The effect of aging on fronto-striatal reactive and proactive inhibitory control

Abstract

Inhibitory control, like most cognitive processes, is subject to an age-related decline. The effect of age on neurofunctional inhibition processing remains uncertain, with age-related increases as well as decreases in activation being reported. This is possibly because reactive (i.e., outright stopping) and proactive inhibition (i.e., anticipation of stopping) have not been evaluated separately. Here, we investigate the effects of aging on reactive as well as proactive inhibition, using functional MRI in 73 healthy subjects aged 30-70years. We found reactive inhibition to slow down with advancing age, which was paralleled by increased activation in the motor cortex. Behaviorally, older adults did not exercise increased proactive inhibition strategies compared to younger adults. However, the pattern of activation in the right inferior frontal gyrus (rIFG) showed a clear age-effect on proactive inhibition: rather than flexibly engaging the rIFG in response to varying stop-signal probabilities, older subjects showed an overall hyperactivation. Whole-brain analyses revealed similar hyperactivations in various other frontal and parietal brain regions. These results are in line with the neural compensation hypothesis of aging: processing becomes less flexible and efficient with advancing age, which is compensated for by overall enhanced activation. Moreover, by disentangling reactive and proactive inhibition, we can show for the first time that the age-related increase in activation during inhibition that is reported generally by prior studies may be the result of compensation for reduced neural flexibility related to proactive control strategies.

Neuro-Cognitive Effects of Acute Tyrosine Administration on Reactive and Proactive Response Inhibition in Healthy Older Adults

“…5, 6; Tables 2–4) g,h,i and deactivation of, e.g., motor cortex in the reactive response inhibition network, as shown previously for the current task in young and older adults (Bloemendaal et al, 2016) and for similar paradigms (Zandbelt and Vink, 2010; Kleerekooper et al, 2016). …”

“…Two forms of response inhibition have been distinguished: reactive response inhibition is the process of canceling an ongoing response at the moment this is needed (i.e., outright stopping), whereas proactive response inhibition entails the preparation for stopping when this may become necessary, e.g., based on cues held in working memory. Age-related impairments have been shown in both reactive inhibition (measured with stop-signal reaction time; SSRT) and proactive inhibition (measured with anticipatory response slowing), particularly under high information load (i.e., high information processing demands for interpreting the stop-signal probability cues; Bloemendaal et al, 2016; Kleerekooper et al, 2016). It is unclear whether tyrosine-induced modulation of catecholaminergic signaling in older adults will affect reactive and/or proactive response inhibition.…”

Resting-State fMRI Associated with Stop-Signal Task Performance in Healthy Middle-Aged and Elderly People

“…In behavioral studies, older adults have often been shown to exhibit longer stopping time, suggesting that there is an age-related inhibitory deficit (e.g., Kramer et al, 1994; Bedard et al, 2002; van de Laar et al, 2011; Kleerekooper et al, 2016). However, other studies found either no age-related decline (e.g., Kray et al, 2009) or only a specific deficit (e.g., Anguera and Gazzaley, 2012).…”

Effect of Aging on Motor Inhibition during Action Preparation under Sensory Conflict

“…Aging is often associated with a decline in various executive functions (Hedden and Gabrieli, 2004; Gazzaley and D’Esposito, 2007; Levin and Netz, 2015) including memory, attention, reasoning abilities and inhibitory control (Fujiyama et al, 2012; Cuypers et al, 2013; Levin et al, 2014; Stewart et al, 2014; Bönstrup et al, 2015; McNab et al, 2015; Smittenaar et al, 2015; Cid-Fernández et al, 2016; Kleerekooper et al, 2016). Several hypotheses have been proposed emphasizing the possible relationship between these deficits and a progressive degeneration of the prefrontal cortex (Hedden and Gabrieli, 2004; Gazzaley et al, 2008).…”