Morphological changes in secondary, but not primary, sensory cortex in individuals with life-long olfactory sensory deprivation

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

doi:10.1016/j.neuroimage.2020.117005

Abstract

Individuals with congenital sensory deprivation usually demonstrate altered brain morphology in areas associated with early processing of the absent sense. Here, we aimed to establish whether this also applies to individuals born without a sense of smell (congenital anosmia) by comparing cerebral morphology between 33 individuals with isolated congenital anosmia and matched controls. We detected no morphological alterations in the primary olfactory (piriform) cortex. However, individuals with anosmia demonstrated gray matter volume atrophy in bilateral olfactory sulci, explained by decreased cortical area, curvature, and sulcus depth. They further demonstrated increased gray matter volume and cortical thickness in the medial orbital gyri; regions closely associated with olfactory processing, sensory integration, and value-coding. Our results suggest that a lifelong absence of sensory input does not necessarily lead to morphological alterations in primary sensory cortex and extend previous findings with divergent morphological alterations in bilateral orbitofrontal cortex, indicating influences of different developmental processes.

Highlights

The notion that the human brain is plastic and undergoes morphological as well as functional alterations in response to changes in experienced demands is widely accepted (Buonomano and Merzenich, 1998; Lindenberger et al, 2017)
All of the significant clusters were located in the orbitofrontal cortex (OFC): two demonstrating gray matter atrophy in the isolated congenital anosmia (ICA) group around the bilateral olfactory sulci, two clusters demonstrating a gray matter volume increase in the ICA group centered around the bilateral medial orbital gyri, and an additional cluster of increased volume in the right posterior orbital gyrus, which will not be further discussed due to its minor size (Fig. 1, Table 2)
In opposition to our initial hypothesis, no significant group differences in gray matter volume within piriform cortex were demonstrated at an family-wise error (FWE)-corrected significance level of p

Summary

Introduction

The notion that the human brain is plastic and undergoes morphological as well as functional alterations in response to changes in experienced demands is widely accepted (Buonomano and Merzenich, 1998; Lindenberger et al, 2017). Visual sensory deprivation has repeatedly been linked to both structural and functional cerebral reorganizations with often profound changes in regions normally focused on the processing of the absent sense, often in primary sensory cortex (for reviews see Bavelier and Neville, 2002; Frasnelli et al, 2011; Merabet and Pascual-Leone, 2010). Few studies have investigated the potential plastic effects of complete olfactory sensory deprivation (anosmia, for a review see Reichert and Scho€pf, 2018) and reports on cerebral reorganization in individuals with lifelong (congenital) anosmia is rare. In comparison to individuals who have gone through normal sensory development, individuals with a congenital or very early acquired complete sensory deprivation would be expected to demonstrate pronounced patterns of cerebral reorganization. Individuals with isolated congenital sensory deprivation constitute a good model for increasing our understanding of the adaptiveness the human brain possesses

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