Across the adult lifespan the ipsilateral sensorimotor cortex negative BOLD response exhibits decreases in magnitude and spatial extent suggesting declining inhibitory control

Abstract

Ipsilateral sensorimotor (iSM1) cortex negative BOLD responses (NBR) are observed to unilateral tasks and are thought to reflect a functionally relevant component of sensorimotor inhibition. Evidence suggests that sensorimotor inhibitory mechanisms degrade with age, along with aspects of motor ability and dexterity. However, understanding of age-related changes to NBR is restricted by limited comparisons between young vs old adults groups with relatively small samples sizes. Here we analysed a BOLD fMRI dataset (obtained from the CamCAN repository) of 581 healthy subjects, gender-balanced, sampled from the whole adult lifespan performing a motor response task to an audiovisual stimulus. We aimed to investigate how sensorimotor and default-mode NBR characteristics of magnitude, spatial extent and response shape alter at every decade of the aging process. We observed a linear decrease in iSM1 NBR magnitude across the whole lifespan, whereas the contralateral sensorimotor (cSM1) PBR magnitude was unchanged. An age-related decrease in the spatial extent of NBR and an increase in the ipsilateral positive BOLD response (PBR) was observed. This occurred alongside an increasing negative correlation between subject's iSM1 NBR and cSM1 PBR magnitude, reflecting a change in the balance between cortical excitation and inhibition. Conventional GLM analysis, using a canonical haemodynamic response (HR) function, showed disappearance of iSM1 NBR in subjects over 50 years of age. However, a deconvolution analysis showed that the shape of the iSM1 HR altered throughout the lifespan, with significantly delayed time-to-peak and decreased magnitude. The most significant decreases in iSM1 HR magnitude occurred in older age (>60 years) but the first changes in HR shape and timing occurred as early as 30 years, suggesting the possibility of separate mechanisms underlying these alterations. Reanalysis using data-driven HRs for each decade detected significant sensorimotor NBR into late older age, showing the importance of taking changes in HR morphology into account in fMRI aging studies. These results may reflect fMRI measures of the age-related decreases in transcollosal inhibition exerted upon ipsilateral sensorimotor cortex and alterations to the excitatory-inhibitory balance in the sensorimotor network.