The human olfactory bulb processes odor valence representation and cues motor avoidance behavior

Determining the valence of an odor to guide rapid approach–avoidance behavior is thought to be one of the core tasks of the olfactory system, and yet little is known of the initial neural mechanisms supporting this process or of its subsequent behavioral manifestation in humans. In two experiments, we measured the functional processing of odor valence perception in the human olfactory bulb (OB)—the first processing stage of the olfactory system—using a noninvasive method as well as assessed the subsequent motor avoidance response. We demonstrate that odor valence perception is associated with both gamma and beta activity in the human OB. Moreover, we show that negative, but not positive, odors initiate an early beta response in the OB, a response that is linked to a preparatory neural motor response in the motor cortex. Finally, in a separate experiment, we show that negative odors trigger a full-body motor avoidance response, manifested as a rapid leaning away from the odor, within the time period predicted by the OB results. Taken together, these results demonstrate that the human OB processes odor valence in a sequential manner in both the gamma and beta frequency bands and suggest that rapid processing of unpleasant odors in the OB might underlie rapid approach–avoidance decisions.

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The human olfactory bulb process odor valence representation and initiate motor avoidance behavior

10.1101/2021.01.20.427468 ◽

2021 ◽

Author(s):

Behzad Iravani ◽

Martin Schaefer ◽

Donald A. Wilson ◽

Artin Arshamian ◽

Johan N. Lundström

Keyword(s):

Olfactory Bulb ◽

Avoidance Response ◽

Avoidance Behavior ◽

Olfactory System ◽

Separate Experiment ◽

Beta Activity ◽

Early Processing ◽

Invasive Method ◽

Approach Avoidance ◽

Beta Frequency

ABSTRACTDetermining the valence of an odor to provide information to guide rapid approach-avoidance behavior is thought to be one of the core tasks of the olfactory system, yet little is known of its initial neural mechanisms or subsequent behavioral manifestation in humans. In two experiments, we measured the functional processing of odor valence perception in the human olfactory bulb (OB)—the first processing stage of the olfactory system—using a non-invasive method as well as assessed subsequent motor avoidance response. We demonstrate that odor valence perception is associated with both gamma and beta activity in the human OB. Moreover, we show that negative, but not positive, odors initiate an early beta response in the OB, a response that is linked to a preparatory neural motor response in motor cortex. Finally, in a separate experiment we show that negative odors trigger a full-body motor avoidance response, manifested as a rapid leaning away from the odor, in the time period predicted by the OB results. Taken together, these results demonstrate that the human OB processes odor valence in a sequential manner in both the gamma and beta frequency bands and suggest that early processing of unpleasant odors in the OB might underlie rapid approach-avoidance decisions.

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Supplemental Material for Embodiment of Approach-Avoidance Behavior: Motivational Priming of Whole-Body Movements in a Virtual World

Motivation Science ◽

10.1037/mot0000205.supp ◽

2020 ◽

Keyword(s):

Avoidance Behavior ◽

Virtual World ◽

Whole Body ◽

Body Movements ◽

Approach Avoidance

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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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The effects of cortisol administration on approach–avoidance behavior: An event-related potential study

Biological Psychology ◽

10.1016/j.biopsycho.2007.07.003 ◽

2007 ◽

Vol 76 (3) ◽

pp. 135-146 ◽

Cited By ~ 53

Author(s):

Jacobien M. van Peer ◽

Karin Roelofs ◽

Mark Rotteveel ◽

J. Gert van Dijk ◽

Philip Spinhoven ◽

...

Keyword(s):

Avoidance Behavior ◽

Event Related Potential ◽

Potential Study ◽

Approach Avoidance

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Fronto-striatal projections regulate approach-avoidance conflict

10.1101/2020.03.05.979708 ◽

2020 ◽

Author(s):

Adrienne C. Loewke ◽

Adelaide R. Minerva ◽

Alexandra B. Nelson ◽

Anatol C. Kreitzer ◽

Lisa A. Gunaydin

Keyword(s):

Anxiety Disorders ◽

Avoidance Behavior ◽

D1 Receptor ◽

Projection Neurons ◽

Medium Spiny Neurons ◽

Neural Pathways ◽

Spiny Neurons ◽

Striatal Projection Neurons ◽

Neural Computations ◽

Approach Avoidance

ABSTRACTThe dorsomedial prefrontal cortex (dmPFC) has been linked to approach-avoidance behavior and decision-making under conflict, key neural computations thought to be altered in anxiety disorders. However, the heterogeneity of efferent prefrontal projections has obscured identification of the specific top-down neural pathways regulating these anxiety-related behaviors. While the dmPFC-amygdala circuit has long been implicated in controlling reflexive fear responses, recent work suggests that this circuit is less important for avoidance behavior. We hypothesized that dmPFC neurons projecting to the dorsomedial striatum (DMS) represent a subset of prefrontal neurons that robustly encode and drive approach-avoidance behavior. Using fiber photometry recording during the elevated zero maze (EZM) task, we show heightened neural activity in prefrontal and fronto-striatal projection neurons, but not fronto-amydalar projection neurons, during exploration of the anxiogenic open arms of the maze. Additionally, through pathway-specific optogenetics we demonstrate that this fronto-striatal projection preferentially excites postsynaptic D1 receptor-expressing medium spiny neurons in the DMS and bidirectionally controls avoidance behavior. We conclude that this striatal-projecting subpopulation of prefrontal neurons regulates approach-avoidance conflict, supporting a model for prefrontal control of defensive behavior in which the dmPFC-amygdala projection controls reflexive fear behavior and the dmPFC-striatum projection controls anxious avoidance behavior. Our findings identify this fronto-striatal circuit as a valuable therapeutic target for developing interventions to alleviate excessive avoidance behavior in anxiety disorders.

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Effects of Ionized Air on Early Acquisition of Sidman Avoidance Behavior by Rats

Psychological Reports ◽

10.2466/pr0.1977.41.3f.1071 ◽

1977 ◽

Vol 41 (3_suppl) ◽

pp. 1071-1074 ◽

Cited By ~ 9

Author(s):

Virginia Falkenberg ◽

Roger E. Kirk

Keyword(s):

Avoidance Response ◽

Avoidance Behavior ◽

Avoidance Performance ◽

Albino Rats ◽

Sidman Avoidance ◽

Sprague Dawley ◽

Air Ions ◽

Air Ionization ◽

Early Acquisition ◽

Ionized Air

This research investigated the effects of positive and negative air ionization on the early acquisition of a Sidman (1953) avoidance response. The subjects were 20 male albino rats of the Sprague-Dawley strain. They were randomly assigned to ionization conditions and given 4 2-hr. acquisition sessions. The temporal parameters of the task were a response-shock interval of 20 sec. and a shock-shock interval of 5 sec. Shocks were delivered as 1-ma. pulses of 1 sec. duration. The results indicated that at the end of 4 2-hr. sessions the avoidance performance of rats trained in the presence of negative air ions was superior to that of rats trained in the presence of positive air ions.

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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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