Sleep deprivation impairs recognition of specific emotions

William D S Killgore, Thomas J Balkin, Angela M Yarnell, Vincent F Capaldi 2nd, William D S Killgore, Thomas J Balkin, Angela M Yarnell, Vincent F Capaldi 2nd

Abstract

Emotional processing is particularly sensitive to sleep deprivation, but research on the topic has been limited and prior studies have generally evaluated only a circumscribed subset of emotion categories. Here, we evaluated the effects of one night of sleep deprivation and a night of subsequent recovery sleep on the ability to identify the six most widely agreed upon basic emotion categories (happiness, surprise, fear, sadness, disgust, anger). Healthy adults (29 males; 25 females) classified a series of 120 standard facial expressions that were computer morphed with their most highly confusable expression counterparts to create continua of expressions that differed in discriminability between emotion categories (e.g., combining 70% happiness+30% surprise; 90% surprise+10% fear). Accuracy at identifying the dominant emotion for each morph was assessed after a normal night of sleep, again following a night of total sleep deprivation, and finally after a night of recovery sleep. Sleep deprivation was associated with significantly reduced accuracy for identifying the expressions of happiness and sadness in the morphed faces. Gender differences in accuracy were not observed and none of the other emotions showed significant changes as a function of sleep loss. Accuracy returned to baseline after recovery sleep. Findings suggest that sleep deprivation adversely affects the recognition of subtle facial cues of happiness and sadness, the two emotions that are most relevant to highly evolved prosocial interpersonal interactions involving affiliation and empathy, while the recognition of other more primitive survival-oriented emotional face cues may be relatively robust against sleep loss.

Keywords: Emotion recognition; Facial expression; Perception; Sleep deprivation.

Figures

Fig. 1
Fig. 1
Example of the Emotion Hexagon Test. Participants were shown a series of 150 facial expressions that comprised morphed blends of pairs of highly confusable emotions (e.g., 70% disgust+30% sadness) for five seconds and used the computer cursor to select the most accurate label for each expression.
Fig. 2
Fig. 2
The continuum of faces used for the Emotion Hexagon Test. A total of 30 morphed faces of the same male poser were used. Each face was a morph between two neighboring faces at varying ratios (e.g., 90% happiness+10% surprise). The blended expressions are listed along the sides of the continua and the proportions of each expression included in the face are listed along the top axis.
Fig. 3
Fig. 3
The figures show the accuracy of recognition performance for each blended emotion at baseline, 23.5-h of sleep deprivation, and again following a 12-h opportunity for recovery sleep. The top panels show that sleep deprivation was associated with a significant decline in the percent of correct responses for faces with dominant expressions of happiness or sadness. None of the other emotional expressions showed significant declines in perception accuracy with sleep deprivation.

References

    1. Alves N.T., Aznar-Casanova J.A., Fukusima S.S. Patterns of brain asymmetry in the perception of positive and negative facial expressions. Laterality. 2009;14:256–272.
    1. Blair R.J. Facial expressions, their communicatory functions and neuro-cognitive substrates. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2003;358:561–572.
    1. Blasi G., Hariri A.R., Alce G. Preferential amygdala reactivity to the negative assessment of neutral faces. Biol. Psychiatry. 2009;66:847–853.
    1. Cote K.A., Mondloch C.J., Sergeeva V., Taylor M., Semplonius T. Impact of total sleep deprivation on behavioural neural processing of emotionally expressive faces. Exp. Brain Res. 2014;232:1429–1442.
    1. Cronlein T., Langguth B., Eichhammer P., Busch V. Impaired recognition of facially expressed emotions in different groups of patients with sleep disorders. PLoS One. 2016;11:e0152754.
    1. Durmer J.S., Dinges D.F. Neurocognitive consequences of sleep deprivation. Semin. Neurol. 2005;25:117–129.
    1. Ekman P. Are there basic emotions? Psychol. Rev. 1992;99:550–553.
    1. Ekman P., Friesen W.V. Consulting Psychologists Press; Palo Alto, CA: 1976. Pictures of Facial Affect.
    1. Goldstein-Piekarski A.N., Greer S.M., Saletin J.M., Walker M.P. Sleep deprivation impairs the human central and peripheral nervous system discrimination of social threat. J. Neurosci. 2015;35:10135–10145.
    1. Green M.J., Phillips M.L. Social threat perception and the evolution of paranoia. Neurosci. Biobehav. Rev. 2004;28:333–342.
    1. Gujar N., Yoo S.S., Hu P., Walker M.P. Sleep deprivation amplifies reactivity of brain reward networks, biasing the appraisal of positive emotional experiences. J. Neurosci. 2011;31:4466–4474.
    1. Huck N.O., Mcbride S.A., Kendall A.P., Grugle N.L., Killgore W.D.S. The effects of modafinil, caffeine, and dextroamphetamine on judgments of simple versus complex emotional expressions following sleep deprivation. Int. J. Neurosci. 2008;118:487–502.
    1. Kahn-Greene E.T., Killgore D.B., Kamimori G.H., Balkin T.J., Killgore W.D.S. The effects of sleep deprivation on symptoms of psychopathology in healthy adults. Sleep Med. 2007;8:215–221.
    1. Keltner D., Shiota M.N. New displays and new emotions: a commentary on Rozin and Cohen. Emotion. 2003;3:86–91. (discussion 92-96)
    1. Killgore W.D.S. Effects of sleep deprivation on cognition. Prog. Brain Res. 2010;185:105–129.
    1. Killgore W.D.S., Kahn-Greene E.T., Lipizzi E.L., Newman R.A., Kamimori G.H., Balkin T.J. Sleep deprivation reduces perceived emotional intelligence and constructive thinking skills. Sleep Med. 2008;9:517–526.
    1. Killgore W.D.S., Killgore D.B., Day L.M., Li C., Kamimori G.H., Balkin T.J. The effects of 53 h of sleep deprivation on moral judgment. Sleep. 2007;30:345–352.
    1. Killgore W.D.S., Schwab Z.J., Tkachenko O. Emotional intelligence correlates with functional responses to dynamic changes in facial trustworthiness. Soc. Neurosci. 2013;8:334–346.
    1. Kyle S.D., Beattie L., Spiegelhalder K., Rogers Z., Espie C.A. Altered emotion perception in insomnia disorder. Sleep. 2014;37:775–783.
    1. Mortillaro M., Mehu M., Scherer K. Subtly different positive emotions can be distinguished by their facial expressions. Social. Psychol. Pers. Sci. 2011;2:262–271.
    1. Pires G.N., Tufik S., Andersen M.L. Effects of REM sleep restriction during pregnancy on rodent maternal behavior. Rev. Bras. Psiquiatr. 2015;37:303–309.
    1. Shiota M.N., Campos B., Keltner D. The faces of positive emotion: prototype displays of awe, amusement, and pride. Ann. N. Y. Acad. Sci. 2003;1000:296–299.
    1. Simon E.B., Oren N., Sharon H. Losing neutrality: the neural basis of impaired emotional control without sleep. J. Neurosci. 2015;35:13194–13205.
    1. Van Der Helm E., Gujar N., Walker M.P. Sleep deprivation impairs the accurate recognition of human emotions. Sleep. 2010;33:335–342.
    1. Walker M.P. The role of sleep in cognition and emotion. Ann. N. Y. Acad. Sci. 2009;1156:168–197.
    1. Walker M.P., Van Der Helm E. Overnight therapy? The role of sleep in emotional brain processing. Psychol. Bull. 2009;135:731–748.
    1. Wells L.J., Gillespie S.M., Rotshtein P. Identification of emotional facial expressions: effects of expression, intensity, and sex on eye gaze. PLoS One. 2016;11:e0168307.
    1. West G.L., Anderson A.A., Ferber S., Pratt J. Electrophysiological evidence for biased competition in V1 for fear expressions. J. Cogn. Neurosci. 2011;23:3410–3418.
    1. Yoo S.-S., Gujar N., Hu P., Jolesz F.A., Walker M.P. The human emotional brain without sleep - a prefrontal amygdala disconnect. Curr. Biol.: CB. 2007;17:R877–R878.

Source: PubMed

Szponzorok és közreműködők

Egészségi állapot

Kábítószer-beavatkozások

3
Iratkozz fel