Lapsing when sleep deprived: Neural activation characteristics of resistant and vulnerable individuals
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)
- et al.
Dissociation of cortical regions modulated by both working memory load and sleep deprivation and by sleep deprivation alone
Neuroimage
(2005) - et al.
The activation of attentional networks
Neuroimage
(2005) - et al.
Improved detection of event-related functional MRI signals using probability functions
Neuroimage
(2001) Forest before trees: the precedence of global features in visual perception
Cogn. Psychol.
(1977)- et al.
Transport and industrial safety, how are they affected by sleepiness and sleep restriction
Sleep Med. Rev.
(2006) - et al.
Interacting roles of attention and visual salience in V4
Neuron
(2003) - et al.
Impact of extended-duration shifts on medical errors, adverse events, and attentional failures
PLoS Med.
(2006) - et al.
Functional neuroimaging and behavioral correlates of capacity decline in visual short-term memory after sleep deprivation
Proc. Natl. Acad. Sci. U. S. A.
(2007) - et al.
Lapsing during sleep deprivation is associated with distributed changes in brain activation
J. Neurosci.
(2008) - Chee, M.W., Tan J.C., Parimal S., Zagorodnov, V., 2010. Sleep deprivation and its effects on object-selective...
Cholinergic augmentation modulates visual task performance in sleep-deprived young adults
J. Neurosci.
Neural mechanisms of selective visual attention
Annu. Rev. Neurosci.
An overview of sleepiness and accidents
J. Sleep Res.
Cumulative sleepiness, mood disturbance, and psychomotor vigilance performance decrements during a week of sleep restricted to 4–5 hours per night
Sleep
Sustained attention performance during sleep deprivation: evidence of state instability
Arch. Ital. Biol.
Psychomotor vigilance performance: Neurocognitive assay sensitive to sleep loss
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.
Local sleep and learning
Nature
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