Social Experience and Personality Affect Resilience to Sleep Deprivation

IN THIS ISSUE OF SLEEP, RUPP AND COLLEAGUES¹ DESCRIBE FOR THE FIRST TIME THE INTERACTIVE EFFECTS OF WAKING SOCIAL EXPERIENCE AND individual personality traits on vulnerability to subsequent sleep loss. Forty-eight men and women aged 18–39 years underwent a 36-h sleep deprivation protocol. They were selected with respect to extraversion vs. introversion criteria, among others, and then randomly assigned to a 12-h socially enriched or impoverished condition, followed by 22 h of supplementary extended wakefulness, during which performance and alertness were tested throughout. The authors did not observe any main effect of either social exposure or personality trait alone on performance and alertness during sleep deprivation. However, they describe that extraverts exposed to socially enriched environments show greater vulnerability to subsequent sleep loss than introverts, at certain circadian times, and that they are less resilient than extraverts exposed to an identical but impoverished environment. In contrast, the ability of introverts to resist sleep loss was relatively unaffected by the social environment.

Knowledge of the factors that determine individual vulnerability to sleep curtailment, whether these factors are genetically, environmentally or personality driven, is crucial in our increasingly sleep deprived society.² Previous studies have consistently shown important inter-individual differences, but relatively stable intra-individual response patterns to sleep deprivation.³ While there is increasing evidence that this individual vulnerability to sleep loss is partly genetically determined, such as per allele status of the PER3 clock gene,⁴ very little is known to date about the role of individual personality traits in resilience to sleep loss. Furthermore, animal research indicates that social exposure may affect sleep homeostasis (i.e., it may significantly increase sleep need and thus affect the ability to stay alert during extended wakefulness).⁵ However, few studies in humans have investigated the role of social stimulation on sleep function and vulnerability to sleep loss. It is the innovative approach of Rupp and colleagues¹ to assess for the first time the single and combined effect of personality trait and social exposure on performance and alertness during sleep deprivation. Their results have implications at a societal level, given the putative decrease in sleep duration over the past decades,² but they may be particularly relevant for specific populations that frequently experience acute or chronic sleep deprivation and high social exposure, such as medical personnel, shift workers, or parents of young children.

A socially enriched environment negatively affects resilience to sleep deprivation in extraverts, but not in introverts. This result may be counterintuitive to some, but was it to be expected? Indeed, Eysenck had theorized that the personality trait of introversion-extraversion would be related to cortical arousal.⁶ This has been supported by functional neuroimaging studies demonstrating that introverts display greater activation of the prefrontal cortex in the resting state.⁷ As optimal levels of performance are suggested to arise at moderate levels of arousal (see also Figure 1¹), introverts may inadvertently avoid social stimulation to prevent excessive cortical arousal, while extraverts seek social stimulation to increase arousal to optimal levels. Greater baseline activation of the prefrontal cortex as seen in introverts has been directly linked to higher resilience to sleep loss,⁸ and individuals that are genetically more resilient to sleep deprivation (being homozygous for the 5-repeat allele of PER3) may sustain this activation following sleep loss.⁹ Consistent with these findings, Rupp and colleagues had previously demonstrated a greater resistance to the effects of sleep loss in introverts, but there was a possible bias in terms of social exposure.¹⁰ By differentially modeling social experience in the present study, it would thus be expected that extraverts in particular would decline in performance and alertness under sleep deprivation following social exposure.

One important aspect of the present data from Rupp et al.¹ that could have been stated more clearly is the importance of circadian modulation. Indeed, time of day (factor “session” in the mixed model ANOVA employed in this study, see Table 3) displays a significant main effect on all outcome measures (psychomotor vigilance—speed and lapses, sleep latency—as per modified maintenance of wakefulness test, subjective sleepiness—as per Stanford Sleepiness Scale) during sleep deprivation. As such, performance does not decline gradually as a function of prior wake time, but undergoes circadian modulation, with its nadir around the circadian trough and subsequent improvement. It has been shown by our group and others that circadian modulation contributes substantially to a multitude of physiological and behavioral parameters, such as mood, sleepiness, and neurobehavioral performance.¹¹ In the present study, the greater vulnerability to sleep deprivation after social exposure in extraverts is directly influenced by circadian phase, as the significant decline in PVT speed and lapses in extraverts is revealed at the circadian trough, between 4 and 6 am. Rupp and colleagues have thoroughly excluded extreme chronotypes from the present study¹ as well as subjects with extreme sleep needs (habitual long or short sleepers) in order to minimize bias. However, previous studies consistently show extraversion being associated with evening chronotype,¹² and circadian preference of the evening type has been linked to lower levels of sleep pressure and a decreased build-up of the homeostatic process S during extended wakefulness.¹³ Minor differences in terms of diurnal preference may thus confound effects on performance after sleep deprivation. The interdependency of personality, social exposure, sleep deprivation, and circadian phase on performance is complex, but may be particularly relevant to an increasing population of shift workers, representing currently between 15% and 30% of the work force. These complex interactions warrant further investigations using highly controlled circadian protocols such as the constant routine protocol.

The common notion that social interaction may help sustain alertness and prevent from falling asleep is not supported by the data of Rupp et al.¹ Interestingly, subjects in the socially enriched condition felt overall less sleepy during the day (higher scores on the Stanford Sleepiness Scale), but were objectively sleepier (shorter sleep latency on the MWT). This may be an indication that daytime sleepiness may be underestimated under socially enriched conditions.

The findings of Rupp and colleagues presented in this issue of SLEEP pave the way for a new line of research investigating the interactions of waking social experience and individual personality traits on vulnerability to sleep deprivation. Among the many questions that remain to be answered: how does social exposure affect sleep physiology and sleep need in humans? In analogy to the findings in animals, we would expect a subsequent increase in sleep need that may be reflected by greater performance vulnerability, but above all by an increase in slow wave activity during recovery sleep—which was not observed in the current data set and thus awaits replication. Furthermore, what is the exact nature of the circadian differences among extraverts and introverts? Are there any cultural differences modulating the effect of social exposure and personality trait on sleep loss vulnerability? How do the abovementioned factors interact with chronic partial sleep deprivation or with prolonged sleep deprivation? Are there any age or gender effects of the observed findings? Overall, a better understanding of the complex interaction of personality trait, social exposure, and circadian phase on performance and alertness will contribute to our understanding of factors that determine individual differences in vulnerability to sleep deprivation—and will thus enable the development of individually targeted interventions to prevent negative outcomes of sleep curtailment.

DISCLOSURE STATEMENT

Dr. Schröder has indicated no financial conflicts of interest.