Neural correlates of age-related changes in cognitive action control

Demographic change leads to an increasing interest in the healthy aging of the brain. The latter has been associated with changes in different domains of cognitive performance across the lifespan, including an age-related deterioration in various aspects of cognitive action control. Analyzing processes of cognitive action control, bottom-up and top-down subprocesses can be differentiated. In previous studies of healthy aging both decreases and increases in regional brain activity have been associated with the aging brain, leading to multiple theories on age-specific neural alterations and yielding a shift to a more integrative view on brain changes over the life span, among others in the context of dynamic processes of neuroplasticity. The neural correlates of an age-related decline in successfully exerting cognitive action control are to a large extent still elusive. We investigated age-related changes of the subprocesses of cognitive action control by employing the spatial stimulus-response compatibility (SRC) task in a functional magnetic resonance imaging (fMRI) study of a population-based sample (n=252, 18-85 years). The SRC task comprises two conditions: under the compatible condition an ipsilateral manual reaction to the presented stimulus is required, whereas the incompatible condition necessitates a contralateral reaction and thus especially triggers top-down directed subprocesses of cognitive action control. Task-related performance (reaction time and error rate) was analyzed on a behavioral level and included in the analysis of the imaging data. Age was included as a covariate. We hypothesized that the influence of age on cognitive action control could be shown on a behavioral and on a neural level and that it is at least partially shared with performance-related effects across the lifespan on the neural level, potentially reflected by neural hyperactivity. On a behavioral level, our findings corroborated an age-related decline in cognitive action control. On a neural level, we replicated the general SRC task network and delineated neural correlates of bottom-up and top-down processes. Within this network we found age-related hyperactivity in bilateral intraparietal sulcus (IPS), superior parietal lobule, cerebellum, right inferior frontal gyrus, dorsolateral prefrontal cortex (DLPFC), mid-cingulate cortex and left anterior Insula (aIns) when dealing with incompatibility-induced response conflicts. We suggest that worse age-related performance is associated with both bottom-up and top-down processes when dealing with the SRC task. Based on our data, as hypothesized, age-related decline in cognitive action control is reflected in regional hyperactivity, rather than hypoactivity. We identified aIns, DLPFC and IPS as key neural correlates. Increased activation of left aIns potentially reflects the higher age-related demand for control and task-set maintenance dealing with incompatibility. Hyperactivity in right DLPFC might be a correlate of successful inhibition processes when dealing with the task. The integrational role of the IPS is highlighted by its age- and performance-related hyperactivity. Our findings may reflect difficulties in overriding bottom-up driven spatial orientation and the requirement for additional controlled processing steps dealing with incompatibility, which become more likely with age. We suggest a significant influence of age on cognitive action control, which is on a neural level at least partially shared with performance-related effects across lifespan. Regional hyperactivity might be compensatory for complementary network changes (esp. functional connectivity). Our findings moreover support the idea of neuroplasticity. Additionally, we identified a putative age-related decline in the ability to integrate semantic knowledge with current task demands that might contribute to the observed age-related decline in performance