Seeing Beyond Your Nose? The Effects of Lifelong Olfactory Sensory Deprivation on Cerebral Audio-visual Integration

Moa G Peter,Gustav Mårtensson,Elbrich M Postma,Love Engström Nordin,Eric Westman,Sanne Boesveldt,Johan N Lundström

doi:10.1016/j.neuroscience.2021.07.017

Abstract

Lifelong auditory and visual sensory deprivation have been demonstrated to alter both perceptual acuity and the neural processing of remaining senses. Recently, it was demonstrated that individuals with anosmia, i.e. complete olfactory sensory deprivation, displayed enhanced multisensory integration performance. Whether this ability is due to a reorganization of olfactory processing regions to focus on cross-modal multisensory information or whether it is due to enhanced processing within multisensory integration regions is not known. To dissociate these two outcomes, we investigated the neural processing of dynamic audio-visual stimuli in individuals with congenital anosmia and matched controls (both groups, n = 33) using functional magnetic resonance imaging. Specifically, we assessed whether the previously demonstrated multisensory enhancement is related to cross-modal processing of multisensory stimuli in olfactory associated regions, the piriform and olfactory orbitofrontal cortices, or enhanced multisensory processing in established multisensory integration regions, the superior temporal and intraparietal sulci. No significant group differences were found in the a priori hypothesized regions using region of interest analyses. However, exploratory whole-brain analysis suggested higher activation related to multisensory integration within the posterior superior temporal sulcus, in close proximity to the multisensory region of interest, in individuals with congenital anosmia. No group differences were demonstrated in olfactory associated regions. Although results were outside our hypothesized regions, combined, they tentatively suggest that enhanced processing of audio-visual stimuli in individuals with congenital anosmia may be mediated by multisensory, and not primary sensory, cerebral regions.

Highlights

Absence of input from one sensory modality can lead to enhanced performance in remaining senses (Merabet and Pascual-Leone, 2010; Frasnelli et al, 2011)
Similar to what we described above, there were no statistical differences between the two groups in either processing of audio-visual stimuli (Fig. 2D, Supplementary Table S1) or multisensory integration of audio-visual stimuli within the defined multisensory integration regions (Fig. 2E, Supplementary Table S2), according to the maximum criterion, at p < .05 uncorrected for multiple comparison
We found that the superior temporal sulcus (ICA p = 1.36∙10À4; Control p = 1.1∙10À4), but not the intraparietal sulcus, showed significant positive audio-visual activation (Fig. 2E, Supplementary Table S3)

Summary

Introduction

Absence of input from one sensory modality can lead to enhanced performance in remaining senses (Merabet and Pascual-Leone, 2010; Frasnelli et al, 2011). Integration of input from remaining senses in sensory deprived individuals tend to not show the same behavioral benefits, compared to sensory intact individuals, as unimodal tasks often do (Collignon et al, 2009; Occelli et al, 2013; Hauthal et al, 2014; Scheller et al, 2021) In contrast to these observations, mainly based on auditory and visual sensory deprivation, olfactory sensory deprivation has been linked to unaltered or even decreased performance in the remaining chemical senses (Gudziol et al, 2001; Frasnelli et al, 2010; Landis et al, 2010), and enhanced audio-visual integration performance (Peter et al, 2019).

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Results

Conclusion