Proactive and Reactive Response Inhibition across the Lifespan.

Raymond J Dolan,Rick A Adams,Peter Smittenaar,Glyn Lewis,Harriet Brown,Xi Luo,Robb B Rutledge,Peter Zeidman

doi:10.1371/journal.pone.0140383

Abstract

One expression of executive control involves proactive preparation for future events, and this contrasts with stimulus driven reactive control exerted in response to events. Here we describe findings from a response inhibition task, delivered using a smartphone-based platform, that allowed us to index proactive and reactive inhibitory self-control in a large community sample (n = 12,496). Change in stop-signal reaction time (SSRT) when participants are provided with advance information about an upcoming trial, compared to when they are not, provides a measure of proactive control while SSRT in the absence of advance information provides a measure of reactive control. Both forms of control rely on overlapping frontostriatal pathways known to deteriorate in healthy aging, an age-related decline that occurs at an accelerated rate in men compared to women. Here we ask whether these patterns of age-related decline are reflected in similar changes in proactive and reactive inhibitory control across the lifespan. As predicted, we observed a decline in reactive control with natural aging, with a greater rate of decline in men compared to women (~10 ms versus ~8 ms per decade of adult life). Surprisingly, the benefit of preparation, i.e. proactive control, did not change over the lifespan and women showed superior proactive control at all ages compared to men. Our results suggest that reactive and proactive inhibitory control partially rely on distinct neural substrates that are differentially sensitive to age-related change.

Highlights

We frequently need to exert rapid reactive control over our actions, such as stopping the car when an animal unexpectedly jumps on to the road
For the benefit of the reader we further unpack leading Go reaction times (RTs) as a function of condition, age and gender in S1A Fig; and the variance in leading vs non-leading Go RT (‘non-leading’ refers to the second response in a trial) in S1B and S1C Fig. Note that the average stop-signal reaction time (SSRT) is in the range of 340 to 400 ms, higher than the average values reported in the literature
We found that these data conform to assumptions of the widely used independent horse race model, which was used to estimate the SSRT in the Prepared and Unprepared conditions

Summary

Introduction

We frequently need to exert rapid reactive control over our actions, such as stopping the car when an animal unexpectedly jumps on to the road. Demographics of Inhibitory Control inhibition literature—the stop-signal task—only measures reactive control [5,6]. This task has provided a detailed understanding of how corticostriatal loops and the hyperdirect pathway subserve reactive control [7,8] and how age-related decline in these pathways is associated with impaired reactive control [9]. Age-related volume reductions are pronounced in frontal regions and occur at a more rapid rate in men than women [16,17,18,19]. We hypothesized that both reactive and proactive inhibitory control would decline with age and this decline would be more pronounced in men than women

Methods

Results

Conclusion