Impairment of attentional networks after 1 night of sleep deprivation - PubMed (original) (raw)
Impairment of attentional networks after 1 night of sleep deprivation
D Tomasi et al. Cereb Cortex. 2009 Jan.
Abstract
Here, we assessed the effects of sleep deprivation (SD) on brain activation and performance to a parametric visual attention task. Fourteen healthy subjects underwent functional magnetic resonance imaging of ball-tracking tasks with graded levels of difficulty during rested wakefulness (RW) and after 1 night of SD. Self-reports of sleepiness were significantly higher and cognitive performance significantly lower for all levels of difficulty for SD than for RW. For both the RW and the SD sessions, task difficulty was associated with activation in parietal cortex and with deactivation in visual and insular cortices and cingulate gyrus but this pattern of activation/deactivation was significantly lower for SD than for RW. In addition, thalamic activation was higher for SD than for RW, and task difficulty was associated with increases in thalamic activation for the RW but not the SD condition. This suggests that thalamic resources, which under RW conditions are used to process increasingly complex tasks, are being used to maintain alertness with increasing levels of fatigue during SD. Thalamic activation was also inversely correlated with parietal and prefrontal activation. Thus, the thalamic hyperactivation during SD could underlie the reduced activation in parietal and blunted deactivation in cingulate cortices, impairing the attentional networks that are essential for accurate visuospatial attention performance.
Figures
Figure 1.
Outline of TRACK epochs of the 2-ball–tracking task. Subjects track the target ball set, which is briefly highlighted (frame 2) after the instruction (frame 1), while all 10 balls move with a random motion for 10 s (frame 3). Then, they respond with a button press if the highlighted balls are those they were tracking (frame 4). The target set if rehighlighted to refocus the subjects’ attention on the balls (frame 5).
Figure 2.
Performance accuracy and RTs for the RW (white) and SD (black) sessions, as a function of the number of tracked balls (VA load). Sample size: 14 healthy men.
Figure 3.
BOLD fMRI activation patterns for the main (RW, SD) and differential (SD > RW and VA load: 4 balls > 2 balls) effects of visual attention, rendered to a structural MRI image. Random-effects analyses (1-way within-subjects ANOVA).
Figure 4.
Average BOLD fMRI signals in specific ROIs (Table 1). Volume = 1.46 cc (left and right ROIs averaged). Sample size: 14 healthy nonsmoking men.
Figure 5.
Statistical maps of functional thalamocortical connectivity during resting epochs, across all 14 healthy subjects and ball-tracking conditions (2, 3, and 4 balls), superimposed to axial slices of a reference brain. Top row: conjunctive analysis of the RW and SD sessions; middle and bottom rows analyses of individual sessions. SPM2 random-effects model: within-subjects ANOVA.
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References
- Adler C, Sax K, Holland S, Schmithorst V, Rosenberg L, Strakowski S. Changes in neuronal activation with increasing attention demand in healthy volunteers: an fMRI study. Synapse. 2001;42:266–272. - PubMed
- Akert K, Monakow K, Künzle H. Projection of precentral motor cortex upon nucleus medialis dorsalis thalami in the monkey. Neurosci Lett. 1979;11:103–106. - PubMed
- Arrington C, Carr T, Mayer A, Rao S. Neural mechanisms of visual attention: object-based selection of a region in space. J Cogn Neurosci. 2000;12(Suppl 2):106–117. - PubMed
- Ashburner J, Neelin P, Collins DL, Evans AC, Friston KJ. Incorporating prior knowledge into image registration. Neuroimage. 1997;6:344–352. - PubMed