Abstract
Introduction:
The sense of touch is fundamental to our perception of reality. Critically, with advancing age, tactile abilities adapt. Lately, healthy aging has been linked to cortical myelin plasticity (Callaghan 2014, Grydeland 2019), but little is known on how this relates to functional cortex organization (e.g., body topography, resting-state connectivity) and tactile behavior. It has been suggested that layer-specific variation in myelin reflects functional specializations of the local cortical architecture (Nieuwenhuys 2013). However, prior in-vivo studies on age-related myeloarchitecture mainly described the cortex as a two-dimensional sheet. Recent advances in magnetic resonance imaging at 7 Tesla (7T-MRI) offer the possibility to study layer-specific myeloarchitecture in humans in-vivo (Kuehn 2017). Here, we targeted the questions of how myeloarchitecture of the human primary somatosensory cortex (S1) hand area varies with respect to cortical layers and age and how variation in layer-specific myelin relates to resting-state connectivity and tactile behavior.
Methods:
24 healthy, right-handed volunteers (n=12 younger: mean age 24 years, 7 females; n=12 older: mean age 71 years, 6 females) underwent 7T-MRI and tactile testing of index finger performance (see fig. 1). Quantitative T1 (qT1, 0.5 mm isotropic), used as myelin proxy (Stueber 2014), and EPI images (0.5 mm isotropic) of S1 (slab) were acquired. During functional scanning, vibro-tactile stimulation was applied to the fingertips of the right hand (localizer in S1, see fig. 1). A 5-minute resting-state scan was recorded. qT1 values were estimated using the equivolume model (Waehnert 2014). S1 was defined using anatomical landmarks (Yousry 1997). Eigenvector Centrality (EC) maps were calculated for n=20 participants (n=9 younger) using rectified linear unit correlation (Lohmann 2018). A mixed effects ANOVA was applied to qT1 (dependent: finger, cortical depth; independent: age group) and EC values (dependent: finger; independent: age group). Age effects on tactile behavior were tested with t-tests. Pearson correlations were calculated.
Results:
qT1 values were extracted from finger representations (d1-d5) of contralateral S1 at different cortical depths (see fig. 2A). A 3-way mixed-effects ANOVA revealed a significant main effect of cortical depth (F(1.19,26.24)=390.86, p<.0001, ηG²=0.74) with decreasing qT1 values (increasing myelin levels) from superficial to deep cortical depth (see fig. 2A) as well as trends towards a main effect of finger (F(2.62,57.65)=2.29, p=.096, ηG²=0.01, see fig. 2A) and an interaction between cortical depth and age group (F(1.19,26.24)=3.34, p=.073, ηG²=0.02, see fig. 2A). A 2-way mixed-effects ANOVA revealed a significant main effect of finger (F(4,72)=3.60, p<.05, ηG²=0.06) and a trend towards a main effect of age (F(1,18)=4.09, p=.058, ηG²=0.13) with lower EC values in older adults. Across fingers, qT1 values were significantly correlated with EC values at superficial cortical depth in younger adults (see fig. 2B). Older compared to younger adults showed higher discrimination thresholds (t(14.38)=5.76, p<0.0001, r=0.84), lower precision grip accuracy (t(18.70)=-4.29, p<0.001, r=0.70) and higher detection thresholds (t(17.95)=3.67, p<.01, r=0.66). There was a negative correlation trend of deep qT1 and precision grip accuracy for d2 in younger adults (see fig. 2C).
Conclusions:
Layer-specific qT1 mapping in younger and older adults suggests that myeloarchitecture of the S1 hand area is inhomogeneous and varies with respect to cortical depth and functional topography (independent of age). Particularly, the index finger appears to have a special role, most likely being preserved in older age. Our data also indicate that layer-specific myelin variation is related to distinctive widespread resting-state connectivity (related to superficial qT1) and phenotypes of behavior involving precise sensorimotor control (related to deep qT1).