Network segregation varies with neural distinctiveness in sensorimotor cortex

Abstract

Normal aging is associated with declines in sensorimotor function. Previous studies have linked age-related behavioral declines to decreases in neural differentiation (i.e., dedifferentiation), including decreases in the distinctiveness of neural activation patterns and in the segregation of large-scale neural networks at rest. However, no studies to date have explored the relationship between these two neural measures and whether they explain the same aspects of behavior. To investigate these issues, we collected a battery of sensorimotor behavioral measures in older and younger adults and estimated (a) the distinctiveness of neural representations in sensorimotor cortex and (b) sensorimotor network segregation in the same participants. Consistent with prior findings, sensorimotor representations were less distinct and sensorimotor resting state networks were less segregated in older compared to younger adults. We also found that participants with the most distinct sensorimotor representations exhibited the most segregated sensorimotor networks. However, only sensorimotor network segregation was associated with individual differences in sensorimotor performance, particularly in older adults. These novel findings link network segregation to neural distinctiveness, but also suggest that network segregation may play a larger role in maintaining sensorimotor performance with age.

Keywords: Aging; Dedifferentiation; Resting-state; Sensorimotor; Task activity.

Figure 1.

Functional mask (size = 1000 vertices in each hemisphere) from a representative older adult participant used for calculating neural distinctiveness of sensorimotor representations evoked from right vs. left hand finger tapping.

Figure 2.

Significant age differences were observed in A) a summary measure of gross motor performance (t=2.69, p=.009); B) fine motor performance (t=5.01, p<.001); C) sensorimotor network segregation (t=2.55, p=.013); and D) neural distinctiveness of sensorimotor representations (t=2.29, p=.027) between young (blue) and older (red) adults.

Figure 3.

Neural distinctiveness as a function of ROI size in young (blue) and older (red) adults. Sensorimotor cortical activation patterns for right vs. left hand movement were more distinctive at smaller ROI sizes and less distinctiveness at larger ROI sizes across all participants. However, the effect of ROI size did not significantly influence the observed age differences in neural distinctiveness (F=.70, p=.48). Error bars denote the standard error of the mean.

Figure 4.

A) Relationship between sensorimotor network segregation and neural distinctiveness of sensorimotor representations using the functional ROI and B) using the Power sensorimotor network ROI across all participants after controlling for the effects of age, GM volume, motion and univariate activation.

Figure 5.

A) Relationship between gross motor performance and A) network segregation and B) neural distinctiveness. Relationship between fine motor performance and C) network segregation and D) neural distinctiveness. Plots are illustrated as partial correlations, controlling for the effects of age, GM volume, motion and univariate activation.