Age differences in prefontal recruitment during verbal working memory maintenance depend on memory load

Abstract

Positron emission tomography (PET) and functional magnetic resonance imaging (fMRI) studies have revealed age-related under-activation, where older adults show less regional brain activation compared to younger adults, as well as age-related over-activation, where older adults show greater activation compared to younger adults. These differences have been found across multiple task domains, including verbal working memory (WM). Curiously, both under-activation and over-activation of dorsolateral prefrontal cortex (DLPFC) have been found for older adults in verbal WM tasks. Here, we use event-related fMRI to test the hypothesis that age-related differences in activation depend on memory load (the number of items that must be maintained). Our predictions about the recruitment of prefrontal executive processes are based on the Compensation Related Utilization of Neural Circuits Hypothesis (CRUNCH; Reuter-Lorenz and Cappell, 2008). According to this hypothesis, more neural resources are engaged by older brains to accomplish computational goals completed with fewer resources by younger brains. Therefore, seniors are more likely than young adults to show over-activations at lower memory loads, and under-activations at higher memory loads. Consistent with these predictions, in right DLPFC, we observed age-related over-activation with lower memory loads despite equivalent performance accuracy across age groups. In contrast, with the highest memory load, older adults were significantly less accurate and showed less DLPFC activation compared to their younger counterparts. These results are considered in relation to previous reports of activation-performance relations using similar tasks, and are found to support the viability of CRUNCH as an account of age-related compensation and its potential costs.

Working memory in middle-aged males: Age-related brain activation changes and cognitive fatigue effects

“…Hence, the level of DLPFC and superior parietal cortex over-activation in middle age did not depend on the level of task demand in terms of WM load or fatigue. This finding is somewhat consistent with studies in older adults demonstrating a plateauing of load-dependent activation after about 4 or 5 items (Cappell et al, 2010;Nagel et al, 2009;Schneider-Garces et al, 2010) and may indicate that activation recruitment in these areas reached its limit.…”

“…The maintenance of an equivalently high level of performance appeared to necessitate increased recruitment of the left DLPFC and superior parietal cortex during encoding in middle-aged compared to young adults. These areas are consistent with areas showing age-related activation differences between young and older adults in previous studies (Cappell et al, 2010;Nagel et al, 2009;Schneider-Garces et al, 2010). According to the CRUNCH model, this increased neural recruitment in older adults results from an age-related decline in neural efficiency (Reuter-Lorenz & Cappell, 2008).…”

“…Bopp & Verhaeghen, 2005;Myerson, Emery, White, & Hale, 2003;Park et al, 2002). Studies using functional magnetic resonance imaging (fMRI) have provided insight into the nature of this decline in old age (older than 60 years) by identifying underlying neural activation changes (Cappell, Gmeindl, & Reuter-Lorenz, 2010;Nagel et al, 2009;Rypma, Berger, & D'Esposito, 2002;Schneider-Garces et al, 2010;Zarahn, Rakitin, Abela, Flynn, & Stern, 2007). However, although an age-related decline in WM maintenance is also present in middle age (between the ages of 40 and 60 years) (Bopp & Verhaeghen, 2005;Myerson et al, 2003;Park et al, 2002), little is known about the nature of the changes, or the associated neural activation, at this stage of life.…”

“…In a behavioral study, Gazzaley, Sheridan, Cooney, and D'Esposito (2007) reported equivalent performance between young and old adults at low WM load, but the appearance of performance decrements in old adults when high WM load was combined with a manipulation that increased task demands, namely distraction (but see Hale et al, 2011). Functional MRI studies have reported increased recruitment of fronto-parietal network areas in older compared to younger adults when WM load was low, despite equivalent behavioral performance (Cabeza et al, 2004), but relatively decreased activation in older adults and an associated performance decline when WM load was high (Cappell et al, 2010;Nagel et al, 2009;Schneider-Garces et al, 2010). These findings have been taken as support for the Compensation-Related Utilization of Neural Circuits Hypothesis (CRUNCH) (Reuter-Lorenz & Cappell, 2008).…”

The cognitive neuroscience of ageing

“…At higher levels of load, this compensatory mechanism is no longer effective, leading to equivalent or less activation in older adults relative to young. Data consistent with this idea have been reported in PFC 65 , and in both PFC and parietal cortex 66,67 during working memory tasks that varied in the number of items that had to be kept in mind. In these studies, older adults had more activation at low levels of working memory load, where performance was equivalent to that of younger adults, but less activity and lower accuracy at higher loads.…”