Do Evoked Potential Differences Reflect a Deficit in Those Suffering a Sleep Disorder, or Resilience in Those Who Can Avoid it?

THE CONSTANT DEMANDS MADE BY OUR 24/7 LIFESTYLE REQUIRE AN EVER INCREASING PROPORTION OF THE WORKFORCE TO ENGAGE IN SOME FORM of shift work. On the face of it, the development of a Shift Work Sleep Disorder (SWSD) would seem the logical outcome of these work habits. The work schedule experienced by shift workers leads them to attempt sleep in opposition to both homeostatic and circadian sleep regulatory mechanisms. This should logically lead to poor sleep, daytime sleepiness and poor sleep satisfaction. The fact that shift workers experiencing SWSD show abnormalities in neurophysiological measures of attention is an important finding, but again, one that should not be unexpected. The novel approach taken by Gumenyuk and colleagues in this issue of SLEEP1 has produced interesting and novel data about SWSD, specifically, the absence of a difference in N1, the appearance of a right hemisphere specific difference in the mismatch negativity (MMN), and an enhanced P3a to novel stimuli in the SWSD group. Gumenyuk et al.1 point to the enhanced P3a in the SWSD group as evidence of hyper arousal and a relative inability to screen out potentially distracting or arousing stimuli that could then disrupt sleep. There are some other data showing electrophysiological evidence in insomniacs supportive of this hypothesis. For example Milner et al.2 reported reduced gating of auditory stimuli during wakefulness as indicated by a lack of reduction in the amplitude of P50 to the second of a pair of auditory click stimuli. Indeed, Turcotte and Bastien have recently hypothesized that underlying neurophysiological mechanisms of chronic insomnia involves both hyper arousal and inhibition deficits,3 with the increased arousal hypothesis supported by an increase in N1 during wakefulness (not seen in SWSD by Gumenyuk et al.1), and the reduced inhibition supported by reduced N350 in early sleep.4 The differential sensitivity of right hemisphere for the MMN seen by Gumenyuk et al.1 is partially supportive of the right hemisphere sensitivity for a reduced P300 after a week of sleep restriction.5 While the P300 in that study was the more traditionally reported as target related P3b, it shares many of the same underlying neurophysiology as the P3a.6 The data presented in Table 1 by Gumenyuk et al.,1 show that SWSD night workers to have significantly lower sleep efficiency (84% vs. 90%), significantly less time asleep in naps (33.9 vs. 38.4 minutes.), and around 36 minutes less total sleep time (6.0 vs. 6.6 hours) than healthy night workers. At one level of analysis, these data could be used to explain the MMN and P3a differences between the groups. However, the difference between the two night worker groups is small compared to the difference seen when comparing them to healthy day workers (who had a mean total sleep time of 8.5 hours and a mean sleep efficiency of 96%), yet there were no apparent neurophysiological difference between the healthy day workers and the healthy night workers. There is of course no biological imperative for the effect of sleep on evoked potentials to be linear, and it is possible that the relatively small differences in sleep between the SWSD and healthy night workers exceed a tipping point. However previous studies have shown significant positive relations between P3a amplitude and sleep efficiency,7 a decline in P3a amplitude with increasing sleepiness,7 and decreased P3a amplitude following sleep deprivation with recovery following a night of sleep.8 It is thus also possible that the sleep differences between the two night worker groups in the Gumenyuk et al. study1 represent another symptom of the problem rather than a cause of the evoked potential difference. While the interpretation of P300 phenomena are challenging, there are convergent data from neuroimaging studies9 that P300 represents the output of a network of cortical and subcortical regions involved in widespread cortical inhibition, presumably related to cognitive closure or termination of mental processes. As previously suggested,10 this interpretation sees P3a amplitude as reflecting the degree to which responses to irrelevant stimuli are inhibited (see review11). Therefore, an alternative explanation of the elevated P3a in the Gumenyuk et al. study1 is that the SWSD group is engaged in greater levels of inhibitory processing rather than less. This has been the interpretation of the data from alcoholics who are known to have impaired inhibitory control mechanisms, and who show reduced P3a components relative to controls.12 In the context of the Gumenyuk et al. study, one would have to hypothesize that this increased inhibitory effort, was designed to compensate for the increased sleepiness in the SWSD group, and possibly the reduced signaling of stimulus deviance as reflected by the smaller right hemisphere MMN amplitude. The resolution of whether the elevated P3a reflects increased or decreased inhibition will require further study comparing the P3a result to other measures of inhibitory processing. However, the careful methodology employed by Gumenyuk et al.1 provides reassurance that the observed result is real and amenable to investigation. While the hyper arousal-reduced inhibition hypothesis is testable, there is another potential future focus from the work not mentioned by Gumenyuk and colleagues. In my opinion, the interesting group in the experiment is the healthy night workers who neither display excessive sleepiness, nor overt insomnia symptomatology, and who do not differ from healthy day workers on the measures of neurophysiological function. This group is clearly worthy of future study. They raise a number of questions, the answers to which would be of potential scientific interest and great practical utility. Why are they able to produce better sleep? Why are they able to function well, despite still having less sleep than typically needed by day workers? What provides them with the resilience to overcome sleep dysregulation enabling them to function well in situations that should leave them sleepy, inattentive, affectively challenged and generally performing below par? Gumenyuk et al.1 have provided a great starting point for a series of worthwhile and important studies.