Elsevier

NeuroImage

Volume 51, Issue 2, June 2010, Pages 835-843
NeuroImage

Lapsing when sleep deprived: Neural activation characteristics of resistant and vulnerable individuals

https://doi.org/10.1016/j.neuroimage.2010.02.031Get rights and content

Abstract

Lapses of attention, in the form of delayed responses to salient stimuli, increase in frequency for some but not all persons after sleep deprivation (SD). To identify patterns of task-related brain activation that might explain differences in vulnerability to SD, we performed fMRI on participants during a visual, selective attention task. We analyzed the correct responses in a trial-by-trial fashion to model the effects of response time. Stimulus contrast was varied to modulate perceptual difficulty. Attentional lapses and low-contrast stimuli were independently associated with increased signal in fronto-parietal regions associated with biasing attention. Sleep-deprived vulnerable individuals showed reduced top down fronto-parietal signal across all levels of image contrast and this reduction was particularly significant during lapses. There was concurrent reduction in extrastriate cortex and thalamus activation. Non-vulnerable persons showed a trend towards higher top-down biasing of attention and preserved visual cortex activation during SD lapses. A major contributor to performance degradation in SD appears to be a reduction in top-down biasing of attention that is independent of task difficulty.

Introduction

Serious industrial catastrophes, transportation accidents, and medical errors result from lapses of attention that occur when sleep-deprived individuals fail to stay alert while fighting the tendency to fall asleep (Mitler et al., 1988, Dinges, 1995, Barger et al., 2006, Philip and Akerstedt, 2006). Lapses can manifest as delayed responses to well-defined target stimuli (Dorrian et al., 2005, Weissman et al., 2006, Chee et al., 2008), response errors (Padilla et al., 2006) or failure to respond (Peiris et al., 2006). We recently showed that lapses resulting from a delayed response in the setting of sleep deprivation (see Methods for an elaboration) differ from lapses of equivalent duration recorded after a normal night of sleep by (1) an attenuated response of frontal and parietal control regions with an accompanying (2) reduction in extrastriate visual cortex activation, and (3) reduced thalamic activation during lapses that contrasts with the elevated thalamic activation during non-lapse periods (Chee et al., 2008).

These findings raised two questions addressed in the present study. The first relates to whether or not these results generalize across individuals who differ in their vulnerability to sleep deprivation. The second question involves the relative contribution of reduced top-down control of attention in the sleep-deprived state vis-à-vis regional failure of the extrastriate visual cortex to adequately capture sensory information.

It is well established that selective attention results in enhanced responses to stimuli within the attended location, driven by top-down signals originating in frontal and parietal regions (Desimone and Duncan, 1995, Reynolds and Chelazzi, 2004). As such, a possible explanation for the reduced extrastriate activation associated with lapses during sleep deprivation is that it merely reflects weakened parietal and frontal biasing signals.

However, an alternative explanation is that use-dependent homeostatic effects (Huber et al., 2004, Huber et al., 2006) could impair the ability of visual cortex to respond appropriately to salient stimuli independent of attention driven effects. The affected extrastriate cortex could also be manifesting “local sleep” whereby cortical areas that were particularly taxed during wakefulness show greater propensity to manifest sleep-like properties (Pigarev et al., 1997, Krueger et al., 2008).

To distinguish between these alternative explanations for reduced extrastriate cortex activation during lapses in SD, we manipulated image contrast to vary the perceptual difficulty of the task. Increasing perceptual difficulty has been shown to elevate activation in fronto-parietal regions involved in mediating cognitive control (Marois et al., 2004). This has the effect of increasing the apparent contrast of the stimulus—making a low contrast stimulus more likely to be perceived. We have previously suggested that lapses in SD might result from a compounded loss of top-down cognitive control superposed on existing deficits that occur when lapsing in the rested state. Under this framework, if reduced visual cortex activation was the product of a decrease in top-down influences, we would expect a concurrent state-related reduction in both fronto-parietal and visual sensory activation across different levels of stimulus contrast. We might additionally expect that such a decline in top-down control of visual attention to be more severe in those vulnerable to the effects of sleep deprivation than in those resistant to its effects.

Conversely, should local sleep or use-dependent degradation of visual cortex function be at fault, we might expect vulnerable individuals to show a disproportionate reduction of visual cortex activation at low levels of stimulus contrast and a concurrent increase in top-down biasing signals arising from fronto-parietal control regions with these low-contrast stimuli (Fig. 1).

Section snippets

Participants

Twenty right-handed, healthy adults (15 females, mean age = 21.5 years, stdev = 2.0 years) participated in the study after giving informed consent. Participants were selected from a pool of university students who responded to a web-based questionnaire. They had to: (1) be right-handed, (2) be between 18 and 35 years of age, (3) have habitual good sleeping habits (sleeping no less than 6.5 h each night for the past 1 month), (4) not be on any long-term medications, (5) have no symptoms associated

Behavioral findings

There was a strong main effect of contrast (F(2,36) = 41.77, p < 0.001) and state (F(1,18) = 22.75, p < 0.001) on performance accuracy. Subjects were less accurate in the low contrast conditions and during SD (Table 1). There was no interaction between contrast and state (F(2,36) = 0.70, n.s.). There was an interaction between vulnerability and state (F(1,18) = 36.82, p < 0.001) in which Vulnerable subjects were less accurate after SD compared to Non-vulnerable subjects.

Subjects were slower in responding to

Discussion

Replicating previous findings, we found that lapses were associated with elevated activation in fronto-parietal control regions that became less pronounced with sleep deprivation. During lapses in SD, Vulnerable persons showed significantly lower signal increases in cognitive biasing regions, a marked drop in visual cortex activation, and reduced thalamic activation. Non-vulnerable persons in contrast, showed higher top-down biasing of attention during lapses in SD, in addition to relatively

Conclusion

In response to the questions that motivated this study, we found vulnerability to sleep deprivation to significantly modulate brain activation patterns during lapses in this state. We also found that the attenuation of top-down biasing signals rather than a primary deficit in visual cortex function can account for the effects observed in the visual cortex. This could be the predominant mechanism underlying lapses and their associated performance degradation in sleep-deprived persons.

Acknowledgments

William Rekshan III, Michele Veldsman, Delise Chong and Annette Chen contributed to data collection. This work was supported by grants awarded to Dr Michael Chee from the Defense Science and Technology Agency Singapore (POD0713897) and the National Research Foundation Singapore (STaR Award).

References (36)

  • ChuahL.Y. et al.

    Cholinergic augmentation modulates visual task performance in sleep-deprived young adults

    J. Neurosci.

    (2008)
  • DesimoneR. et al.

    Neural mechanisms of selective visual attention

    Annu. Rev. Neurosci.

    (1995)
  • DingesD.F.

    An overview of sleepiness and accidents

    J. Sleep Res.

    (1995)
  • DingesD.F. et al.

    Cumulative sleepiness, mood disturbance, and psychomotor vigilance performance decrements during a week of sleep restricted to 4–5 hours per night

    Sleep

    (1997)
  • DoranS.M. et al.

    Sustained attention performance during sleep deprivation: evidence of state instability

    Arch. Ital. Biol.

    (2001)
  • DorrianJ. et al.

    Psychomotor vigilance performance: Neurocognitive assay sensitive to sleep loss

  • GoebelR. et al.

    Analysis of functional image analysis contest (FIAC) data with brainvoyager QX: from single-subject to cortically aligned group general linear model analysis and self-organizing group independent component analysis

    Hum. Brain Mapp.

    (2006)
  • HuberR. et al.

    Local sleep and learning

    Nature

    (2004)
  • Cited by (137)

    • Acute sleep deprivation in humans

      2023, Encyclopedia of Sleep and Circadian Rhythms: Volume 1-6, Second Edition
    • Sleep deprivation detected by voice analysis

      2024, PLoS Computational Biology
    View all citing articles on Scopus
    View full text