Intrinsic intranasal chemosensory brain networks shown by resting-state functional MRI

Abstract

The human brain is organized into functional networks for sensory-motor and cognitive processing. Intrinsic networks are detectable in the absence of stimulation or task demands, whereas extrinsic networks are detectable when stimulated by sensory or cognitive demands. Intranasal chemosensory processing relies on two dissociable networks for processing incoming trigeminal and olfactory stimulation, but it is not known whether these networks are intrinsically organized. The aim of this study was to identify whether brain networks for intranasal chemosensory processing are detectable in functional connectivity resting-state functional MRI (fMRI). Sixteen healthy adults participated in a 5-min resting-state fMRI study. Functional connectivity seeds were defined from coordinates that anchor olfactory (i.e. bilateral piriform and orbitofrontal cortex) and trigeminal (bilateral anterior insula and cingulate cortex) networks in published task activation studies, and the resulting networks were thresholded at P less than 0.001. The olfactory network showed extended functional connectivity to the thalamus, medial prefrontal cortex, caudate, nucleus accumbens, parahippocampal gyrus, and hippocampus. The trigeminal network showed extended functional connectivity to the precuneus, thalamus, caudate, brainstem, and cerebellum. Both networks overlapped in the thalamus, caudate, medial prefrontal cortex, and insula. These results show that brain networks for intranasal chemosensory processing are intrinsically organized, not just extrinsically instantiated in response to task demands, and resemble networks for processing olfactory and trigeminal stimulation. As such, it may be possible to study the functional organization and dynamics of the olfactory network in resting-state fMRI as well as its implications for aging and disease.

Age-related resting-state functional connectivity in the olfactory and trigeminal networks

“…Table 1 tabulates the MNI coordinates and t-values for peak voxels from the contrast of the ON and TN. The unique brain regions belonging to the ON and TN, against a common baseline, have been reported in Tobia et al, 2016 [1]. Figure 2 shows regions where either the ON or TN was significantly correlated with age.…”

“…Seed time courses were extracted in MNI space as the average time course within a three voxel radius (6mm) centered on coordinates that anchor fMRI activation of the olfactory [22] and trigeminal [23] systems, as in our previous publication [1]. Coordinates reported by Iannilli et al were in Talairach space and were converted to MNI space via the Brett transform using GingerALE software [24].…”

“…Previously, employing functional Magnetic Resonance Imaging (fMRI) and a seed-based resting state functional connectivity (FC) technique, we showed that both the ON and TN are intrinsically organized against a common baseline [1,6,7]. The same work showed that the ON, but not the TN, included FC with the hippocampus and medial temporal lobe memory systems [1].…”

“…The same work showed that the ON, but not the TN, included FC with the hippocampus and medial temporal lobe memory systems [1]. There is evidence suggesting that structural changes of these intranasal chemosensory is a natural consequence of aging, but how these structural changes related to aging affect functional characteristics remains poorly understood [8].…”

“… Brain networks for intranasal chemosensation have been shown to be intrinsically organized in humans [1]. However, little is known about how changes in the intrinsic functional connectivity (FC) in chemosensory networks are related to aging.…”