Semantic context‐dependent neural representations of odors in the human piriform cortex revealed by 7T MRI

• Published in: Human brain mapping 2024-04, Vol.45 (6), p.e26681-n/a
• Main Authors: Okumura, Toshiki, Kida, Ikuhiro, Yokoi, Atsushi, Nakai, Tomoya, Nishimoto, Shinji, Touhara, Kazushige, Okamoto, Masako
• Format: Article
• Language: English
• Subjects: Adult; Brain Mapping; Female; human olfaction; Humans; Magnetic Resonance Imaging; Male; Odorants; Olfactory Perception - physiology; piriform cortex; Piriform Cortex - diagnostic imaging; Piriform Cortex - physiology; semantic context; Semantics; ultra‐high field fMRI; Young Adult
• ISSN: 1065-9471; 1097-0193
• DOI: 10.1002/hbm.26681

Olfactory perception depends not only on olfactory inputs but also on semantic context. Although multi‐voxel activity patterns of the piriform cortex, a part of the primary olfactory cortex, have been shown to represent odor perception, it remains unclear whether semantic contexts modulate odor representation in this region. Here, we investigated whether multi‐voxel activity patterns in the piriform cortex change when semantic context modulates odor perception and, if so, whether the modulated areas communicate with brain regions involved in semantic and memory processing beyond the piriform cortex. We also explored regional differences within the piriform cortex, which are influenced by olfactory input and semantic context. We used 2 × 2 combinations of word labels and odorants that were perceived as congruent and measured piriform activity with a 1‐mm isotropic resolution using 7T MRI. We found that identical odorants labeled with different words were perceived differently. This labeling effect was observed in multi‐voxel activity patterns in the piriform cortex, as the searchlight decoding analysis distinguished identical odors with different labels for half of the examined stimulus pairs. Significant functional connectivity was observed between parts of the piriform cortex that were modulated by labels and regions associated with semantic and memory processing. While the piriform multi‐voxel patterns evoked by different olfactory inputs were also distinguishable, the decoding accuracy was significant for only one stimulus pair, preventing definitive conclusions regarding the locational differences between areas influenced by word labels and olfactory inputs. These results suggest that multi‐voxel patterns of piriform activity can be modulated by semantic context, possibly due to communication between the piriform cortex and the semantic and memory regions. Associating distinct word labels with specific odorants not only differentiated perceptions of the same odorants but also differentiated multi‐voxel activity patterns within the primary olfactory cortex, as demonstrated by using ultra‐high field functional magnetic resonance imaging (fMRI).