1/f neural noise and electrophysiological indices of contextual prediction in aging

Abstract

Prediction of upcoming words during reading has been suggested to enhance the efficiency of discourse processing. Emerging models have postulated that predictive mechanisms require synchronous firing of neural networks, but to date, this relationship has been investigated primarily through oscillatory activity in narrow frequency bands. A recently-developed measure proposed to reflect broadband neural activity - and thereby synchronous neuronal firing - is 1/f neural noise extracted from EEG spectral power. Previous research has indicated that this measure of 1/f neural noise changes across the lifespan, and these neural changes predict age-related behavioral impairments in visual working memory. Using a cross-sectional sample of young and older adults, we examined age-related changes in 1/f neural noise and whether this measure predicted ERP correlates of successful lexical prediction during discourse comprehension. 1/f neural noise across two different language tasks revealed high within-subject correlations, indicating that this measure can provide a reliable index of individualized patterns of neural activation. In addition to age, 1/f noise was a significant predictor of N400 effects of successful lexical prediction; however, noise did not mediate age-related declines in other ERP effects. We discuss broader implications of these findings for theories of predictive processing, as well as potential applications of 1/f noise across research populations.

Keywords: Aging; Discourse processing; ERPs; Neural noise; Prediction.

Figure 1

1/f neural noise across task and age. (A) EEG was recorded during and briefly following rapid-serial visual presentation (RSVP) of sentences in both Prediction and Comprehension Paradigms. EEG recordings used to calculate 1/f noise were collected until 300ms prior to the end of each sentence, immediately followed by non-overlapping EEG recordings that were later averaged to generate ERP waveforms to critical words. (B) 1/f neural noise was estimated for both paradigms from the slope (dotted lines) of the power spectrum across frequency (2–25Hz, plotted above with 95% confidence intervals), excluding alpha frequency (7–14Hz, shaded). (C) Correlations between Age and 1/f slopes are plotted topographically. Correlations were maximal over central electrode sites for both paradigms (addition signs). Age correlations with neural noise were not significantly different as a function of task, but topographic differences between tasks emerged over frontal electrode sites (dotted outline). (D) 1/f slopes were strongly correlated between tasks for older readers.

Figure 2

ERPs in the Prediction Paradigm. ERP difference waveforms were generated for the effects of Prediction (unpredicted minus predicted words in moderate cloze passages) and Context (unpredicted low cloze minus unpredicted moderate cloze critical words), plotted at a frontal medial (AFz) and central (Cz) electrode site. Effects of Prediction and Context are plotted for young and older adults for N400 effects (A) and PNP effects (B), alongside topographic plots (right) indicating where effects were maximal in 100ms centered maximal epochs.

Figure 3

Age, 1/f noise, and ERPs. N400 amplitudes for Prediction and Context were reduced in older readers (blue) relative to younger adults (red, A), but no significant effects of age were found for either of the PNP effects. (Error bars indicate standard errors (SEM).) 1/f neural noise was significantly correlated with amplitudes of both N400 effects (B), but not with the PNP effects. A mediation model generated for the Prediction N400 (C, left) shows that 1/f neural noise partially mediated age-related reductions in the Prediction N400. In contrast, a similar mediation analysis performed for the Context N400 (C, right) shows that 1/f neural noise is not predictive of Context N400 amplitudes after controlling for age, and does not mediate age-related reduction of the Context N400 (dotted lines).