Skip to main content
SpringerLink
Log in

Impact of total sleep deprivation on behavioural neural processing of emotionally expressive faces

Experimental Brain Research Aims and scope Submit manuscript

Cite this article

Abstract

Sleep deprivation impacts subjective mood states, but very little research has examined the impact on processing emotional information. In the current study, we investigated the impact of total sleep deprivation on neural responses to emotional facial expressions as well as the accuracy and speed with which these faces were categorized. Forty-nine participants completed two tasks in which they were asked to categorize emotional facial expressions as Happy, Sad, Angry, or Fearful. They were shown the ‘full’ expression of the emotions in one task and more subtle expressions in a second task in which expressions were ‘morphed’ with neutral faces so that the intensity of emotion varied. It was expected that sleep deprivation would lead to greater reactivity (indexed by larger amplitude N170 event-related potentials), particularly for negative and more subtle facial expressions. In the full face task, sleep-deprived (SD) participants were significantly less accurate than controls (C) at identifying Sad faces and slower to identify all emotional expressions. P1 was smaller and N170 was larger for the SD compared to C group, but for all emotions, indicating generalized impairment in low-level visual processing. In the more difficult morphed face task, SD participants were less accurate than C participants for Sad faces; as well, the group difference in reaction time was greatest for Sad faces. For the SD group, N170 increased in amplitude with increasing perceptual difficulty for the Fearful and Angry faces, but decreased in amplitude with increasing difficulty for Sad faces. These data illustrate that sleep deprivation led to greater neural reactivity for the threat-related negative emotions as they became more subtle; however, there was a failure to engage these perceptual resources for the processing of Sad faces. Sleep loss preferentially impacted the processing of Sad faces; this has widespread implications for sleep-deprived groups.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Adolphs R (2002) Recognizing emotions from facial expressions: psychological and neurological mechanisms. Behav Cog Neurosci Rev 1:21–62

    Article  Google Scholar 

  • Batty M, Taylor MJ (2003) Early processing of the six basic facial emotional expressions. Cog Brain Res 17:613–620

    Article  Google Scholar 

  • Bentin S, Golland Y (2002) Meaningful processing of meaningless stimuli: the influence of perceptual experience on early visual processing of stimuli. Cognition 86:B1–B14

    Article  PubMed  Google Scholar 

  • Blau VC, Maurer U, Tottenham N, McCandliss BD (2007) The face-specific N170 component is modulated by emotional facial expression. Behav Brain Funct 3:1–13

    Article  Google Scholar 

  • Bullock M, Russell JA (1984) Preschool children’s interpretation of facial expressions of emotion. Int J Behav Dev 7:193–214

    Article  Google Scholar 

  • Colrain IM, Campbell KB (2007) The use of evoked potentials in sleep research. Sleep Med Rev 11:277–293

    Article  PubMed Central  PubMed  Google Scholar 

  • Cote KA, McCormick CM, Geniole SN, Renn RP, MacAulay SD (2013) Sleep deprivation lowers aggression and testosterone in men. Biol Psych 92:249–256

    Article  Google Scholar 

  • Eimer M (2000) The face-specific N170 component reflects late stages in the structural encoding of faces. Neuro Rep 11:2319–2324

    CAS  Google Scholar 

  • Ekman P, Friesen WV, Tompkins SS (1971) Facial affect scoring technique: a first validity study. Semiotica 3:37–47

    Article  Google Scholar 

  • Franzen PL, Buysse DJ, Dahl RE, Thompson W, Siegle GJ (2009) Sleep deprivation alters pupillary reactivity to emotional stimuli in healthy young adults. Biol Psych 80:300–305

    Article  Google Scholar 

  • George N, Jemel B, Fiori N, Chaby L, Renault B (2005) Electrophysiological correlates of facial decision: insights from upright and upside-down Mooney-face perception. Cog Brain Res 24:663–673

    Article  Google Scholar 

  • Goel N, Rao H, Durmer JS, Dinges DF (2009) Neurocognitive consequences of sleep deprivation. Semin Neurol 29:320–339

    Article  PubMed Central  PubMed  Google Scholar 

  • Gujar N, Yoo S, Hu P, Walker MP (2011) Sleep deprivation amplifies reactivity of brain reward networks biasing the appraisal of positive emotional experiences. J Neurosci 31:4466–4474

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Harrison Y, Horne JA (2000) The impact of sleep deprivation on decision making: a review. J Exp Psychol 6:236–249

    CAS  Google Scholar 

  • Haxby JV, Hoffman EA, Gobbini MI (2002) The distributed human neural system for face perception. Trends Cog Sci 4:223–233

    Article  Google Scholar 

  • Huck NO, McBride SA, Kendall AP, Grugle NL, Killgore WDS (2008) The effects of modafinil, caffeine, and dextroamphetamine on judgments of simple versus complex emotional expressions following sleep deprivation. Int J Neurosci 118:487–502

    Article  CAS  PubMed  Google Scholar 

  • Humphrey DG, Kramer AF, Stanny RR (1994) Influence of extended wakefulness on automatic and nonautomatic processing. Hum Factors 36:652–669

    CAS  PubMed  Google Scholar 

  • Itier RJ, Taylor MJ (2004) N170 or N1? Spatiotemporal differences between object and face processing using ERPs. Cereb Cortex 14:132–142

    Article  PubMed  Google Scholar 

  • Jacques C, d’Arripe O, Rossion B (2007) The time course of the inversion effect during individual face discrimination. J Vis 7:1–9

    Article  Google Scholar 

  • Killgore WDS (2010) Effects of sleep deprivation on cognition. Prog Brain Res 185:105–129

    Article  PubMed  Google Scholar 

  • Macchi Cassia V, Kuefner D, Westerlund A, Nelson CA (2006) The role of vertical symmetry and up-down featural arrangement. J Cog Neurosci 18:1343–1358

    Article  Google Scholar 

  • Meaux E, Roux S, Batty M (2013) Early visual ERPs are influenced by individual emotional skills. Soc Cogn Affect Neurosci [Epub ahead of print]

  • Mondloch CJ, Segalowitz SJ, Lewis TL, Dywan J, Le Grand R, Maurer D (2013) The effect of early visual deprivation on the development of face detection. Dev Sci. doi:10.1111/desc.12065

  • Pallesen S, Johnsen BH, Hansen A, Eid J, Thayer JF, Olsen T, Hugdahl K (2004) Sleep deprivation and hemispheric asymmetry for facial recognition reaction time and accuracy. Percept Motor Skills 98:1305–1314

    PubMed  Google Scholar 

  • Patrick GTW, Gilbert JA (1896) On the effects of loss of sleep. Psych Rev 3:469–483

    Article  Google Scholar 

  • Pilcher JJ, Huffcutt AJ (1996) Effects of sleep deprivation on performance: a meta-analysis. Sleep 19:318–326

    CAS  PubMed  Google Scholar 

  • Renn RP, Cote KA (2013) Performance monitoring following total sleep deprivation: effects of task type and error rate. Int J Psychophys 88:64–73

    Article  Google Scholar 

  • Rosales-Lagarde A, Armony JL, Del Río-Portilla Y, Trejo-Martínez D, Conde R, Corsi-Cabrera M (2012) Enhanced emotional reactivity after selective REM sleep deprivation in humans: an fMRI study. Front Behav Neurosci 18(6):25

    Google Scholar 

  • Rossion B, Caharel S (2011) ERP evidence for the speed of face categorization in the human brain: disentangling the contribution of low-level visual cues from face perception. Vis Res 51:1297–1311

    Article  PubMed  Google Scholar 

  • Rossion B, Jacques C (2008) Does physical interstimulus variance account for early electrophysiological face sensitive responses in the human brain? Ten lessons on the N170. Neuroimage 39:1959–1979

    Article  PubMed  Google Scholar 

  • Rossion B, Jacques C (2012) The N170: understanding the time-course of face perception in the human brain. In: Luck S, Kappenman E (eds) The Oxford handbook of ERP components. Oxford University Press, Oxford, pp 115–142

    Google Scholar 

  • Rossion B, Gauthier I, Tarr MJ, Despland P, Bruyer R, Linotte S, Crommelinck M (2000) The N170 occipito-temporal component is delayed and enhanced to inverted faces but not to inverted objects: an electrophysiological account of face-specific processes in the human brain. Neuro Rep 11:69–72

    CAS  Google Scholar 

  • Rousselet GA, Husk JS, Bennett PJ, Sekuler AB (2008) Time course and robustness of ERP object and face differences. J Vis 8:1–18

    Article  Google Scholar 

  • Russell JA (1994) Is there universal recognition of emotion from facial expression? A review of the cross-cultural studies. Psychol Bull 115:102–141

    Article  CAS  PubMed  Google Scholar 

  • Sadeh B, Yovel G (2010) Why is the N170 enhanced for inverted faces? An ERP competition experiment. Neuroimage 53:782–789

    Article  PubMed  Google Scholar 

  • Tempesta A, Couyoumdjian A, Curcio G, Moroni F, Marzano C, De Gennaro L, Ferrara M (2010) Lack of sleep affects the evaluation of emotional stimuli. Brain Res Bull 82:104–108

    Article  PubMed  Google Scholar 

  • Tottenham N, Tanaka JW, Leon AC, McCarry T, Nurse M, Hare TA, Nelson C (2009) The NimStim set of facial expressions: judgments from untrained research participants. Psychiatry Res 168:242–249

    Article  PubMed Central  PubMed  Google Scholar 

  • van der Helm E, Gujar N, Walker M (2010) Sleep deprivation impairs the accurate recognition of human emotions. Sleep 33:335–342

    PubMed Central  PubMed  Google Scholar 

  • Yoo S-S, Gujar N, Hu P, Jolesz FA, Walker MP (2007) The human emotional brain without sleep—a prefrontal amygdala disconnect. Current Biol 17:877–878

    Article  Google Scholar 

  • Zheng X, Mondloch CJ, Nishimura M, Vida M, Segalowitz S (2011) Telling one face from another: electrocortical correlates of individual facial characteristics. Neuropsycologia 49:3254–3264

    Article  Google Scholar 

  • Zheng X, Mondloch CJ, Segalowitz S (2012) The timing of individual face recognition in the brain. Neuropsychologia 50:1451–1461

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This research was carried out in the Brock University Sleep Research Laboratory, which is funded by the Natural Science and Engineering Research Council (NSERC) of Canada. Face stimuli were created in C. Mondloch’s Face Perception Lab through support by an Insight Grant from the Social Science and Humanities Research Council (SSHRC) of Canada.

Author information

Authors and Affiliations

  1. Department of Psychology, Brock University, 500 Glenridge Ave., St. Catharines, ON, L2S 3A1, Canada

    K. A. Cote, C. J. Mondloch, V. Sergeeva, M. Taylor & T. Semplonius

Authors
  1. K. A. Cote
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. J. Mondloch
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. V. Sergeeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. Taylor
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. T. Semplonius
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to K. A. Cote.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Cote, K.A., Mondloch, C.J., Sergeeva, V. et al. Impact of total sleep deprivation on behavioural neural processing of emotionally expressive faces. Exp Brain Res 232, 1429–1442 (2014). https://doi.org/10.1007/s00221-013-3780-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-013-3780-1

Keywords

search

Navigation