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

Abstract

Determining 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.

Olfactory Language Requires an Integrative and Interdisciplinary Approach

“…My claim is that the direct experience of valence always precedes categorization or identification. This seems to be borne out by recent data that demonstrates an initial, fast neural response to odor valence in the olfactory bulb that may itself be projected from olfactory receptor neurons [11]. This gives further credence to the idea that the direct experience of valence precedes odor identification.…”

“…Languages with basic smell terms all make more distinctions between types of unpleasant odors than types of pleasant odors. Unpleasant odors have distinct evolutionary relevance, and the brain rapidly processes warning signals from odors to prepare a behavioral response [11]. It is not surprising, therefore, that unpleasant odors are the most significant for people to communicate about.…”

An olfactory-based Brain-Computer Interface: electroencephalography changes during odor perception and discrimination

“…In humans, theta oscillations have been linked to odor processing (Jiang et al, 2017) and working memory for odors (Yang et al, 2021). The involvement of beta and gamma oscillations in olfactory processing has been demonstrated in numerous studies in animals (Adrian, 1942;Rosero and Aylwin, 2011;Lockmann et al, 2018) and in humans, as well (Jung et al, 2006;Iravani et al, 2020Iravani et al, , 2021Yang et al, 2022).…”

Representational maps in the brain: concepts, approaches, and applications

“…Up to date, analysis of representational maps has been used in the form of RSA for neural recordings from different experimental techniques such as EEG/MEG (Su et al, 2012;Cichy et al, 2014;Kaneshiro et al, 2015;Wang et al, 2020) and PET (Kao et al, 2021), covering different sensory modalities like vision (Cohen et al, 2014;Kaneshiro et al, 2015;Cichy et al, 2016;Guntupalli et al, 2016;Wardle et al, 2016;Groen et al, 2018;Xu and Vaziri-Pashkam, 2021;Luo and Collins, 2023), audition (Perez-Bellido et al, 2018;Berezutskaya et al, 2020;Mattioni et al, 2020;Bodin et al, 2021), somatosensation (Lee Masson et al, 2018;Liu et al, 2021;Ariani et al, 2022;Kryklywy et al, 2023), olfaction (Fournel et al, 2016;Iravani et al, 2021;Kato et al, 2022) and motor planning (Ariani et al, 2022).…”