Losing the struggle to stay awake: divergent thalamic and cortical activity during microsleeps - PubMed (original) (raw)

Losing the struggle to stay awake: divergent thalamic and cortical activity during microsleeps

Govinda R Poudel et al. Hum Brain Mapp. 2014 Jan.

Abstract

Maintaining alertness is critical for safe and successful performance of most human activities. Consequently, microsleeps during continuous visuomotor tasks, such as driving, can be very serious, not only disrupting performance but sometimes leading to injury or death due to accidents. We have investigated the neural activity underlying behavioral microsleeps--brief (0.5-15 s) episodes of complete failure to respond accompanied by slow eye-closures--and EEG theta activity during drowsiness in a continuous task. Twenty healthy normally-rested participants performed a 50-min continuous tracking task while fMRI, EEG, eye-video, and responses were simultaneously recorded. Visual rating of performance and eye-video revealed that 70% of the participants had frequent microsleeps. fMRI analysis revealed a transient decrease in thalamic, posterior cingulate, and occipital cortex activity and an increase in frontal, posterior parietal, and parahippocampal activity during microsleeps. The transient activity was modulated by the duration of the microsleep. In subjects with frequent microsleeps, power in the post-central EEG theta was positively correlated with the BOLD signal in the thalamus, basal forebrain, and visual, posterior parietal, and prefrontal cortices. These results provide evidence for distinct neural changes associated with microsleeps and with EEG theta activity during drowsiness in a continuous task. They also suggest that the occurrence of microsleeps during an active task is not a global deactivation process but involves localized activation of fronto-parietal cortex, which, despite a transient loss of arousal, may constitute a mechanism by which these regions try to restore responsiveness.

Keywords: EEG; drowsiness; fMRI; microsleeps; visuomotor tracking.

Copyright © 2012 Wiley Periodicals, Inc.

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Figures

Figure 1

Figure 1

Tracking task and eyelid and response behaviour associated with a typical microsleep during the tracking task. (a) Participants used a finger‐based joystick to track the displayed yellow target disc moving in a quasi‐random trajectory (dotted line) with a red cursor disc. (b) Accurate tracking led to the movement of the response disc along the same trajectory as the target disc as displayed in the target (smooth black line) and response (jerky red line) position for one cycle (30‐s) of tracking. (c) Tracking response (jerky red line) is flat in both directions (leading to an increase in tracking error and zero speed) and eyes slowly close during a typical microsleep. The units are in pixels (px). [Color figure can be viewed in the online issue, which is available at

http://wileyonlinelibrary.com

.]

Figure 2

Figure 2

Number and median duration of microsleeps (BMs) in the 20 participants during 50 min of tracking.

Figure 3

Figure 3

Per minute estimates of percentage time spent in microsleeps (PERBM), percentage time with greater than 80% eye closure (PERCLOS), relative theta power at Pz, and tracking error in three representative participants. The top panel depicts PERBM in the participant with highest number (190) of microsleeps (I) and a participant with a moderate number (77) of microsleeps (II). The middle panel depicts tracking error (thin line) and PERCLOS (thick line) in the same two participants plus a participant with no microsleeps (III). The bottom panel depicts tracking error (thin line) and relative theta power (thick line) in the same participants. Pearson correlations (r) between time‐courses are displayed within each panel. [Color figure can be viewed in the online issue, which is available at

http://wileyonlinelibrary.com

.]

Figure 4

Figure 4

Group‐level significant (Z > 4.5, P < 0.01, family‐wise‐error corrected) pattern of activation (Red‐yellow) and deactivation (blue‐light blue) during microsleeps are shown overlaid on average structural slices. The group‐level pattern was obtained from the 14 participants with frequent microsleeps. The slices are presented in radiological convention and labeled with MNI coordinates. [Color figure can be viewed in the online issue, which is available at

http://wileyonlinelibrary.com

.]

Figure 5

Figure 5

The BOLD signal modulated by duration in the (a) right superior parietal cortex (MNI coordinates (mm): 22, −44, 58), (b) right thalamus (MNI coordinates (mm): 14, −10, 4), and (c) left thalamus (−14, −14, 4). Average BOLD signal time‐course for three different duration microsleeps bins (0.5–5 s, 5–10 s, and 10–15 s) are shown. The time‐courses were obtained from the eight participants who had microsleeps in all three duration bins. The vertical bars represent the standard error of the mean across subjects (N = 8). The onset of microsleeps is at time zero. Note that both activation and deactivation signals mirror the duration of microsleeps. [Color figure can be viewed in the online issue, which is available at

http://wileyonlinelibrary.com

.]

Figure 6

Figure 6

Group‐level statistical maps showing positive correlation (P < 0.05, family‐wise‐error corrected) between BOLD and theta activity (average of P1, P2, and Pz) in individuals with frequent microsleeps. The group‐level pattern was obtained from the 10 participants with frequent microsleeps and electrode impedance <15 kΩ. The axial slices are presented in radiological convention and labeled with MNI coordinates. [Color figure can be viewed in the online issue, which is available at

http://wileyonlinelibrary.com

.]

Figure 7

Figure 7

Group‐level statistical maps showing negative correlation (P < 0.01, cluster‐extent of 50 voxels) between BOLD and spontaneous alpha activity (average of O1, O2, Oz) in individuals with frequent microsleeps. The group‐level pattern was obtained from the 10 participants with frequent microsleeps and electrode impedance <15 kΩ. The axial slices are presented in radiological convention and labeled with MNI coordinates. [Color figure can be viewed in the online issue, which is available at

http://wileyonlinelibrary.com

.]

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