Abstract
Whether and how sleep loss affects executive functioning are still under debate. In this study, we examined the role of individual differences in determining the levels of working memory (WM) efficiency and proactive interference (PI) after sleep deprivation. Fifty-two participants performed a test battery included a modified Sternberg task and the Jonides’ 2-back task under two sleep conditions: baseline (BL, a night of regular sleep), and total sleep deprivation (SD, 24 h of wakefulness). In general, we replicated Tucker and colleagues’ (2010) results. However, when we divided the subjects into two groups according to WM efficiency after SD, participants that showed a greater efficiency were more susceptible to PI, while those with lower WM efficiency showed a level of resistance to PI similar to BL. These results indicate that resistance to PI after SD is dependent on WM efficiency, highlighting the importance of individual differences in sleep deprivation studies.
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Abbreviations
- BL:
-
Baseline
- SD:
-
Sleep deprivation
- M:
-
Mean
- std:
-
Standard deviation
- SSS:
-
Stanford Sleepiness Scale
- GVAS:
-
Global Vigor–Affect Scale
- VAS:
-
Visual Analog Scale
- NT:
-
Non-target
- T:
-
Target
- ANOVA:
-
Analysis of variance
- Mdn:
-
Median
- RT:
-
Reaction times
- PE:
-
Preserved-efficiency group
- WE:
-
Worsened-efficiency group
- WM:
-
Working memory
- PI:
-
Proactive interference
References
Alvarez, J. A., & Emory, E. (2006). Executive function and the frontal lobes: A meta-analytic review. Neuropsychology Review, 16(1), 17–42. https://doi.org/10.1007/s11065-006-9002-x.
Baddeley, A. (2003). Working memory: Looking back and looking forward. Nature Reviews Neuroscience, 4(October), 829–839. https://doi.org/10.1038/nrn1201.
Basner, M., & Dinges, D. F. (2011). Maximizing sensitivity of PVT to sleep loss. Sleep, 34(5), 581–591.
Bunge, S. A., Ochsner, K. N., Desmond, J. E., Glover, G. H., & Gabrieli, J. D. (2001). Prefrontal regions involved in keeping information in and out of mind. Brain: A Journal of Neurology, 124(Pt 10), 2074–2086. https://doi.org/10.1093/brain/124.10.2074.
Bunting, M. (2006). Proactive interference and item similarity in working memory. Journal of Experimental Psychology: Learning, Memory and Cognition, 32(2), 183–196. https://doi.org/10.1037/0278-7393.32.2.183.
Buysse, D. J., Reynolds, C. F., Monk, T. H., Berman, S. R., & Kupfer, D. J. (1989). The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Research, 28(2), 193–213. https://doi.org/10.1016/0165-1781(89)90047-4.
Chan, R. C. K., Shum, D., Toulopoulou, T., & Chen, E. Y. H. (2008). Assessment of executive functions: Review of instruments and identification of critical issues. Archives of Clinical Neuropsychology, 23(2), 201–216. https://doi.org/10.1016/j.acn.2007.08.010.
Chee, M. W. L., & Tan, J. C. (2010). Lapsing when sleep deprived: Neural activation characteristics of resistant and vulnerable individuals. NeuroImage, 51(2), 835–843. https://doi.org/10.1016/j.neuroimage.2010.02.031.
Chee, M. W. L., Chuah, L. Y. M., Venkatraman, V., Chan, W. Y., Philip, P., & Dinges, D. F. (2006). Functional imaging of working memory following normal sleep and after 24 and 35 h of sleep deprivation: Correlations of fronto-parietal activation with performance. NeuroImage, 31(1), 419–428. https://doi.org/10.1016/j.neuroimage.2005.12.001.
Chiappe, P., Hasher, L., & Siegel, L. (2000). Working memory, inhibitory control and reading disability. Memory & Cognition, 28(1), 8–17.
Choo, W. C., Lee, W. W., Venkatraman, V., Sheu, F. S., & Chee, M. W. L. (2005). Dissociation of cortical regions modulated by both working memory load and sleep deprivation and by sleep deprivation alone. NeuroImage, 25(2), 579–587. https://doi.org/10.1016/j.neuroimage.2004.11.029.
Chuah, Y. M. L., Venkatraman, V., Dinges, D. F., & Chee, M. W. L. (2006). The neural basis of interindividual variability in inhibitory efficiency after sleep deprivation. The Journal of Neuroscience, 26(27), 7156–7162. https://doi.org/10.1523/JNEUROSCI.0906-06.2006.
Cui, J., Tkachenko, O., Gogel, H., Kipman, M., Preer, L. A., Weber, M., et al. (2015). NeuroImage microstructure of frontoparietal connections predicts individual resistance to sleep deprivation. NeuroImage, 106, 123–133. https://doi.org/10.1016/j.neuroimage.2014.11.035.
Damasio, A. R. (1994). Descartes’ error: Emotion, reason, and the human brain. New York: Grosset/Putnam.https://doi.org/10.7202/051028ar
del Angel, J., Cortez, J., JuÁrez, D., Guerrero, M., GarcÍa, Aí, RamÍrez, C., et al. (2015). Effects of sleep reduction on the phonological and visuospatial components of working memory. Sleep Science, 8(2), 68–74. https://doi.org/10.1016/j.slsci.2015.06.001.
Dinges, D. F., Pack, F., Williams, K., Gillen, K. A., Powell, J. W., Ott, G. E., Pack, A. I. (1997). Cumulative sleepiness, mood disturbance and psychomotor vigilance performance decrements during aweek of sleep restricted to 4–5 hours per night. Sleep: Journal of Sleep Research & Sleep Medicine, Vol. 20, pp. 267–277. US: American Academy of Sleep Medicine.
Doran, S. M., Van Dongen, H. P. A., & Dinges, D. F. (2001). Susteined attention performance during sleep deprivation: Evidence of state instability. Archives Italiennes de Biologie, 139, 253–267.
Drummond, S. P. A., Paulus, M. P., & Tapert, S. F. (2006). Effects of two nights sleep deprivation and two nights recovery sleep on response inhibition. Journal of Sleep Research, 15(3), 261–265. https://doi.org/10.1111/j.1365-2869.2006.00535.x.
Engle, R. W. (2002). Working memory capacity as executive attention. Current Directions in Psychological Science, 11(1), 19–23. https://doi.org/10.1111/1467-8721.00160.
Fournier, L. R., Hansen, D. A., Stubblefield, A. M., & Van Dongen, H. P. A. (2018). Action plan interrupted: Resolution of proactive interference while coordinating execution of multiple action plans during sleep deprivation. Psychological Research Psychologische Forschung. https://doi.org/10.1007/s00426-018-1054-z.
Friedman, N. P., & Miyake, A. (2004). The relations among inhibition and interference control functions: A latent-variable analysis. Journal of Experimental Psychology: General, 133(1), 101–135. https://doi.org/10.1037/0096-3445.133.1.101.
Gerhardsson, A., Åkerstedt, T., Axelsson, J., Fischer, H., Lekander, M., & Schwarz, J. (2018). Effect of sleep deprivation on emotional working memory. Journal of Sleep Research, (May). https://doi.org/10.1111/jsr.12744
Grafman, J., & Litvan, I. (1999). Importance of deficits in executive functions. Lancet, 354(9194), 1921–1923. https://doi.org/10.1016/S0140-6736(99)90438-5.
Harrison, Y., & Horne, J. A. (1998). Sleep loss impairs short and novel language tasks having a prefrontal focus. Journal of Sleep Research, 7(2), 95–100. https://doi.org/10.1046/j.1365-2869.1998.00104.x.
Harrison, Y., & Horne, J. A. (2000). The impact of sleep deprivation on decision making: A review. Journal of Experimental Psychology. Applied, 6(3), 236–249. https://doi.org/10.1037/1076-898X.6.3.236.
Hasher, L., & Zacks, R. T. (1988). Working memory, comprehension, and aging: A review and a new view. In G. H. Bower (Ed.), The Psychology of learning and motivation (Vol. 22, pp. 193–225). New York: Academic Press.
Hoddes, E., Zarcone, V., Smythe, H., Phillips, R., & Dement, W. C. (1973). Quantification of sleepiness: A new approach. Psychophysiology, 10, 431–436. https://doi.org/10.1111/j.1469-8986.1973.tb00801.x.
Horne, J. A., & Ostberg, O. (1976). A self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms. International Journal of Chronobiology, 4, 97–110. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/1027738
Jonides, J., Schumacher, E. H., & Smith, E. E. (1997). Verbal working memory load affects regional brain activation as mesured by PET. Journal of Cognitive Neuroscience, 9, 462–475.
Kane, M. J., & Engle, R. W. (2000). Working-memory capacity, proactive interference, and divided attention: Limits on long-term memory retrieval. Journal of Experimental Psychology. Learning, Memory, and Cognition, 26(2), 336–358. https://doi.org/10.10371/0278-7393.26.2.336
Kareken, D. A., Moberg, P. J., & Gur, R. C. (1996). Proactive inhibition and semantic organization relationship with verbal memory in patients with schizophrenia. Journal of the International Neuropsychological Society, 2(6), 486–493. https://doi.org/10.1017/s135561770000165x.
Keppel, G., & Underwood, B. J. (1962). Proactive inhibition in short-term retention of single items. Journal of Verbal Learning and Verbal Behavior, 1, 153–161. https://doi.org/10.1016/S0022-5371(62)80023-1.
Kliegl, O., Pastötter, B., & Bäuml, K. H. T. (2015). The contribution of encoding and retrieval processes to proactive interference. Journal of Experimental Psychology: Learning Memory and Cognition, 41(6), 1778–1789. https://doi.org/10.1037/xlm0000096.
Lilienthal, L., Rose, N. S., Tamez, E., Myerson, J., & Hale, S. (2015). Individuals with low working memory spans show greater interference from irrelevant information because of poor source monitoring, not greater activation. Memory & Cognition, 43(3), 357–366. https://doi.org/10.3758/s13421-014-0465-3.
Lim, J., & Dinges, D. F. (2008). Sleep deprivation and vigilant attention. Annals of the New York Academy of Sciences, 1129, 305–322. https://doi.org/10.1196/annals.1417.002.
Lim, J., Choo, W., & Chee, M. W. L. (2007). Reproducibility of changes in behaviour and fMRI activation associated with sleep deprivation in a working memory task. Sleep, 30(1), 61–70.
Lustig, C., May, C., & Hasher, L. (2001). Working memory span and role of proactive interference. Journal of Experimental Psychology: General, 130(2), 199–207.
Lythe, K. E., Williams, S. C. R., Anderson, C., Libri, V., & Mehta, M. A. (2012). Frontal and parietal activity after sleep deprivation is dependent on task difficulty and can be predicted by the fMRI response after normal sleep. Behavioural Brain Research, 233(1), 62–70. https://doi.org/10.1016/j.bbr.2012.04.050.
Martínez-Cancino, D., Azpiroz, J., & Jiménez-Angeles, L. (2015). The effects of sleep deprivation in working memory using the N-back task. In IFMBE Proceedings (Vol. 49). https://doi.org/10.1007/978-3-319-13117-7_108
Miyake, A., Friedman, N. P., Emerson, M. J., Witzki, A. H., Howerter, A., & Wager, T. D. (2000). The unity and diversity of executive functions and their contributions to complex “Frontal Lobe” tasks: A latent variable analysis. Cognitive Psychology, 41(1), 49–100. https://doi.org/10.1006/cogp.1999.0734.
Monk, T. H. (1989). A visual analogue scale technique to measure global vigor and affect. Psychiatry Research, 27(1), 89–99. https://doi.org/10.1016/0165-1781(89)90013-9.
Owen, A. M., McMillan, K. M., Laird, A. R., & Bullmore, E. (2005). N-back working memory paradigm: A meta-analysis of normative functional neuroimaging studies. Human Brain Mapping, 25(1), 46–59. https://doi.org/10.1002/hbm.20131.
Rohrer, D. (1996). On the relative and absolute strength of a memory trace. Memory and Cognition, 24(2), 188–201. https://doi.org/10.3758/BF03200880.
Rosen, V. M., & Engle, R. W. (1998). Working memory capacity and suppression. Journal of Memory and Language, 39(3), 418–436. https://doi.org/10.1006/jmla.1998.2590.
Rupp, T. L., Wesensten, N. J., & Balkin, T. J. (2012). Trait-like vulnerability to total and partial sleep loss. Sleep, 35(8), 1163–1172. https://doi.org/10.5665/sleep.2010.
Sagaspe, P., Sanchez-Ortuno, M., Charles, A., Taillard, J., Valtat, C., Bioulac, B., et al. (2006). Effects of sleep deprivation on color-word, emotional, and specific stroop interference and on self-reported anxiety. Brain and Cognition, 60(1), 76–87. https://doi.org/10.1016/j.bandc.2005.10.001.
Schaedler, T., Santos, J. S., Vincenzi, R. A., Isabel, S., Pereira, R., & Louzada, F. M. (2018). Executive functioning is preserved in healthy young adults under acute sleep restriction. Sleep Science, 11(3), 152–159. https://doi.org/10.5935/1984-0063.20180029.
Slama, H., Chylinski, D. O., Deliens, G., Leproult, R., Schmitz, R., & Peigneux, P. (2018). Sleep deprivation triggers cognitive control impairments in task-goal switching. Sleep, 41(2), 1–12. https://doi.org/10.1093/sleep/zsx200.
Smith, E. E., & Jonides, J. (1999). Storage and executive processes in the frontal lobes. Science, 283, 1657–1661. Retrieved from https://www.sciencedirect.com/science/article/pii/095943889390204C.
Steer, R. A., Ball, R., Ranieri, W. F., & Beck, A. T. (1997). Further evidence for the construct validity of the Beck Depression Inventory-II with psychiatric outpatients. Psychological Reports, 80(2), 443–446. https://doi.org/10.2466/pr0.1997.80.2.443.
Sternberg, S. (1966). High-speed scanning in human memory. Science, 153(3736), 652–654. Retrieved from https://www.jstor.org/stable/1719418
Thomas, M. L., Sing, H. C., Belenky, G., Holcomb, H. H., Mayberg, H. S., Dannals, R. F., et al. (2000). Neural basis of alertness and cognitive performance impairments during sleepiness II. Effects of 48 and 72 h of sleep deprivation on waking human regional brain activity. Journal of Sleep Research, 9, 335–352. https://doi.org/10.1016/S1472-9288(03)00020-7.
Tkachenko, O., & Dinges, D. F. (2018). Interindividual variability in neurobehavioral response to sleep loss: A comprehensive review. Neuroscience and Biobehavioral Reviews, 89(October 2017), 29–48. https://doi.org/10.1016/j.neubiorev.2018.03.017
Tucker, A. M., Whitney, P., Belenky, G., Hinson, J. M., & Van Dongen, H. P. A. (2010). Effects of sleep deprivation on dissociated components of executive functioning. Sleep, 33(1), 47–57. Retrieved from https://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2802247&tool=pmcentrez&rendertype=abstract
Van Dongen, H. P. A., Baynard, M. D., Maislin, G., & Dinges, D. F. (2004). Systematic interindividual differences in neurobehavioral impairment from sleep loss: Evidence of trait-like differential vulnerability. Sleep, 27(3), 423–433.
Wu, J. C., Gillin, J. C., Buchsbaum, M. S., Chen, P., Keator, D. B., Khosla, W. N., et al. (2006). Frontal lobe metabolic decreases with sleep deprivation not totally reversed by recovery sleep. Neuropsychopharmacology, 31(12), 2783–2792. https://doi.org/10.1038/sj.npp.1301166.
Xu, J., Zhu, Y., Fu, C., Sun, J., Li, H., Yang, X., et al. (2016). Frontal metabolic activity contributes to individual differences in vulnerability toward total sleep deprivation-induced changes in cognitive function. Journal of Sleep Research, 25(2), 169–180. https://doi.org/10.1111/jsr.12354.
Yeo, B. T. T., Tandi, J., & Chee, M. W. L. (2015). Functional connectivity during rested wakefulness predicts vulnerability to sleep deprivation. NeuroImage, 111(1), 147–158. https://doi.org/10.1016/j.neuroimage.2015.02.018.
Acknowledgements
We gratefully thank Alessia Sassano, Virginia Veruma, Daniela Zarbo and Nicolò Zorzetto for their contribution in data collection. We are indebted to the two anonymous reviewers for providing insightful comments on earlier versions of this manuscript.
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This work was supported by a grant from the Swiss National Science Foundation (grant number 320030_182589).
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Riontino, L., Cavallero, C. Individual differences in working memory efficiency modulate proactive interference after sleep deprivation. Psychological Research 85, 480–490 (2021). https://doi.org/10.1007/s00426-020-01292-6
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DOI: https://doi.org/10.1007/s00426-020-01292-6