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Brain Areas Responsible for Vigilance: An EEG Source Imaging Study

Abstract

Vigilance, sometimes referred to as sustained attention, is an important type of human attention as it is closely associated with cognitive activities required in various daily-life situations. Although many researchers have investigated which brain areas control the maintenance of vigilance, findings have been inconsistent. We hypothesized that this inconsistency might be due to the use of different experimental paradigms in the various studies. We found that most of the previous studies used paradigms that included specific cognitive tasks requiring a high cognitive load, which could complicate identification of brain areas associated only with vigilance. To minimize the influence of cognitive processes other than vigilance on the analysis results, we adopted the d2-test of attention, which is a well-known neuropsychological test of attention that does not require high cognitive load, and searched for brain areas at which EEG source activities were temporally correlated with fluctuation of vigilance over a prolonged period of time. EEG experiments conducted with 31 young adults showed that left prefrontal cortex activity was significantly correlated with vigilance variation in the delta, beta1, beta2, and gamma frequency bands, but not the theta and alpha frequency bands. Our study results suggest that the left prefrontal cortex plays a key role in vigilance modulation, and can therefore be used to monitor individual vigilance changes over time or serve as a potential target of noninvasive brain stimulation.

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Notes

  1. Trial-to-trial reaction time variability (RTV) was also evaluated for each of 27 segments because increased RTV might be potentially associated with decreased attention. RTV of each segment was defined as the standard deviation of response speed within the segment. However, no significant correlation was found between temporal changes in RTV and CP. The temporal variability of RTV was consistent over the entire experiment (mean of RTV over 27 time segments: 89.13 ms, standard deviation of RTV over 27 segments: 6.38 ms).

References

  • Babiloni C et al (2006) Frontal white matter volume and delta EEG sources negatively correlate in awake subjects with mild cognitive impairment and Alzheimer’s disease. Clin Neurophysiol 117:1113–1129

    Article  PubMed  Google Scholar 

  • Bates ME, Lemay EP (2004) The d2 test of attention: construct validity and extensions in scoring techniques. J Int Neuropsychol Soc 10:392–400

    Article  PubMed  Google Scholar 

  • Bekhtereva V, Sander C, Forschack N, Olbrich S, Hegerl U, Müller MM (2014) Effects of EEG-vigilance regulation patterns on early perceptual processes in human visual cortex. Clin Neurophysiol 125:98–107. doi:10.1016/j.clinph.2013.06.019

    Article  PubMed  Google Scholar 

  • Bogler C, Mehnert J, Steinbrink J, Haynes J-D (2014) Decoding vigilance with NIRS

  • Brickenkamp R, Zillmer E (1998) The d2 test of attention (1st US ed.). Hogrefe & Huber Publishers, Cambridge

    Google Scholar 

  • Caggiano DM, Parasuraman R (2004) The role of memory representation in the vigilance decrement. Psychon Bull Rev 11:932–937

    Article  PubMed  PubMed Central  Google Scholar 

  • Corbetta M, Miezin FM, Dobmeyer S, Shulman GL, Petersen SE (1991) Selective and divided attention during visual discriminations of shape, color, and speed: functional anatomy by positron emission tomography. J Neurosci 11:2383–2402

    CAS  PubMed  Google Scholar 

  • Corbetta M, Kincade JM, Ollinger JM, McAvoy MP, Shulman GL (2000) Voluntary orienting is dissociated from target detection in human posterior parietal cortex. Nature Neurosci 3:292–297

    CAS  Article  PubMed  Google Scholar 

  • Corbetta M, Kincade J, Shulman G (2002) Neural systems for visual orienting and their relationships to spatial working memory Cognitive. J Neurosci 14:508–523

    Google Scholar 

  • Corbetta M, Patel G, Shulman GL (2008) The reorienting system of the human brain: from environment to theory of mind. Neuron 58:306–324

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Corkum PV, Siegel LS (1993) Is the continuous performance task a valuable research tool for use with children with Attention-Deficit-Hyperactivity Disorder? J Child Psychol Psychiatry 34:1217–1239

    CAS  Article  PubMed  Google Scholar 

  • Coull JT, Nobre AC (1998) Where and when to pay attention: the neural systems for directing attention to spatial locations and to time intervals as revealed by both PET and fMRI The. J Neurosci 18:7426–7435

    CAS  PubMed  Google Scholar 

  • Coull J, Frith C, Frackowiak RSJ, Grasby P (1996) A fronto-parietal network for rapid visual information processing: a PET study of sustained attention and working memory. Neuropsychologia 34:1085–1095

    CAS  Article  PubMed  Google Scholar 

  • de Jong T, van Joolingen WR (1998) Scientific discovery learning with computer simulations of conceptual domains. Rev Edu Res 68:179–201

    Google Scholar 

  • DeGangi G, Porges S (1990) Neuroscience foundations of human performance Rockville, American Occupational Therapy Association Inc., Bethesda

    Google Scholar 

  • Desimone R, Duncan J (1995) Neural mechanisms of selective visual attention. Annu Rev Neurosci 18:193–222

    CAS  Article  PubMed  Google Scholar 

  • Dockree PM, Kelly SP, Foxe JJ, Reilly RB, Robertson IH (2007) Optimal sustained attention is linked to the spectral content of background EEG activity: greater ongoing tonic alpha (∼10 Hz) power supports successful phasic goal activation. Eur J Neurosci 25:900–907

    Article  PubMed  Google Scholar 

  • Drechsler R, Straub M, Doehnert M, Heinrich H, Steinhausen HC, Brandeis D (2007) Controlled evaluation of a neurofeedback training of slow cortical potentials in children with attention deficit/hyperactivity disorder (ADHD). Behav Brain Funct 3:35

    Article  PubMed  PubMed Central  Google Scholar 

  • Dussault C, Jouanin J-C, Philippe M, Guezennec C-Y (2005) EEG and ECG changes during simulator operation reflect mental workload and vigilance. Aviat Space Environ Med 76:344–351

    PubMed  Google Scholar 

  • Egeth HE, Yantis S (1997) Visual attention: control, representation, and time course. Annu Rev Psychol 48:269–297

    CAS  Article  PubMed  Google Scholar 

  • Freeman FG, Mikulka PJ, Scerbo MW, Scott L (2004) An evaluation of an adaptive automation system using a cognitive vigilance task. Biol Psychol 67:283–297

    Article  PubMed  Google Scholar 

  • Fuchs M, Kastner J, Wagner M, Hawes S, Ebersole JS (2002) A standardized boundary element method volume conductor model. Clin Neurophysiol 113:702–712

    Article  PubMed  Google Scholar 

  • Gevins A, Smith ME, McEvoy L, Yu D (1997) High-resolution EEG mapping of cortical activation related to working memory: effects of task difficulty, type of processing, and practice. Cerebral cortex 7:374–385

    CAS  Article  PubMed  Google Scholar 

  • Harmony T et al. (1996) EEG delta activity: an indicator of attention to internal processing during performance of mental tasks. Int J Psychophysiol 24:161–171

    CAS  Article  PubMed  Google Scholar 

  • He BJ, Snyder AZ, Vincent JL, Epstein A, Shulman GL, Corbetta M (2007) Breakdown of functional connectivity in frontoparietal networks underlies behavioral deficits in spatial neglect. Neuron 53:905–918

    CAS  Article  PubMed  Google Scholar 

  • Hinds O, Thompson TW, Ghosh S, Yoo JJ, Whitfield-Gabrieli S, Triantafyllou C, Gabrieli JDE (2013) Roles of default-mode network and supplementary motor area in human vigilance performance: evidence from real-time fMRI. J Neurophysiol 109:1250–1258. doi:10.1152/jn.00533.2011

    CAS  Article  PubMed  Google Scholar 

  • Hopfinger J, Buonocore M, Mangun G (2000) The neural mechanisms of top-down attentional control. Nature Neurosci 3:284–291

    CAS  Article  PubMed  Google Scholar 

  • Ishii R et al (1999) Medial prefrontal cortex generates frontal midline theta rhythm. Neuroreport 10:675–679

    CAS  Article  PubMed  Google Scholar 

  • Kastner S, Pinsk MA, De Weerd P, Desimone R, Ungerleider LG (1999) Increased activity in human visual cortex during directed attention in the absence of visual stimulation. Neuron 22:751–761

    CAS  Article  PubMed  Google Scholar 

  • Kelly SP, Lalor EC, Reilly RB, Foxe JJ (2006) Increases in alpha oscillatory power reflect an active retinotopic mechanism for distracter suppression during sustained visuospatial attention. J Neurophysiol 95:3844–3851

    Article  PubMed  Google Scholar 

  • Kincade JM, Abrams RA, Astafiev SV, Shulman GL, Corbetta M (2005) An event-related functional magnetic resonance imaging study of voluntary and stimulus-driven orienting of attention. J Neurosci 25:4593–4604

    CAS  Article  PubMed  Google Scholar 

  • Klimesch W (1999) EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis. Brain Res Rev 29:169–195

    CAS  Article  PubMed  Google Scholar 

  • Klimesch W (2012) Alpha-band oscillations, attention, and controlled access to stored information. Trends Cognit Sci 16:606–617

    Article  Google Scholar 

  • Lawrence N, Ross T, Hoffmann R, Garavan H, Stein E (2003) Multiple neuronal networks mediate sustained attention Cognitive. J Neurosci 15:1028–1038

    Google Scholar 

  • Mackworth JF (1964) Performance decrement in vigilance, threshold, and high-speed perceptual motor tasks. Can J Psychol/Rev canadienne de psychologie 18:209

    CAS  Article  Google Scholar 

  • Oken BS, Salinsky MC, Elsas SM (2006) Vigilance, alertness, or sustained attention: physiological basis and measurement. Clin Neurophysiol 117:1885–1901. doi:10.1016/j.clinph.2006.01.017

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Olbrich S, Mulert C, Karch S, Trenner M, Leicht G, Pogarell O, Hegerl U (2009) EEG-vigilance and BOLD effect during simultaneous EEG/fMRI measurement. Neuroimage 45:319–332

    Article  PubMed  Google Scholar 

  • Parasuraman R (1979) Memory load and event rate control sensitivity decrements in sustained attention. Science 205:924–927

    CAS  Article  PubMed  Google Scholar 

  • Park JY, Jhung K, Lee J, An SK (2013) Theta-gamma coupling during a working memory task as compared to a simple vigilance task. Neurosci Lett 532:39–43. doi:10.1016/j.neulet.2012.10.061

    CAS  Article  PubMed  Google Scholar 

  • Pascual-Marqui R (2002) Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. Methods Find Exp Clin Pharmacol 24:5–12

    PubMed  Google Scholar 

  • Paus T, Zatorre RJ, Hofle N, Caramanos Z, Gotman J, Petrides M, Evans AC (1997) Time-related changes in neural systems underlying attention and arousal during the performance of an auditory vigilance task. J Cogn Neurosci 9:392–408

    CAS  Article  PubMed  Google Scholar 

  • Rueckert L, Baboorian D, Stavropoulos K, Yasutake C (1999) Individual differences in callosal efficiency: correlation with attention. Brain Cogn 41:390–410

    CAS  Article  PubMed  Google Scholar 

  • Sarter M, Givens B, Bruno JP (2001) The cognitive neuroscience of sustained attention: where top-down meets bottom-up. Brain Res Rev 35:146–160

    CAS  Article  PubMed  Google Scholar 

  • Sauseng P, Hoppe J, Klimesch W, Gerloff C, Hummel F (2007) Dissociation of sustained attention from central executive functions: local activity and interregional connectivity in the theta range. Eur J Neurosci 25:587–593

    CAS  Article  PubMed  Google Scholar 

  • Smit AS, Eling PA, Coenen AM (2004) Mental effort affects vigilance enduringly: after-effects in EEG and behavior. Int J Psychophysiol 53:239–243

    Article  PubMed  Google Scholar 

  • Smit AS, Eling PA, Hopman MT, Coenen AM (2005) Mental and physical effort affect vigilance differently. Int J Psychophysiol 57:211–217

    Article  PubMed  Google Scholar 

  • Song J et al (2015) EEG source localization: sensor density and head surface coverage. J Neurosci Methods 256:9–21. doi:10.1016/j.jneumeth.2015.08.015

    Article  PubMed  Google Scholar 

  • Treisman AM, Gelade G (1980) A feature-integration theory of attention. Cognit Psychol 12:97–136

    CAS  Article  PubMed  Google Scholar 

  • Wright RD, Ward LM (2008) Orienting of attention. Oxford University Press, Oxford

    Google Scholar 

Download references

Acknowledgements

This research was supported by the National Research Foundation of Korea(NRF) grants funded by Korea government (MSIP) (NRF-2015M3C7A1031969 and 2015R1A2A1A15054662).

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Correspondence to Chang-Hwan Im.

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Kim, JH., Kim, DW. & Im, CH. Brain Areas Responsible for Vigilance: An EEG Source Imaging Study. Brain Topogr 30, 343–351 (2017). https://doi.org/10.1007/s10548-016-0540-0

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  • DOI: https://doi.org/10.1007/s10548-016-0540-0

Keywords

  • Vigilance
  • Sustained attention
  • Electroencephalography
  • Source imaging
  • D2 test of attention