Neural processing of the reward value of pleasant odorants

Midroit, Maëllie; Chalençon, Laura; Renier, Nicolas; Milton, Adrianna J.; Thévenet, M; Sacquet, Joëlle; Breton, Marine; Forest, Jérémy; Noury, Norbert; Richard, Marion; Raineteau, Olivier; Ferdenzi, Camille; Fournel, Arnaud; Wesson, Daniel W.; Bensafi, Moustafa; Didier, Anne; Mandairon, Nathalie

doi:10.1016/j.cub.2021.01.066

Cited by 40 publications

(32 citation statements)

References 106 publications

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“…Whether this region-specific valence separation in processing also occurs in humans is not known. However, a recent study on human participants demonstrated that, akin to rodents, pleasant but not negative odors are preferentially processed in the olfactory tubercle ( 59 ). Moreover, intracranial electric stimulation of the OFC, an area previously linked to odor valence processing in humans, could only produce pleasant odor experiences ( 60 ).…”

Section: Discussionmentioning

confidence: 99%

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

Iravani

Schaefer

Wilson

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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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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Section: Discussionmentioning

confidence: 99%

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

Iravani

Schaefer

Wilson

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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“…Electrophysiological recordings in the OT have revealed that OT neurons differentiate between rewarded and unrewarded odors in a go/no-go task, and quickly track changing odor-outcome contingencies ( Gadziola et al, 2015 ; Millman and Murthy, 2020 ). These effects may extend to humans with elevated OT activity and development of place preference in response to attractive odorants ( Midroit et al, 2021 ). Moreover, the OT appears to be the olfactory processing site most strongly involved in tracking odor-outcome associations, as direct comparison to recordings in posterior piriform cortex revealed weaker representation of odor-reward contingency ( Gadziola et al, 2020 ; Millman and Murthy, 2020 ).…”

Section: Introductionmentioning

confidence: 99%

Distinct representation of cue-outcome association by D1 and D2 neurons in the ventral striatum’s olfactory tubercle

Martiros

Kapoor

Kim

et al. 2022

eLife

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Positive and negative associations acquired through olfactory experience are thought to be especially strong and long-lasting. The conserved direct olfactory sensory input to the ventral striatal olfactory tubercle (OT) and its convergence with dense dopaminergic input to the OT could underlie this privileged form of associative memory, but how this process occurs is not well understood. We imaged the activity of the two canonical types of striatal neurons, expressing D1- or D2-type dopamine receptors, in the OT at cellular resolution while mice learned odor-outcome associations ranging from aversive to rewarding. D1 and D2 neurons both responded to rewarding and aversive odors. D1 neurons in the OT robustly and bidirectionally represented odor valence, responding similarly to odors predicting similar outcomes regardless of odor identity. This valence representation persisted even in the absence of a licking response to the odors and in the absence of the outcomes, indicating a true transformation of odor sensory information by D1 OT neurons. In contrast, D2 neuronal representation of the odor-outcome associations was weaker, contingent on a licking response by the mouse, and D2 neurons were more selective for odor identity than valence. Stimulus valence coding in the OT was modality-sensitive, with separate sets of D1 neurons responding to odors and sounds predicting the same outcomes, suggesting that integration of multimodal valence information happens downstream of the OT. Our results point to distinct representation of identity and valence of odor stimuli by D1 and D2 neurons in the OT.

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“…It receives projections from dopaminergic neurons in the ventral tegmental area which would be involved in the formation of olfactory preferences (Zhang et al, 2017). Likewise, increased activity of projections from the MOB towards the OT (Midroit et al, 2021) or from the Ventral Tegmental Area to the OT during odor exposure increases the attractiveness of odors (Zhang et al, 2017). Whereas it was not clearly established early on, the MOB receives direct projections from the reward system.…”

Section: Alteration Of the Mesocorticolimbic System Could Impact Food Odor Perception And Attractionmentioning

confidence: 99%

Olfaction in the context of obesity and diabetes: Insights from animal models to humans

et al. 2022

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Neural processing of the reward value of pleasant odorants

Cited by 40 publications

References 106 publications

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

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

Distinct representation of cue-outcome association by D1 and D2 neurons in the ventral striatum’s olfactory tubercle

Olfaction in the context of obesity and diabetes: Insights from animal models to humans

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