The Phase of Spontaneous Pre-stimulus EEG Oscillations Predicts Auditory Pattern Identification

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Recent studies have shown that the power and phase of spontaneous pre-stimulus oscillations in the electroencephalogram (EEG) predict behavior on simple perceptual and cognitive tasks. Such findings suggest that pre-stimulus EEG may be used to augment human performance in operational environments. For instance, EEG measures could inform the timing of signal presentation in order to align with an optimal brain state. Work with visual stimuli has consistently demonstrated an influence of pre-stimulus features on performance in simple stimulus detection tasks (e.g. Busch et al., 2009; Dugué et al., 2011). However, results in the auditory modality have been mixed, with a relationship between pre-stimulus EEG and performance seen only with the entrainment of oscillations to rhythmic background stimulation (Ng et al., 2012). Little is known about the predictive capacity of pre-stimulus features when more complex decisions need to be made (e.g. extracting meaning from sounds). This raises the possibility that pre-stimulus cortical oscillatory activity only shows a relationship with performance in supra-threshold tasks requiring more complex processing, given that extensive feature processing in the auditory system occurs sub-cortically. To address this gap in the knowledge, the present study examined pre-stimulus EEG as it relates to accuracy in a rapid auditory processing task. In contrast to previous work in the auditory domain, no background noise was present, and a relatively complex pattern identification task was used. We hypothesized that pre-stimulus power and/or phase in the theta and alpha bands would relate in a predictable way to performance accuracy. On each trial, participants heard three 40-ms sinusoidal tones separated by 40-ms inter-stimulus intervals, one of which was at a different frequency than the other two. Participants’ task was to indicate the order of the tones (low-low-high, low-high-low, etc.). An adaptive one-up, one-down procedure was used to determine the frequency separation associated with each participant’s 50% correct identification threshold. Afterwards, each participant completed 250 trials while the EEG was collected from a 68-channel array of electrodes. Resulting data were sorted into correct and incorrect trials to facilitate single-trial analysis of predictive pre-stimulus EEG features. Using a phase-opposition sum (POS) measure, our results demonstrate that pre-stimulus alpha band phase differs between correct and incorrect trials. Specifically, strong phase opposition occurred between approximately -200 to -100 ms prior to onset of the tones, and fell within the 7 to 11 Hz range (high theta / low alpha band). As a complementary measure of performance-related phase opposition, we sorted individual trials into phase bins, such that each individual’s most accurate bin was aligned at zero; we found a significant difference in mean accuracy between those bins closest to the most accurate bin and those furthest. This was consistent across participants, further supporting the relationship between spontaneous pre-stimulus EEG phase and pattern identification. By performing two further control analyses we were able to rule out the possibility of pre-stimulus contamination by post-stimulus activity. These findings have important ramifications in the neuroergonomics field. For instance, aircraft operators often have many signals to attend to, both visual and auditory. While much work has explored the perceptual and cognitive effects of longer-term brain states such as drowsiness or acute stress, understanding the influences of short-term shifts in brain state may be important for optimizing conditions under which an operator can detect, identify, and understand crucial signals. Being able to present signals in alignment with these short-term states may be one direction towards such optimization; inducing oscillatory entrainment in the operator himself may be another.