Disruption in neural phase synchrony is related to identification of inattentional deafness in real-world setting

Abstract

Individuals often have reduced ability to hear alarms in real world situations (e.g., anesthesia monitoring, flying airplanes) when attention is focused on another task, sometimes with devastating consequences. This phenomenon is called inattentional deafness and usually occurs under critical high workload conditions. It is difficult to simulate the critical nature of these tasks in the laboratory. In this study, dry electroencephalography is used to investigate inattentional deafness in real flight while piloting an airplane. The pilots participating in the experiment responded to audio alarms while experiencing critical high workload situations. It was found that missed relative to detected alarms were marked by reduced stimulus evoked phase synchrony in theta and alpha frequencies (6-14 Hz) from 120 to 230 ms poststimulus onset. Correlation of alarm detection performance with intertrial coherence measures of neural phase synchrony showed different frequency and time ranges for detected and missed alarms. These results are consistent with selective attentional processes actively disrupting oscillatory coherence in sensory networks not involved with the primary task (piloting in this case) under critical high load conditions. This hypothesis is corroborated by analyses of flight parameters showing greater maneuvering associated with difficult phases of flight occurring during missed alarms. Our results suggest modulation of neural oscillation is a general mechanism of attention utilizing enhancement of phase synchrony to sharpen alarm perception during successful divided attention, and disruption of phase synchrony in brain networks when attentional demands of the primary task are great, such as in the case of inattentional deafness.

Keywords: attention; auditory perception; electroencephalography; inattentional deafness; intertrial coherence; neural oscillation; neuroergonomics; phase resetting; workload.

Figure 1

Experimental equipment and setup. Top: DR‐400 Robin 4 seat airplane used in the experiment. Bottom left: Button response unit attached to the control stick. Used by the participant to identify when an audio alarm was heard. Bottom right: The configuration of individuals in the airplane consisted of the participant (pilot) in the front left seat (shown here wearing the Cognionics HD‐72 dry‐wireless 64 channel EEG system), the certified flight instructor in the front right seat, and the research engineer in the back right seat (experimental computer shown on research engineer's lap)

Figure 2

In‐flight navigation to a grass airstrip. Top: Pilot (shown here wearing the Cognionics HD‐72 dry‐wireless 64 channel EEG system) looking at aeronautical charts to navigate to an airfield with a grass airstrip while simultaneously carrying out the audio task of responding by button press to audio alarm stimuli. Bottom: The grass airstrip (in the center of the image) can be quite difficult to see from the air. One needs to find landmarks on the aeronautical chart (e.g., a river) to help locate the grass airstrip amongst all the other green fields

Figure 3

Average event‐related potentials for hits and misses across all participants for (a) independent component IC activations and (b) electrode channel Cz. Bootstrap statistical analyses were conducted. Region of interest (N1 from 70 to 110 ms; T2 from 150 to 190 ms) corrected false discovery rate FDR thresholds for the difference between hits and misses are denoted by magenta asterisks * and uncorrected thresholds are denoted by black asterisks*

Figure 4

Poststimulus onset intertrial coherence (ITC) for alarm hits and misses. Results for ITC bootstrap analyses. The mean and statistically thresholded (p < .05 one‐tailed corrected) mean relative to baseline are given for alarm hits, misses, and hits‐misses

Figure 5

Participant level mean correlation between performance and inter‐trial coherence (ITC). Top shows the time frequency elements showing a significant difference between ITC for hits relative to misses from Figure 3. The arrows depict the location of the strongest significant correlation (p < .05 two‐tailed corrected) for the bootstrap correlation analysis for hits and for misses. (a) The fitted linear regression slope (solid blue line) of the peak time frequency correlation (r = .71) between hit rate and ITC for hits located at ∼13 Hz around 50 ms poststimulus onset. (b) The fitted linear regression slope (solid blue line) of the peak time frequency correlation (r = −.62) between miss rate and ITC for misses located at ∼8 Hz around 165 ms poststimulus onset. The blue asterisks are the individual data points for each participant and the dotted blue lines are the confidence bounds of the fitted linear model