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. 2022 Aug;44(4):2291-2303.
doi: 10.1007/s11357-022-00577-5. Epub 2022 May 12.

Cognitive control, interference inhibition, and ordering of information during working memory in younger and older healthy adults

Mina Mirjalili  1   2   3   4 , Reza Zomorrodi  1   5 , Zafiris J Daskalakis  6 , Sean L Hill  1   3   4   7   8 , Sanjeev Kumar  1   2   3   8   9 , Daniel M Blumberger  1   2   5   8 , Corinne E Fischer  8   10 , Alastair J Flint  8   11 , Nathan Herrmann  8   12 , Krista L Lanctôt  8   9   12 , Linda Mah  8   13 , Benoit H Mulsant  1   2   8 , Bruce G Pollock  1   2   8   9 , Tarek K Rajji  14   15   16   17   18   19 ; PACt-MD Study Group
Affiliations

Cognitive control, interference inhibition, and ordering of information during working memory in younger and older healthy adults

Mina Mirjalili et al. Geroscience. 2022 Aug.

Abstract

Investigating effects of aging on neurophysiological mechanisms underlying working memory provides a better understanding of potential targets for brain intervention to prevent cognitive decline. Theta-gamma coupling (TGC) indexes the ability to order information processed during working memory tasks. Frontal theta event-related synchronization (ERS) and parietal alpha event-related desynchronization (ERD) index cognitive control and interference inhibition, respectively. Relative contributions of TGC, theta ERS, and alpha ERD in relation to stimulus presentation are not characterized. Further, differential effect of normal aging on pre- or post-stimulus processes is unknown. Electroencephalography was recorded in 66 younger and 41 older healthy participants while performing 3-back working memory task. We assessed relationships between 3-back task performance and each of post-stimulus TGC, pre-stimulus parietal alpha ERD, and pre-stimulus frontal theta ERS in each age group. While older adults performed worse on 3-back task than younger adults, TGC, alpha ERD, or theta ERS did not differ between the two groups. TGC was positively associated with 3-back performance in both age groups; pre-stimulus alpha ERD was associated with performance among younger adults; and pre-stimulus theta ERS was not associated with performance in either group. Our findings suggest that both pre-stimulus interference inhibition and post-stimulus ordering of information are important for working memory in younger adults. In contrast, performance in older adults appears to depend only on post-stimulus ordering of information. These specific contributions of neurophysiological resources may explain the poorer performance of older adults and suggest different targets to enhance working memory in age groups.

Keywords: Aging; EEG; Event-related desynchronization; Event-related synchronization; Theta gamma coupling; Working memory.

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Conflict of interest statement

DMB receives research support from the CIHR, NIH, Brain Canada and the Temerty Family Foundation through the CAMH Foundation and the Campbell Research Institute. He received research support and in-kind equipment support for an investigator-initiated study from Brainsway Ltd, and he was the principal site investigator for three sponsor-initiated studies for Brainsway Ltd. He receives in-kind equipment support from Magventure for investigator-initiated research. He received medication supplies for an investigator-initiated trial from Indivior. He has participated in a scientific advisory board meeting for Janssen and Welcony Inc. ZJD has received research and equipment in-kind support for an investigator-initiated study through Brainsway Inc and Magventure Inc. His work was supported by the Canadian Institutes of Health Research (CIHR), the National Institutes of Mental Health (NIMH), and the Temerty Family and Grant Family and through the Centre for Addiction and Mental Health (CAMH) Foundation and the Campbell Institute. CEF receives grant funding from Brain Canada, Patient Centred Outcomes Research Institute (PCORI), St. Michaels Hospital Foundation, Hoffman LaRoche and Vielight Inc. AJF has received grant support from the U.S. National Institutes of Health, the Patient-Centered Outcomes Research Institute, the Canadian Institutes of Health Research, Brain Canada, the Ontario Brain Institute, the Alzheimer’s Association, AGE-WELL, and the Canadian Foundation for Healthcare Improvement. KLL has grant support from the U.S. National Institutes of Health, the Canadian Institutes of Health Research, the Weston Brain Institute, the Alzheimer’s Drug Discovery Foundation, and the Alzheimer’s Association, has received consultation fees from Acadia, BioXcel Therapeutics, Cerevel Therapeutics, ICG Pharma, Kondor Pharma, Otsuka, and holds stock options in Highmark Interactive. SK has received grant support from Brain Canada, NIH, Brain and Behavior Foundation (NARSAD), BrightFocus Foundation, Weston Brain Institute, Canadian Centre for Aging and Brain Health Innovation, CAMH foundation and University of Toronto, and in Kind equipment support from Soterix Medical Inc. BHM holds and receives support from the Labatt Family Chair in Biology of Depression in Late-Life Adults at the University of Toronto. He currently receives research support from Brain Canada, the Canadian Institutes of Health Research, the CAMH Foundation, the Patient-Centered Outcomes Research Institute (PCORI), the US National Institute of Health (NIH), Capital Solution Design LLC (software used in a study founded by CAMH Foundation), and HAPPYneuron (software used in a study founded by Brain Canada). Within the past 5 years, he has also received research support from Eli Lilly (medications for a NIH-funded clinical trial) and Pfizer (medications for a NIH-funded clinical trial). TKR has received research support from Brain Canada, Brain and Behavior Research Foundation, BrightFocus Foundation, Canada Foundation for Innovation, Canada Research Chair, Canadian Institutes of Health Research, Centre for Aging and Brain Health Innovation, National Institutes of Health, Ontario Ministry of Health and Long-Term Care, Ontario Ministry of Research and Innovation, and the Weston Brain Institute. TKR also received in-kind equipment support for an investigator-initiated study from Magstim, and in-kind research accounts from Scientific Brain Training Pro. TKR participated in 2021 in an advisory board for Biogen Canada Inc. TKR is also an inventor on the United States Provisional Patent No. 17/396,030 that describes cell-based assays and kits for assessing serum cholinergic receptor activity.

Figures

Fig. 1
Fig. 1
The 3-back task and process of EEG markers calculation. a Each trial starts with a plus-sign and after 1500 ms, a letter is presented for 250 ms. Trials where the presented letter matches the letter presented three trials back are labelled as target, whereas the trials where the stimulus is different are labeled as non-target. There is a 3000 ms time window after the letter presentation for the participant to respond. b EEG signal is recorded and preprocessed for each participant. To calculate TGC, time windows from post-stimulus (post-letter) period concatenated to generate a 5-second signal and then coupling between theta phase and gamma amplitude was calculated. To calculate ERD and ERS, signal from pre-stimulus time window was extracted and ERD/S were calculated for each trial. ERS trials (depicted as red squares) and ERD trials (depicted as blue squares) were separated and then averaged. TGC, theta-gamma coupling; ERS, event-related synchronization; ERD, event-related desynchronization
Fig. 2
Fig. 2
Association between 3-back performance and EEG markers. d’ values versus a log transformed weighted TGC, b weighted alpha ERD, and c log transformed weighted theta ERS in older (blue) and younger (orange) adults. Blue lines indicate the linear regression fit in older group (n = 41). Orange lines indicate the linear regression fit in younger group (n = 66). TGC is associated with performance in older (standardized beta = 0.475, p = 0.003) and younger adults (standardized beta = 0.405, p = 0.001). Alpha ERD is associated with performance in only younger adults (standardized beta = 0.380, p = 0.001). TGC, theta-gamma coupling; ERD, event-related desynchronization; ERS, event-relate synchronization
Fig. 3
Fig. 3
Topographic maps of EEG markers. Topographic maps of a TGC, b alpha ERD, and c theta ERS within younger adults (first column), older adults (second column), and the difference between younger and older adults (third column). Rectangles show frontal region for TGC, parietal region for alpha ERD, and frontal region for theta ERS. Independent two-sample t-tests showed no significant difference in EEG markers between younger and older adults (p’s > 0.05). TGC, theta-gamma coupling; ERS, event-related synchronization; ERD, event-related desynchronization
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