Abstract
Many studies have demonstrated the impairment of sustained attention due to total sleep deprivation (TSD). However, it remains unclear whether and how TSD affects the processing of visual selective attention. In the current study, 24 volunteers performed a visual search task before and after TSD over a period of 36 h while undergoing spontaneous electroencephalography. Paired-sample t-tests of behavioral performance revealed that, compared with baseline values, the participants showed lower accuracy and higher variance in response time in visual search tasks performed after TSD. Analysis of the event-related potentials (ERPs) showed that the mean amplitude of the N2-posterior-contralateral (N2pc) difference wave after TSD was less negative than that at baseline and the mean amplitude of P3 after TSD was more positive than that at baseline. Our findings suggest that TSD significantly attenuates attentional direction/orientation processing and triggers a compensatory effect in the parietal brain to partially offset the impairments. These findings provide new evidence and improve our understanding of the effects of sleep loss.
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References
Burke TM, Scheer FA, Ronda JM, Czeisler CA, Wright KP Jr (2015) Sleep inertia, sleep homeostatic and circadian influences on higher-order cognitive functions. J Sleep Res 24(4):364–371. https://doi.org/10.1111/jsr.12291
Buysse DJ, Reynolds CF, III., Monk TH, Berman SR, Kupfer DJ (1989) The Pittsburgh sleep quality index: a new instrument for psychiatric practice and research. Psychiatry Res 28(2):193–213. https://doi.org/10.1016/0165-1781(89)90047-4
Cai Y, Mai Z, Li M, Zhou X, Ma N (2021) Altered frontal connectivity after sleep deprivation predicts sustained attentional impairment: A resting-state functional magnetic resonance imaging study. J Sleep Res 30(5):e13329. https://doi.org/10.1111/jsr.13329
Chen W, Chen J, Lin X, Li P, Shi L, Liu J, Sun H, Lu L, Shi J (2018) Dissociable effects of sleep deprivation on functional connectivity in the dorsal and ventral default mode networks. Sleep Med 50:137–144. https://doi.org/10.1016/j.sleep.2018.05.040
Clark K, Appelbaum LG, van den Berg B, Mitroff SR, Woldorff MG (2015) Improvement in visual search with practice: mapping learning-related changes in neurocognitive stages of processing. J Neurosci 35(13):5351–5359. https://doi.org/10.1523/JNEUROSCI.1152-14.2015
Coull JT (1998) Neural correlates of attention and arousal: insights from electrophysiology, functional neuroimaging and psychopharmacology. Prog Neurobiol 55(4):343–361. https://doi.org/10.1016/S0301-0082(98)00011-2
Deantoni M, Villemonteix T, Balteau E, Schmidt C, Peigneux P (2021) Post-training sleep modulates topographical relearning-dependent resting state activity. Brain Sci 11(4). https://doi.org/10.3390/brainsci11040476
Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134(1):9–21. https://doi.org/10.1016/j.jneumeth.2003.10.009
Donchin E (1981) Surprise!… Surprise? Psychophysiology 18(5):493–513. https://doi.org/10.1111/j.1469-8986.1981.tb01815.x
Donchin E, Coles M (1988) Is the P300 component a manifestation of context updating? Behav Brain Sci 11(3):357–374. https://doi.org/10.1017/S0140525X00058027
Drummond SPA, Brown GG, Gillin JC, Stricker JL, Wong EC, Buxton RB (2000) Altered brain response to verbal learning following sleep deprivation. Nature 403:655–657. https://doi.org/10.1038/35001068
Gossard TR, Westerland SM, Linn-Evans M, Timm PC, Sandness DJ, Dueffert L, Louis St, E. K (2019) 0142 The cumulative effect of partial chronic sleep restriction on the neural processing stream in neurologically normal individuals. Sleep 42(Supplement1):A58–A59. https://doi.org/10.1093/sleep/zsz067.141
Gibbings A, Ray LB, Berberian N, Nguyen T, Zandi Shahidi A, Owen AM, Comeau FJE, Fogel SM (2020) EEG and behavioural correlates of mild sleep deprivation and vigilance. Clin Neurophysiol 132(1):45–55. https://doi.org/10.1016/j.clinph.2020.10.010
Gumenyuk V, Roth T, Korzyukov O, Jefferson C, Bowyer S, Drake CL (2011) Habitual Short Sleep Impacts Frontal Switch Mechanism in Attention to Novelty. Sleep 34(12):1659–1670. https://doi.org/10.5665/sleep.1430
Hamamé CM, Cosmelli D, Henriquez R, Aboitiz F (2011) Neural mechanisms of human perceptual learning: electrophysiological evidence for a two-stage process. PLoS ONE 6(4):e19221. https://doi.org/10.1371/journal.pone.0019221
Hopf JM, Luck SJ, Boelmans K, Schoenfeld MA, Boehler CN, Rieger J, Heinze HJ (2006) The neural site of attention matches the spatial scale of perception. J Neurosci 26(13):3532–3540. https://doi.org/10.1523/JNEUROSCI.4510-05.2006
Hopf JM, Luck SJ, Girelli M, Hagner T, Mangun GR, Scheich H, Heinze HJ (2000) Neural sources of focused attention in visual search. Cereb Cortex 10(12):1233–1241. https://doi.org/10.1093/cercor/10.12.1233
Hopf J, Vogel E, Woodman G, Heinze H, Luck SJ (2002) Localizing visual discrimination processes in time and space. J Neurophysiol 88(4):2088–2095. https://doi.org/10.1152/jn.2002.88.4.2088
Krause AJ, Simon EB, Mander BA, Greer SM, Saletin JM, Goldstein-Piekarski AN, Walker MP (2017) The sleep-deprived human brain. Nat Rev Neurosci 18(7):404–418. https://doi.org/10.1038/nrn.2017.55
Li C, Huang D, Qi J, Chang H, Meng Q, Wang J, Liu J, Ye E, Shao Y, Zhang X (2016) Short-term memory deficits correlate with hippocampal-thalamic functional connectivity alterations following acute sleep restriction. Brain Imaging and Behavior 11(4):954–963. https://doi.org/10.1007/s11682-016-9570-1
Lim J, Dinges DF (2008) Sleep deprivation and vigilant attention. Ann N Y Acad Sci 1129:305–322. https://doi.org/10.1196/annals.1417.002
Liu H, Li H, Wang Y, Lei X (2014) Enhanced brain small-worldness after sleep deprivation: a compensatory effect. J Sleep Res 23(5):554–563. https://doi.org/10.1111/jsr.12147
Lopez-Calderon J, Luck SJ (2014) ERPLAB: An open-source toolbox for the analysis of event-related potentials. Front Hum Neurosci 8:213. https://doi.org/10.3389/fnhum.2014.00213
Luck SJ (2005) Ten simple rules for designing ERP experiments. In: Handy TC (ed) Event-related potentials: A methods handbook. MIT Press, Cambridge, MA, pp 17–32
Luck SJ (2012) Electrophysiological correlates of the focusing of attention within complex visual scenes: N2pc and related ERP components. In: Kappenman ES, Luck SJ (eds) The Oxford Handbook of Event-Related Potential Components. Oxford University Press, Inc., New York
Luck SJ, Kappenman ES (2012) ERP components and selective attention. In: Kappenman ES, Luck SJ (eds) The Oxford Handbook of Event-Related Potential Components. Oxford University Press, Inc., New York
Mao T, Dinges D, Deng Y, Zhao K, Yang Z, Lei H, Fang Z, Yang FN, Galli O, Goel N, Basner M, Rao H (2021) Impaired vigilant attention partly accounts for inhibition control deficits after total sleep deprivation and partial sleep restriction. Nat Sci Sleep 13:1545–1560. https://doi.org/10.2147/nss.s314769
Matusz PJ, Turoman N, Tivadar RI, Retsa C, Murray MM (2019) Brain and Cognitive Mechanisms of Top-Down Attentional Control in a Multisensory World: Benefits of Electrical Neuroimaging. J Cogn Neurosci 31(3):412–430. https://doi.org/10.1162/jocn_a_01360
McMahon WR, Ftouni S, Drummond SPA, Maruff P, Lockley SW, Rajaratnam SMW, Anderson C (2018) The wake maintenance zone shows task dependent changes in cognitive function following one night without sleep. Sleep 41(10):zsy148. https://doi.org/10.1093/sleep/zsy148
Muller-Gass A, Campbell K (2019) Sleep deprivation moderates neural processes associated with passive auditory capture. Brain Cogn 132:89–97. https://doi.org/10.1016/j.bandc.2019.03.004
Muto V, Bourdiec S-L, Matarazzo A, Foret L, Mascetti A, Jaspar L, Vandewalle M, Phillips G, Degueldre C, Balteau C, Luxen E, Collette A, Maquet P (2012) Influence of acute sleep loss on the neural correlates of alerting, orientating and executive attention components. J Sleep Res 21:648–658. https://doi.org/10.1111/j.1365-2869.2012.01020.x
Pion-Tonachini L, Kreutz-Delgado K, Makeig S (2019) ICLabel: An automated electroencephalographic independent component classifier, dataset, and website. NeuroImage 198:181–197. https://doi.org/10.1016/j.neuroimage.2019.05.026
Poh JH, Chong PL, Chee MW (2016) Sleepless night, restless mind: Effects of sleep deprivation on mind wandering. J Exp Psychol Gen 145(10):1312–1318. https://doi.org/10.1037/xge0000207
Qi J, Li B, Zhang Y, Pan B, Gao Y, Zhan H, Liu Y, Shao Y, Weng X, Zhang X (2021a) Disrupted small-world networks are associated with decreased vigilant attention after total sleep deprivation. Neuroscience 471:51–60. https://doi.org/10.1016/j.neuroscience.2021a.07.010
Qi J, Li B, Zhang Y, Pan B, Gao Y, Zhan H, Liu Y, Shao Y, Zhang X (2021b) Altered functional connectivity between the nucleus basalis of Meynert and anterior cingulate cortex is associated with declined attentional performance after total sleep deprivation. Behav Brain Res 409:113321. https://doi.org/10.1016/j.bbr.2021b.113321
Qi J, Li B, Zhang Y, Pan B, Gao Y, Zhan H, Liu Y, Shao Y, Zhang X (2021c) Altered insula-prefrontal functional connectivity correlates to decreased vigilant attention after total sleep deprivation. Sleep Med 84:187–194. https://doi.org/10.1016/j.sleep.2021c.05.037
Polich J (2007) Updating P300: An integrative theory of P3a and P3b. Clin Neurophysiol 118(10):2128–2148. https://doi.org/10.1016/j.clinph.2007.04.019
Pomplun M, Silva EJ, Ronda JM, Cain SW, Münch MY, Czeisler CA, Duffy JF (2012) The effects of circadian phase, time awake, and imposed sleep restriction on performing complex visual tasks: Evidence from comparative visual search. J Vis 12(7):14–14. https://doi.org/10.1167/12.7.14
Shenfield L, Beanland V, Filtness A, Apthorp D (2020) The impact of sleep loss on sustained and transient attention: an EEG study. Peerj 8:e8960. https://doi.org/10.7717/peerj.8960
Song T, Yu K, Wang L, Xu L, Xu M, Peng Z, Dai C, Wang H, Yang T, Shao Y, Wang X, Lv J (2022) Total sleep deprivation triggers greater activation in the parietal brain in the visual working memory updating processes: An event-related potentials study. Front NeuroSci 16:736437. https://doi.org/10.3389/fnins.2022.736437
Sprecher KE, Ritchie HK, Burke TM, Depner CM, Smits AN, Dorrestein PC, Wright KP Jr (2019) Trait-like vulnerability of higher-order cognition and ability to maintain wakefulness during combined sleep restriction and circadian misalignment. Sleep 42(8):zsz113. https://doi.org/10.1093/sleep/zsz113
Su Y, Huang W, Yang N, Yan K, Ding Y, Qu Z (2020) Attentional capture by a color singleton is stronger at spatially relevant than irrelevant locations: Evidence from an ERP study. Psychophysiology 57(10):e13640. https://doi.org/10.1111/psyp.13640
Sun M, Wang E, Huang J, Zhao C, Guo J, Li D, Sun L, Du B, Ding Y, Song Y (2018) Attentional selection and suppression in children and adults. Dev Sci 21(6):e12684. https://doi.org/10.1111/desc.12684
Turcotte I, Bastien CH (2009) Is quality of sleep related to the N1 and P2 ERPs in chronic psychophysiological insomnia sufferers? Int J Psychophysiol 72(3):314–322. https://doi.org/10.1016/j.ijpsycho.2009.02.001
Turoman N, Tivadar RI, Retsa C, Murray MM, Matusz PJ (2021) Towards understanding how we pay attention in naturalistic visual search settings, NeuroImage. 244:118556. https://doi.org/10.1016/j.neuroimage.2021.118556
Verleger R (1988) Event-related potentials and cognition: A critique of the context updating hypothesis and an alternative interpretation of P3. Behav Brain Sci 11(3):343–356. https://doi.org/10.1017/S0140525X00058015
Vogel E, Luck SJ (2000) The visual N1 component as an index of a discrimination process. Psychophysiology 37(2):190–203. https://doi.org/10.1111/1469-8986.3720190
Wang E, Sun L, Sun M, Huang J, Tao Y, Zhao X, Wu Z, Ding Y, Newman DP, Bellgrove MA, Wang Y, Song Y (2016) Attentional selection and suppression in children with attention-deficit/hyperactivity disorder. Biol Psychiatry: Cogn Neurosci Neuroimaging 1(4):372–380. https://doi.org/10.1016/j.bpsc.2016.01.004
Wienke C, Bartsch MV, Vogelgesang L, Reichert C, Hinrichs H, Heinze HJ, Dürschmid S (2021) Mind-wandering is accompanied by both local sleep and enhanced processes of spatial attention allocation. Cereb cortex Commun 2(1):tgab001. https://doi.org/10.1093/texcom/tgab001
Wiggins E, Mottarella M, Good K, Eggleston S, Stevens C (2018) 24-h sleep deprivation impairs early attentional modulation of neural processing: An event-related brain potential study. Neurosci Lett 677:32–36. https://doi.org/10.1016/j.neulet.2018.04.022
Yamazaki EM, Antler CA, Lasek CR, Goel N (2021) Residual, differential neurobehavioral deficits linger after multiple recovery nights following chronic sleep restriction or acute total sleep deprivation. Sleep 44(4):zsaa224. https://doi.org/10.1093/sleep/zsaa224
Yang CM, Lo HS (2007) ERP evidence of enhanced excitatory and reduced inhibitory processes of auditory stimuli during sleep in patients with primary insomnia. Sleep 30(5):585–592. https://doi.org/10.1093/sleep/30.5.585
Yoo S, Hu P, Gujar N, Jolesz F, Walker M (2007) A deficit in the ability to form new human memories without sleep. Nat Neurosci 10(3):385–392. https://doi.org/10.1038/nn1851
Zerouali Y, Jemel B, Godbout R (2010) The effects of early and late night partial sleep deprivation on automatic and selective attention: An ERP study. Brain Res 1308:87–99. https://doi.org/10.1016/j.brainres.2009.09.090
Zhu Y, Feng Z, Xu J, Fu C, Sun J, Yang X, Shi D, Qin W (2016) Increased interhemispheric resting-state functional connectivity after sleep deprivation: a resting-state fMRI study. Brain Imaging and Behavior 10(3):911–919. https://doi.org/10.1007/s11682-015-9490-5
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Song, T., Xu, L., Peng, Z. et al. Total sleep deprivation impairs visual selective attention and triggers a compensatory effect: evidence from event-related potentials. Cogn Neurodyn 17, 621–631 (2023). https://doi.org/10.1007/s11571-022-09861-8
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DOI: https://doi.org/10.1007/s11571-022-09861-8