Effects of sleep deprivation on dissociated components of executive functioning.

SLEEP LOSS IS A GROWING THREAT TO SAFETY IN MODERN SOCIETIES, AS BOTH WORK HOURS AND COMMUTE TIMES ARE EXTENDED.1 SLEEP LOSS impairs performance on simple cognitive tasks such as signal detection and reaction time (RT) tests.2 Many occupational settings, however, require executive functioning—the ability to initiate, monitor, and stop actions so as to achieve goals3—in order to execute complex tasks such as interpersonal communication, creative problem solving, and decision making.4 Thus, an important question is to what extent executive functions are impaired by sleep loss.5 The real-world relevance of this question is illustrated by occupational disasters including the nuclear meltdown of Chernobyl, the grounding of the Exxon Valdez, and the disastrous launch decision of the Challenger space shuttle, all of which involved complex decision errors for which sleep loss has been cited to be a contributing factor. Several studies have examined deficits in executive functioning during sleep deprivation.6–20 Between studies there has been considerable inconsistency as to whether and how executive functions were found to be impaired.21 For example, two recent studies found that sleep deprivation impaired performance on a go/no-go task,8,9 which is typically considered to measure the ability to inhibit a prepotent response. Another study, using Stroop task performance as an index of ability to inhibit a prepotent response, reported that this executive function was not impaired during sleep deprivation.19 Similarly, one study reported that sleep deprivation changed behavioral decisions involving risk on a lottery choice task,16 while another study using a different gambling task observed no significant differences in choices made after sleep loss.20 Inconsistencies like these have made it difficult to derive a uniform account of whether and how sleep deprivation affects executive functions. Horne and colleagues12 have posited that sleep deprivation especially impairs performance on tasks tapping executive functions because these tasks selectively rely on the prefrontal cortex. A basis for this theory is provided by EEG-based and neuroimaging evidence that sleep loss affects the frontal lobes more than most other brain areas. For instance, studies have shown that sleep pressure, as operationalized by increased theta power density in the waking EEG, is most evident in frontal areas during total sleep deprivation (TSD).22,23 Using PET neuroimaging, which allows greater anatomical specificity, it has been documented that TSD decreases metabolism specifically in the prefrontal cortex.24 From findings like these it has been inferred that sleep loss would impair executive functioning and performance on tasks that rely on prefrontal cortical function more than non-executive task performance. In this vein, a parallel between the cognitive impairments seen in sleep deprivation and those seen in aging has been hypothesized,12 as both conditions seem to selectively involve reduced activity in the prefrontal cortex. There is ample evidence, however, that sleep deprivation also impairs performance on cognitive tasks requiring relatively little executive control.25 This includes the psychomotor vigilance test (PVT), a simple RT task measuring sustained attention.26 Based in part on detailed analyses of RT data from the PVT, Dinges and colleagues postulated that performance impairment during sleep deprivation is caused by an increase in moment-to-moment variability of attention resulting from the interaction of the homeostatic drive for sleep, the circadian drive for wakefulness, and compensatory effort to perform.27 They hypothesized that the variability in performance due to difficulty sustaining attention would transfer to a wide variety of cognitive tasks since “attention is a requirement of many goal-directed activities.”27 According to this “state instability” theory, sleep deprivation does not necessarily cause impairments in executive functions tasks because of selective deficits in the prefrontal cortex, but at least in part due to deficits in the ability to sustain attention. The theory implies that through impairment of sustained attention, sleep deprivation affects cognitive performance globally, including not only executive functioning and other higher order cognitive processes, but many other aspects of performance as well. One reason that different views exist as to how and why executive functioning may be degraded during sleep deprivation is that the tasks commonly used to measure executive functions do not allow dissociation of the various cognitive processes contributing to performance. By definition, executive functions operate on other cognitive processes, and any task that targets executive functions therefore also implicates non-executive cognitive processes (i.e., the task impurity problem).3 As such, a low score on an executive functions test does not necessarily arise from impairment of the target executive functions; it could also result from impairment of other component cognitive processes involved in the task.28 In the present laboratory study, we investigated sleep-deprived performance on an executive functions battery. The tasks in the battery were selected because they allow for the dissociation of some of the intertwined components of cognitive performance. Our battery made it possible to isolate 2 specific executive function components: working memory scanning efficiency, and suppression of irrelevant information that leads to proactive interference (that is, inhibition of information that is no longer relevant). Both of these executive function components involve the prefrontal cortex.29,30 They are associated with working memory capacity, and are fundamentally important to executive control during complex task performance.28 We investigated the extent to which working memory scanning efficiency, resistance to proactive interference, and other elements of task performance are affected by acute TSD.