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

Visual categorization is the brain ability to rapidly and automatically respond to a certain category of inputs. Whether category-selective neural responses are purely visual or can be influenced by other sensory modalities remains unclear. Here, we test whether odors modulate visual categorization,...

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Main Authors: Diane Rekow, Jean-Yves Baudouin, Karine Durand, Arnaud Leleu
Format: Article
Language:English
Published: Elsevier 2022-07-01
Series:NeuroImage
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1053811922003068
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author Diane Rekow
Jean-Yves Baudouin
Karine Durand
Arnaud Leleu
author_facet Diane Rekow
Jean-Yves Baudouin
Karine Durand
Arnaud Leleu
author_sort Diane Rekow
collection DOAJ
description Visual categorization is the brain ability to rapidly and automatically respond to a certain category of inputs. Whether category-selective neural responses are purely visual or can be influenced by other sensory modalities remains unclear. Here, we test whether odors modulate visual categorization, expecting that odors facilitate the neural categorization of congruent visual objects, especially when the visual category is ambiguous. Scalp electroencephalogram (EEG) was recorded while natural images depicting various objects were displayed in rapid 12-Hz streams (i.e., 12 images / second) and variable exemplars of a target category (either human faces, cars, or facelike objects in dedicated sequences) were interleaved every 9th stimulus to tag category-selective responses at 12/9 = 1.33 Hz in the EEG frequency spectrum. During visual stimulation, participants (N = 26) were implicitly exposed to odor contexts (either body, gasoline or baseline odors) and performed an orthogonal cross-detection task. We identify clear category-selective responses to every category over the occipito-temporal cortex, with the largest response for human faces and the lowest for facelike objects. Critically, body odor boosts the response to the ambiguous facelike objects (i.e., either perceived as nonface objects or faces) over the right hemisphere, especially for participants reporting their presence post-stimulation. By contrast, odors do not significantly modulate other category-selective responses, nor the general visual response recorded at 12 Hz, revealing a specific influence on the categorization of congruent ambiguous stimuli. Overall, these findings support the view that the brain actively uses cues from the different senses to readily categorize visual inputs, and that olfaction, which has long been considered as poorly functional in humans, is well placed to disambiguate visual information.
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spelling doaj.art-72129d454a734d75bea99a69e0c2d1b72022-12-22T00:36:38ZengElsevierNeuroImage1095-95722022-07-01255119181Smell what you hardly see: Odors assist visual categorization in the human brainDiane Rekow0Jean-Yves Baudouin1Karine Durand2Arnaud Leleu3Development of Olfactory Communication & Cognition Lab, Center for Taste, Smell & Feeding Behavior, Université Bourgogne Franche-Comté, CNRS, Inrae, Institut Agro Dijon, 21000, Dijon, France; Corresponding authors at: Centre des Sciences du Goût et de l’Alimentation, Équipe « Cognition & Communication Olfactives en Développement », 9E Boulevard Jeanne d'Arc, 21000 Dijon, FranceLaboratoire Développement, Individu, Processus, Handicap, Éducation (DIPHE), Département Psychologie du Développement, de l'Éducation et des Vulnérabilités (PsyDÉV), Institut de psychologie, Université de Lyon (Lumière Lyon 2), 5, avenue Pierre-Mendès-France, 69676, Bron, FranceDevelopment of Olfactory Communication & Cognition Lab, Center for Taste, Smell & Feeding Behavior, Université Bourgogne Franche-Comté, CNRS, Inrae, Institut Agro Dijon, 21000, Dijon, FranceDevelopment of Olfactory Communication & Cognition Lab, Center for Taste, Smell & Feeding Behavior, Université Bourgogne Franche-Comté, CNRS, Inrae, Institut Agro Dijon, 21000, Dijon, France; Corresponding authors at: Centre des Sciences du Goût et de l’Alimentation, Équipe « Cognition & Communication Olfactives en Développement », 9E Boulevard Jeanne d'Arc, 21000 Dijon, FranceVisual categorization is the brain ability to rapidly and automatically respond to a certain category of inputs. Whether category-selective neural responses are purely visual or can be influenced by other sensory modalities remains unclear. Here, we test whether odors modulate visual categorization, expecting that odors facilitate the neural categorization of congruent visual objects, especially when the visual category is ambiguous. Scalp electroencephalogram (EEG) was recorded while natural images depicting various objects were displayed in rapid 12-Hz streams (i.e., 12 images / second) and variable exemplars of a target category (either human faces, cars, or facelike objects in dedicated sequences) were interleaved every 9th stimulus to tag category-selective responses at 12/9 = 1.33 Hz in the EEG frequency spectrum. During visual stimulation, participants (N = 26) were implicitly exposed to odor contexts (either body, gasoline or baseline odors) and performed an orthogonal cross-detection task. We identify clear category-selective responses to every category over the occipito-temporal cortex, with the largest response for human faces and the lowest for facelike objects. Critically, body odor boosts the response to the ambiguous facelike objects (i.e., either perceived as nonface objects or faces) over the right hemisphere, especially for participants reporting their presence post-stimulation. By contrast, odors do not significantly modulate other category-selective responses, nor the general visual response recorded at 12 Hz, revealing a specific influence on the categorization of congruent ambiguous stimuli. Overall, these findings support the view that the brain actively uses cues from the different senses to readily categorize visual inputs, and that olfaction, which has long been considered as poorly functional in humans, is well placed to disambiguate visual information.http://www.sciencedirect.com/science/article/pii/S1053811922003068EEG frequency-taggingmultisensory integrationvisual categorizationodorolfaction
spellingShingle Diane Rekow
Jean-Yves Baudouin
Karine Durand
Arnaud Leleu
Smell what you hardly see: Odors assist visual categorization in the human brain
NeuroImage
EEG frequency-tagging
multisensory integration
visual categorization
odor
olfaction
title Smell what you hardly see: Odors assist visual categorization in the human brain
title_full Smell what you hardly see: Odors assist visual categorization in the human brain
title_fullStr Smell what you hardly see: Odors assist visual categorization in the human brain
title_full_unstemmed Smell what you hardly see: Odors assist visual categorization in the human brain
title_short Smell what you hardly see: Odors assist visual categorization in the human brain
title_sort smell what you hardly see odors assist visual categorization in the human brain
topic EEG frequency-tagging
multisensory integration
visual categorization
odor
olfaction
url http://www.sciencedirect.com/science/article/pii/S1053811922003068
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