Human olfactory-auditory integration requires phase synchrony between sensory cortices

Guangyu Zhou,Ghazaleh Arabkheradmand,Stephan U Schuele,Christina Zelano,Torben Noto,Donald A Wilson,Jonas K Olofsson,Jay A Gottfried,Joshua M Rosenow,Gregory Lane

doi:10.1038/s41467-019-09091-3

Abstract

Multisensory integration is particularly important in the human olfactory system, which is highly dependent on non-olfactory cues, yet its underlying neural mechanisms are not well understood. In this study, we use intracranial electroencephalography techniques to record neural activity in auditory and olfactory cortices during an auditory-olfactory matching task. Spoken cues evoke phase locking between low frequency oscillations in auditory and olfactory cortices prior to odor arrival. This phase synchrony occurs only when the participant’s later response is correct. Furthermore, the phase of low frequency oscillations in both auditory and olfactory cortical areas couples to the amplitude of high-frequency oscillations in olfactory cortex during correct trials. These findings suggest that phase synchrony is a fundamental mechanism for integrating cross-modal odor processing and highlight an important role for primary olfactory cortical areas in multisensory integration with the olfactory system.

Highlights

Multisensory integration is important in the human olfactory system, which is highly dependent on non-olfactory cues, yet its underlying neural mechanisms are not well understood
The phase of low-frequency oscillations in both auditory and olfactory cortical areas coupled to the amplitude of high-frequency oscillations in olfactory cortex prior to odor arrival during correct trials. These findings suggest that phase synchrony is a fundamental mechanism for integrating cross-modal odor processing and highlight an important role for primary olfactory cortical areas in multisensory integration with the olfactory system
Spectrotemporal responses to the auditory cues prior to odor arrival in auditory and olfactory regions of interest, including auditory cortical areas surrounding the superior temporal gyrus (STG) and the superior temporal sulcus (STS) (Fig. 1b) and PC (Fig. 1c), were examined using time–frequency analysis

Summary

Introduction

Multisensory integration is important in the human olfactory system, which is highly dependent on non-olfactory cues, yet its underlying neural mechanisms are not well understood. Spoken cues evoke phase locking between low frequency oscillations in auditory and olfactory cortices prior to odor arrival This phase synchrony occurs only when the participant’s later response is correct. The phase of low frequency oscillations in both auditory and olfactory cortical areas couples to the amplitude of high-frequency oscillations in olfactory cortex during correct trials These findings suggest that phase synchrony is a fundamental mechanism for integrating cross-modal odor processing and highlight an important role for primary olfactory cortical areas in multisensory integration with the olfactory system. Several cortical brain areas have been identified that may integrate information from multiple primary sensory areas[5], in support of the classical hierarchical model of multisensory integration. More recent studies have found involvement of primary sensory areas in multisensory processing[12,13,14], indicating that multisensory integration may involve more distributed neural networks beyond classic hierarchical multisensory-specific areas, including primary sensory cortices[15]

Methods

Results

Conclusion