Human body odor increases familiarity for faces during encoding‐retrieval task

Abstract

Odors can increase memory performance when presented as context during both encoding and retrieval phases. Since information from different sensory modalities is integrated into a unified conceptual knowledge, we hypothesize that the social information from body odors and faces would be integrated during encoding. The integration of such social information would enhance retrieval more so than when the encoding occurs in the context of common odors. To examine this hypothesis and to further explore the underlying neural correlates of this behavior, we have conducted a functional magnetic resonance imaging study in which participants performed an encoding‐retrieval memory task for faces during the presentation of common odor, body odor or clean air. At the behavioral level, results show that participants were less biased and faster in recognizing faces when presented in concomitance with the body odor compared to the common odor. At the neural level, the encoding of faces in the body odor condition, compared to common odor and clean air conditions, showed greater activation in areas related to associative memory (dorsolateral prefrontal cortex), odor perception and multisensory integration (orbitofrontal cortex). These results suggest that face and body odor information were integrated and as a result, participants were faster in recognizing previously presented material.

Olfaction in the Multisensory Processing of Faces: A Narrative Review of the Influence of Human Body Odors

“…Body odors have been found to modulate the visual processing of both invariant (i.e., sex, attractiveness, and identity), and transient (i.e., emotional expressions and health) face properties. Spontaneously processed as carrying social information (Pause, 2012), body odors easily bind with face-related visual cues in a multisensory percept (Cecchetto et al, 2020), and overall, social smells bear on how we look at faces. However, large discrepancies emerge across studies in the way chemosensory information is integrated with faces, ranging from the multisensory integration of what seems redundant properties (e.g., identity: Platek et al, 2004;emotion: Zhou and Chen, 2009;Kamiloglu et al, 2018;de Groot et al, 2021) to a more loosely matched correspondence with a rather unspecific influence of body odors (e.g., sex: Mutic et al, 2016;emotion: Mujica-Parodi et al, 2009;de Groot et al, 2015b;Rocha et al, 2018;health: Regenbogen et al, 2017).…”

The scent of attraction and the smell of success: crossmodal influences on person perception

“…Though, in such cases, it may be difficult to rule out any influence of the intrinsic qualities of the body odour from the positive associations that have subsequently been conditioned through extensive repeated exposure to the odour. In the future, it would be interesting to know whether a fine fragrance that was robustly attached to a loved one (should they always choose to wear the same scent) might take on some, or even all, of the same-stress reducing properties as body odours, or whether instead there is something special about the latter (see Boyle et al, 2009 ; Lundstrom et al, 2008 ; though see also Cecchetto et al, 2020 ).…”

Smell what you hardly see: Odors assist categorization in the human visual cortex

“…Emotional body odors (i.e., collected in anxiogenic or happy contexts) elicit (in)congruency effects on the perception of facial expressions (Kamiloğlu et al, 2018;Mujica-Parodi et al, 2009;Rocha et al, 2018;Wudarczyk et al, 2016;Zernecke et al, 2011;Zhou and Chen, 2009), which is also biased by hedonically-contrasted non-body odors (Cook et al, 2017;Leleu et al, 2015a;Leppänen and Hietanen, 2003;Seubert et al, 2010;Syrjänen et al, 2017Syrjänen et al, , 2018. The neural underpinnings of these odor influences on facial information have been explored, revealing various patterns of modulations in "visual" brain regions (Cecchetto et al, 2020;Wudarczyk et al, 2016;Novak et al, 2015;Seubert et al, 2010), or in the EEG activity elicited by the face stimulus (Adolph et al, 2013;Cook et al, 2017;Forscher and Li, 2012;Leleu et al, 2015b;Poncet et al, 2021;Rubin et al, 2012;Syrjänen et al, 2018). Interestingly, given the high relevance of the sense of smell at the beginning of life (Schaal et al, 2020, for review) compared to the relative immaturity of the visual system (Braddick and Atkinson, 2011), odors strongly influence how infants look at faces (Durand et al, 2020(Durand et al, , 2013, or how their brain responds to facial information (Jessen, 2020;Leleu et al, 2020;Rekow et al, 2020Rekow et al, , 2021b.…”

“…These regions go beyond visual inputs and generate categorical responses, that is, distinct responses to different categories (i.e., between-category discrimination) and similar responses to different exemplars of one category despite their physical variability (i.e., withincategory generalization, Bracci and Op de Beeck, 2016;Hagen et al, 2020;Jacques et al, 2016b). While wellknown category-selective visual regions (e.g., the fusiform gyrus) have been associated with odor effects in previously reviewed neuroimaging studies (Cecchetto et al, 2020;Lundström et al, 2019;Seubert et al, 2010;Wudarczyk et al, 2016), their activity was often considered for different behavioral responses to a single category rather than different visual categories irrespective of the behavioral output (i.e., to measure a categoryselective neural response). Similarly, in EEG studies, odor effects have been rarely explored for selective responses to a variety of inputs from a given category contrasted to many other object categories (e.g., only a few individual faces for each emotion in the numerous studies investigating the effect of odors on the perception of facial expressions) and sometimes measured at late latencies over parietal and frontal regions (e.g., Hörberg et al, 2020;Ohla et al, 2018), contrary to occipito-temporal category-selective EEG responses (e.g., Jacques et al, 2016a).…”

“…The influence of odors on vision has also been extensively described for one of the most important objects of the human visual environment, i.e., faces. Odors facilitate face memory (Cecchetto et al, 2020;Steinberg et al, 2012) and orient judgments of face attractiveness (Demattè et al, 2007;Parma et al, 2012;Rikowski and Grammer, 1999), face sex (Kovács et al, 2004), or faceevoked personality traits (Cook et al, 2015(Cook et al, , 2017(Cook et al, , 2018Dalton et al, 2013;Li et al, 2007). Emotional body odors (i.e., collected in anxiogenic or happy contexts) elicit (in)congruency effects on the perception of facial expressions (Kamiloğlu et al, 2018;Mujica-Parodi et al, 2009;Rocha et al, 2018;Wudarczyk et al, 2016;Zernecke et al, 2011;Zhou and Chen, 2009), which is also biased by hedonically-contrasted non-body odors (Cook et al, 2017;Leleu et al, 2015a;Leppänen and Hietanen, 2003;Seubert et al, 2010;Syrjänen et al, 2017Syrjänen et al, , 2018.…”