Memory failure predicted by attention lapsing and media multitasking

Abstract

With the explosion of digital media and technologies, scholars, educators and the public have become increasingly vocal about the role that an 'attention economy' has in our lives¹. The rise of the current digital culture coincides with longstanding scientific questions about why humans sometimes remember and sometimes forget, and why some individuals remember better than others^2-6. Here we examine whether spontaneous attention lapses-in the moment^7-12, across individuals^13-15 and as a function of everyday media multitasking^16-19-negatively correlate with remembering. Electroencephalography and pupillometry measures of attention^20,21 were recorded as eighty young adults (mean age, 21.7 years) performed a goal-directed episodic encoding and retrieval task²². Trait-level sustained attention was further quantified using task-based²³ and questionnaire measures^24,25. Using trial-to-trial retrieval data, we show that tonic lapses in attention in the moment before remembering, assayed by posterior alpha power and pupil diameter, were correlated with reductions in neural signals of goal coding and memory, along with behavioural forgetting. Independent measures of trait-level attention lapsing mediated the relationship between neural assays of lapsing and memory performance, and between media multitasking and memory. Attention lapses partially account for why we remember or forget in the moment, and why some individuals remember better than others. Heavier media multitasking is associated with a propensity to have attention lapses and forget.

Extended Data Figure 1.

Experimental design. a, Schematic of goal-directed memory task with EEG+pupillometry epochs. b, Schematic of electrode clusters from which alpha or ERP signal was extracted for respective analyses; electrode clusters are illustrated on a 128-channel net. Pupil diameter from the right eye (upper right) was recorded concurrently via an eyetracking system. L=left, R=right.

Extended Data Figure 2.

Pre-goal attention lapses relate to canonical neural signals of recollection- and familiarity-based memory as assayed by grand-average left-lateralized Parietal Old/New and FN400 ERP effects, respectively. a, Evidence of peak Parietal Old/New signal (indicated by black arrow) in the 500–600ms post-probe window as a function of memory outcome in conceptual and perceptual source retrieval trials. b, Trial-level interaction between pre-goal attention lapses and Parietal Old/New signal on remembered (source hits) vs. forgotten (misses) trials. c, Evidence of peak FN400 signal (indicated by black arrow) in the 400–500ms post-probe window as a function of memory outcome in novelty detection trials. d, Trial-level interaction between pre-goal attention lapses and FN400 signal on correctly endorsed new items (hits) vs. misses. For visualization, quintiles are shown for the relationship between pre-goal lapsing and ERP signal; statistics included an interaction term for retrieval goal state (for Parietal Old/New) and treated pre-goal lapsing and ERP signal continuously in trial-level mixed models. Y-axis units are z-scores. Error bars represent 1 standard error of the mean. Note that z-scoring within run and time-binning in 0.1s (100ms) intervals reduces smaller temporal effects that are sometimes exhibited in grand-average ERP plots (for visualization of grand-average ERP plots downsampled to 0.01s intervals (10ms), see ED Fig4). CR=correct rejection; FA=false alarm. N=75.

Extended Data Figure 3.

Evidence of mean peak Parietal Old/New signal (indicated by black arrow) in the 500–600ms post-probe window as a function of memory outcome in source retrieval trials. a, b, Data are split by conceptual (a) and perceptual (b) source trials. CRold=correct rejection to old item; FAold=false alarm to old item. For conceptual cuing, hits and misses are to conceptually studied items and CRs and FAs are to perceptually studied items. For perceptual cuing, hits and misses are to perceptually studied items and CRs and FAs are to conceptually studied items. N=75.

Extended Data Figure 4.

Grand-average left-lateralized ERPs revealing recollection-based Parietal Old/New and familiarity-based FN400 memory effects, downsampled to 10ms time-bin intervals. a, b, The same profile of findings is observed as with the 100ms time-bins (see main text), such that evidence of peak Parietal Old/New signal (indicated by black arrow) is exhibited 500–600ms post-probe onset as a function of memory outcome in conceptual and perceptual source retrieval trials (a) and evidence of peak FN400 signal (indicated by black arrow) is exhibited 400–500ms post-probe onset as a function of memory outcome in novelty detection trials (b). Y-axis units are within-run z-scores. CR=correct rejection; FA=false alarm. N=75.

Extended Data Figure 5.

Trait-level differences in sustained attention at encoding help to explain why individuals are more prone to remembering or forgetting. a, b, Greater pre-goal attention lapsing at encoding is related to greater pre-goal attention lapsing at retrieval (a) and lower d’ on the memory task (b). For visualization, raw scores are plotted; statistics included z-scored assays with Pearson correlations. N=75 for alpha retrieval data and N=80 for all other data. Importantly, as reported in SI, these trait differences in attention at encoding do not fully explain the relationship between trait differences in attention at retrieval and memory ability.

Extended Data Figure 6.

Evidence of a phasic Pupil Old/New effect in novelty detection trials 300–500ms post-probe, particularly between correctly rejected old objects vs. hits to new objects. The mean peak difference is at 400ms post-probe (indicated by black arrow). X-axis units are 100ms time-bin intervals, and Y-axis units are within-run z-scores. CR=correct rejection; FA=false alarm. N=75.

Extended Data Figure 7.

Key results from extreme groups analyses of multitasking, memory, and sustained attention for light and heavy media multitaskers. a, b, c, Heavy media multitaskers exhibited lower d’ on the memory tasks (a), more attention lapses on the gradCPT (b), and more evidence of attention lapsing (assayed by mean alpha power and pupil variability) on the memory task (c), relative to light media multitaskers. Error bars represent one standard error of the mean, and mean metrics are shown. N=18 light and N=18 heavy media multitaskers for alpha data, and N=20 light and N=20 heavy media multitaskers for all other data. d, Histogram of scores (N=80) on the Media Multitasking Inventory, illustrated via the bottom 25% of scores (light media multitaskers), the middle 50% of scores (intermediate media multitaskers), and the top 25% of scores (heavy media multitaskers). LMM=Light media multitasker, HMM=Heavier media multitasker, MMT=Media multitasking.

Figure 1.

Pre-goal attention lapses relate to forgetting (misses) vs. remembering (hits) across three retrieval goal conditions, and this relationship is partially mediated by goal-coding strength via midfrontal ERP cluster. a, b, Attention lapses from alpha (a) and pupil (b) assays. Mean unweighted standardized betas are shown in graphs with x- and y-axes, and quintiles for lapsing-goal coding (error bars represent 1 SEM); statistics included interaction term for retrieval goal, and treated lapsing-goal coding continuously (weighted standardized betas) in trial-level mixed models. Numeric axis units with decimals are z-scores. The trial-wise mediation models reflect mean weighted standardized betas, with two-sided p-values (alpha indirect effect: p=.042 and direct effect: p=.017; pupil indirect effect: p=.041 and direct effect: p=.008). Z and t statistical tests, where applicable, with no multiple comparison adjustment. N=75 human subjects from 1 independent experiment.

Figure 2.

Trait-level differences in sustained attention help to explain why individuals are more prone to remembering or forgetting. a, b, Greater lapsing is related to worse d’ on the memory tasks (a) and attention on the gradCPT (b). c, Worse attention on the gradCPT is related to worse memory d’. Raw scores are plotted for graphs with x- and y-axes; statistics included z-scores with Pearson correlations. d, Formal mediation models with mean standardized betas, and two-sided p-values (alpha indirect effect: p=.003; pupil indirect effect: p=.018). N=75 for alpha data and N=80 for all other data with human subjects from 1 independent experiment; hence the effect sizes between commission error and d’ are not identical for alpha and pupil models (Methods). Z and t statistical tests, where applicable, with no multiple comparison adjustment. gradCPT=gradual-onset continuous performance task.

Figure 3.

Trait-level differences in sustained attention partially explain the negative relationship between media multitasking and memory. a, b, Heavier MMT is related to worse d’ (a) and greater lapsing during retrieval (b). c, Heavier MMT is related to higher commission error and RT variability during the gradCPT. Raw scores are plotted for graphs with x- and y-axes; statistics included z-scored assays with Pearson correlations. d, Formal mediation model with mean standardized betas, and two-sided p-values (indirect effect: p=.005 and direct effect: p=.024). N=75 for alpha data and N=80 for all other data with human subjects from 1 independent experiment. Z and t statistical tests, where applicable, with no multiple comparison adjustment. MMT=Media multitasking, gradCPT=gradual-onset continuous performance task.