patterning in bulbar activity elicited by olfactory stimuli. We used computational modeling combined with electrophysiological recordings to investigate the basic synaptic organization necessary and sufficient to generate sustained gamma rhythms. We found that features of gamma oscillations obtained in vitro were identical to those of a model based on lateral inhibition as the coupling modality (i.e., low irregular firing rate and high oscillation stability). In contrast, they differed substantially from those of a model based on lateral excitatory coupling (i.e., high regular firing rate and instable oscillations). Therefore we could precisely tune the oscillation frequency by changing the kinetics of inhibitory events supporting the lateral inhibition. Moreover, gradually decreasing GABAergic synaptic transmission decreased the degree of relay neuron synchronization in response to sensory inputs, both theoretically and experimentally. Thus we have shown that lateral inhibition provides a mechanism by which the dynamic processing of odor information might be finely tuned within the OB circuit.

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