Olfactory–trigeminal integration in the primary olfactory cortex

Author:

Karunanayaka Prasanna R.123ORCID,Lu Jiaming14,Elyan Rommy1,Yang Qing X.15,Sathian K.267

Affiliation:

1. Department of Radiology Pennsylvania State University College of Medicine Hershey Pennsylvania USA

2. Department of Neural and Behavioral Sciences Pennsylvania State University College of Medicine Hershey Pennsylvania USA

3. Department of Public Health Sciences Pennsylvania State University College of Medicine Hershey Pennsylvania USA

4. Drum Tower Hospital Medical School of Nanjing University Nanjing China

5. Department of Neurosurgery Pennsylvania State University College of Medicine Hershey Pennsylvania USA

6. Department of Neurology Penn State Health Milton S. Hershey Medical Center Hershey Pennsylvania USA

7. Department of Psychology Pennsylvania State University College of Liberal Arts State College Pennsylvania USA

Abstract

AbstractHumans naturally integrate signals from the olfactory and intranasal trigeminal systems. A tight interplay has been demonstrated between these two systems, and yet the neural circuitry mediating olfactory–trigeminal (OT) integration remains poorly understood. Using functional magnetic resonance imaging (fMRI), combined with psychophysics, this study investigated the neural mechanisms underlying OT integration. Fifteen participants with normal olfactory function performed a localization task with air‐puff stimuli, phenylethyl alcohol (PEA; rose odor), or a combination thereof while being scanned. The ability to localize PEA to either nostril was at chance. Yet, its presence significantly improved the localization accuracy of weak, but not strong, air‐puffs, when both stimuli were delivered concurrently to the same nostril, but not when different nostrils received the two stimuli. This enhancement in localization accuracy, exemplifying the principles of spatial coincidence and inverse effectiveness in multisensory integration, was associated with multisensory integrative activity in the primary olfactory (POC), orbitofrontal (OFC), superior temporal (STC), inferior parietal (IPC) and cingulate cortices, and in the cerebellum. Multisensory enhancement in most of these regions correlated with behavioral multisensory enhancement, as did increases in connectivity between some of these regions. We interpret these findings as indicating that the POC is part of a distributed brain network mediating integration between the olfactory and trigeminal systems.Practitioner Points Psychophysical and neuroimaging study of olfactory–trigeminal (OT) integration. Behavior, cortical activity, and network connectivity show OT integration. OT integration obeys principles of inverse effectiveness and spatial coincidence. Behavioral and neural measures of OT integration are correlated.

Funder

National Institute on Aging

Penn State College of Medicine

Publisher

Wiley

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