Inter- and Intra-Hemispheric Age-Related Remodeling in Visuo-Spatial Working Memory

Abstract

Electroencephalography (EEG) studies investigating visuo-spatial working memory (vWM) in aging typically adopt an event-related potential (ERP) analysis approach that has shed light on the age-related changes during item retention and retrieval. However, this approach does not fully enable a detailed description of the time course of the neural dynamics related to aging. The most frequent age-related changes in brain activity have been described by two influential models of neurocognitive aging, the Hemispheric Asymmetry Reduction in Older Adults (HAROLD) and the Posterior-Anterior Shift in Aging (PASA). These models posit that older adults tend to recruit additional brain areas (bilateral as predicted by HAROLD and anterior as predicted by PASA) when performing several cognitive tasks. We tested younger (N = 36) and older adults (N = 35) in a typical vWM task (delayed match-to-sample) where participants have to retain items and then compare them to a sample. Through a data-driven whole scalp EEG analysis we aimed at characterizing the temporal dynamics of the age-related activations predicted by the two models, both across and within different stages of stimulus processing. Behaviorally, younger outperformed older adults. The EEG analysis showed that older adults engaged supplementary bilateral posterior and frontal sites when processing different levels of memory load, in line with both HAROLD and PASA-like activations. Interestingly, these age-related supplementary activations dynamically developed over time. Indeed, they varied across different stages of stimulus processing, with HAROLD-like modulations being mainly present during item retention, and PASA-like activity during both retention and retrieval. Overall, the present results suggest that age-related neural changes are not a phenomenon indiscriminately present throughout all levels of cognitive processing.

Cognitive reserve counteracts typical neural activity changes related to ageing

“…Thus, the results of the present study align with studies showing negative relationships between increased inter-hemispheric dedifferentiation and cognitive functioning in older adults (Knights et al, 2021; Koen and Rugg, 2019; Morcom and Jonson, 2015). Finally, differences between HCR and LCR groups in inter-hemispheric asymmetries for P300 but not for N200 are consistent with a recent ERP study (Tagliabue et al, 2022), suggesting that reduced inter-hemispheric asymmetrical activity associated with ageing does not uniformly affect all stages of information processing.…”

Cognitive reserve counteracts typical neural activity changes related to ageing

“…Thus, the results of the present study align with studies showing negative relationships between increased inter-hemispheric dedifferentiation and cognitive functioning in older adults (Knights et al, 2021;Koen and Rugg, 2019;Morcom and Johnson, 2015). Finally, differences between HCR and LCR groups in inter-hemispheric asymmetries for P300 but not for N200 are consistent with a recent ERP study (Tagliabue et al, 2022), suggesting that reduced inter-hemispheric asymmetrical activity associated with ageing does not uniformly affect all stages of information processing.…”

“…In this regard, functional magnetic resonance imaging (fMRI) studies revealed a posterior to anterior shift of brain activity (e.g., Davis et al, 2008;Morcom and Henson, 2018) and reduced inter-hemispheric asymmetries (e.g., Cabeza, 2002;Roe et al, 2020) in older adults during the performance of cognitive tasks. Accordingly, research using ERPs reported that ageing was associated with diminished parietal ERP amplitudes in addition to increased frontal activity (Daffner et al, 2011;Friedman et al, 1997;Saliasi et al, 2013;van Dinteren et al, 2014) as well as reduced inter-hemispheric asymmetries (Angel et al, 2011;Learmonth et al, 2017;Tagliabue et al, 2022) during the performance of cognitive tasks. The posterior to anterior shift of activity was related to deployment of frontal mechanisms to compensate processing deficits in posterior areas, whereas the loss of brain asymmetries was taken as a sign of compensatory activity by the contralateral hemisphere as well as dysfunctional processes characterised by loss of cortical specificity (for a review, see McDonough et al, 2022).…”

Aging and feature binding in visual working memory

“…A typical cognitive impairment that follows the discourse of aging is reduced performance in working memory (WM) tasks (Salthouse et al, 1991 ; Park et al, 2002 ). This is generally observed as a lower accuracy in older adults (OAs) compared to young adults (YAs) with increasing sets of objects that need to be remembered (Jost et al, 2011 ; Sander et al, 2011 ; Tagliabue et al, 2019 , 2022 ). Because of the set size manipulation, most studies have concluded that there is a reduction in the amount of object representations that OAs can hold in WM in comparison to YAs (Jost et al, 2011 ; Schwarzkopp et al, 2016 ; Tagliabue et al, 2020 but see Oberauer and Kliegl, 2010 ); this interpretation falls in line with the viewpoint of WM capacity as a fixed-slot model (Luck and Vogel, 1997 ; Cowan, 2001 ; see Adam et al, 2017 for more recent results), in which an individual's WM is set at a fixed number of representations, regardless of the content of the representations (Awh et al, 2007 ).…”