Effects of Sleep Deprivation on Dissociated Components of Executive Functioning

effects of sleep deprivation on executive functions Effects of Sleep Deprivation on Dissociated Components of Executive Functioning Adrienne M. Tucker, PhD1,2; Paul Whitney, PhD3; Gregory Belenky, MD1; John M. Hinson, PhD3; Hans P.A. Van Dongen, PhD1 Sleep and Performance Research Center, Washington State University, Spokane, WA; 2Taub Institute of Cognitive Neuroscience, Columbia University, New York, NY; 3Department of Psychology, Washington State University, Pullman, WA 1 Study Objectives: We studied the effects of sleep deprivation on executive functions using a task battery which included a modified Sternberg task, a probed recall task, and a phonemic verbal fluency task. These tasks were selected because they allow dissociation of some important executive processes from non-executive components of cognition. Design: Subjects were randomized to a total sleep deprivation condition or a control condition. Performance on the executive functions task battery was assessed at baseline, after 51 h of total sleep deprivation (or no sleep deprivation in the control group), and following 2 nights of recovery sleep, at fixed time of day (11:00). Performance was also measured repeatedly throughout the experiment on a control task battery, for which the effects of total sleep deprivation had been documented in previously published studies. Setting: Six consecutive days and nights in a controlled laboratory environment with continuous behavioral monitoring. Participants: Twenty-three healthy adults (age range 22–38 y; 11 women). Twelve subjects were randomized to the sleep deprivation condition; the others were controls. Results: Performance on the control task battery was considerably degraded during sleep deprivation. Overall performance on the modified Sternberg task also showed impairment during sleep deprivation, as compared to baseline and recovery and compared to controls. However, two dissociated components of executive functioning on this task—working memory scanning efficiency and resistance to proactive interference—were maintained at levels equivalent to baseline. On the probed recall task, resistance to proactive interference was also preserved. Executive aspects of performance on the phonemic verbal fluency task showed improvement during sleep deprivation, as did overall performance on this task. Conclusion: Sleep deprivation affected distinct components of cognitive processing differentially. Dissociated non-executive components of cognition in executive functions tasks were degraded by sleep deprivation, as was control task performance. However, the executive functions of working memory scanning efficiency and resistance to proactive interference were not significantly affected by sleep deprivation, nor were dissociated executive processes of phonemic verbal fluency performance. These results challenge the prevailing view that executive functions are especially vulnerable to sleep loss. Our findings also question the idea that impairment due to sleep deprivation is generic to cognitive processes subserved by attention. Keywords: Executive functions, cognitive performance, working memory, Sternberg task, probed recall, verbal fluency, psychomotor vigilance test (PVT), digit–symbol substitution task (DSST), subjective sleepiness, total sleep deprivation Citation: Tucker AM; Whitney P; Belenky G; Hinson JM; Van Dongen HPA. Effects of sleep deprivation on dissociated components of executive functioning. SLEEP 2010;33(1):47-57. 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 Submitted for publication February, 2009 Submitted in final revised form July, 2009 Accepted for publication September, 2009 Address correspondence to: Hans P.A. Van Dongen, PhD, Sleep and Performance Research Center, Washington State University Spokane, P.O. Box 1495, Spokane, WA 99210-1495; Tel: (509) 358-7755; Fax: (509) 358-7810; E-mail: SLEEP, Vol. 33, No. 1, 2010 47 Sleep Deprivation and Executive Functioning—Tucker et al 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 amp (...truncated)