Skip to main content
SpringerLink
Log in

Exploring the temporal dynamics of sustained and transient spatial attention using steady-state visual evoked potentials

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

While the behavioral dynamics as well as the functional network of sustained and transient attention have extensively been studied, their underlying neural mechanisms have most often been investigated in separate experiments. In the present study, participants were instructed to perform an audio–visual spatial attention task. They were asked to attend to either the left or the right hemifield and to respond to deviant transient either auditory or visual stimuli. Steady-state visual evoked potentials (SSVEPs) elicited by two task irrelevant pattern reversing checkerboards flickering at 10 and 15 Hz in the left and the right hemifields, respectively, were used to continuously monitor the locus of spatial attention. The amplitude and phase of the SSVEPs were extracted for single trials and were separately analyzed. Sustained attention to one hemifield (spatial attention) as well as to the auditory modality (intermodal attention) increased the inter-trial phase locking of the SSVEP responses, whereas briefly presented visual and auditory stimuli decreased the single-trial SSVEP amplitude between 200 and 500 ms post-stimulus. This transient change of the single-trial amplitude was restricted to the SSVEPs elicited by the reversing checkerboard in the spatially attended hemifield and thus might reflect a transient re-orienting of attention towards the brief stimuli. Thus, the present results demonstrate independent, but interacting neural mechanisms of sustained and transient attentional orienting.

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
Fig. 5

Similar content being viewed by others

Notes

  1. The factor SSVEP Stimulus Hemifield (left vs. right) was skipped, as no significant effects were found. The data were thus collapsed across hemifields to increase signal-to-noise (SNR) of the SSVEPs, especially of the single-trial amplitude responses. See “Results” and “Discussion”.

References

  • Andersen SK, Müller MM (2010) Behavioral performance follows the time course of neural facilitation and suppression during cued shifts of feature-selective attention. Proc Natl Acad Sci 107:13878–13882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Attar CH, Andersen SK, Müller MM (2010) Time course of affective bias in visual attention: convergent evidence from steady-state visual evoked potentials and behavioral data. Neuroimage 53:1326–1333.

    Article  Google Scholar 

  • Bruns P, Röder B (2010) Tactile capture of auditory localization: an event-related potential study. Eur J Neurosci 31:1844–1857

    Article  PubMed  Google Scholar 

  • Busse L, Katzner S, Treue S (2008) Temporal dynamics of neuronal modulation during exogenous and endogenous shifts of visual attention in macaque area MT. Proc Natl Acad Sci USA 105:16380–16385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chica AB, Lupianez J (2009) Effects of endogenous and exogenous attention on visual processing: an inhibition of return study. Brain Res 1278:75–85

    Article  CAS  PubMed  Google Scholar 

  • Chica AB, Bartolomeo P, Lupianez J (2013) Two cognitive and neural systems for endogenous and exogenous spatial attention. Behav Brain Res 237:107–123

    Article  PubMed  Google Scholar 

  • Cohen MX, Gulbinaite R (2016) Rhythmic entrainment source separation: Optimizing analyses of neural responses to rhythmic sensory stimulation. Neuroimage 147:43–56

    Article  PubMed  Google Scholar 

  • Corbetta M, Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3:201–215

    Article  CAS  PubMed  Google Scholar 

  • David O, Harrison L, Friston KJ (2005) Modelling event-related responses in the brain. Neuroimage 25:756–770

    Article  PubMed  Google Scholar 

  • de Cheveigné A, Arzounian D (2015) Scanning for oscillations. J Neural Eng 12:066020

    Article  PubMed  Google Scholar 

  • de Cheveigne A, Simon JZ (2008) Denoising based on spatial filtering. J Neurosci Methods 171:331–339

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ding N, Simon JZ (2009) Neural representations of complex temporal modulations in the human auditory cortex. J Neurophysiol 102:2731–2743

    Article  PubMed  PubMed Central  Google Scholar 

  • Ding J, Sperling G, Srinivasan R (2006) Attentional modulation of SSVEP power depends on the network tagged by the flicker frequency. Cereb Cortex 16:1016–1029

    Article  PubMed  Google Scholar 

  • Dmochowski JP, Greaves AS, Norcia AM (2015) Maximally reliable spatial filtering of steady state visual evoked potentials. Neuroimage 109:63–72

    Article  PubMed  Google Scholar 

  • Doallo S, Lorenzo-Lopez L, Vizoso C, Rodriguez Holguin S, Amenedo E, Bara S, Cadaveira F (2004) The time course of the effects of central and peripheral cues on visual processing: an event-related potentials study. Clin Neurophysiol 115:199–210

    Article  CAS  PubMed  Google Scholar 

  • Doallo S, Lorenzo-Lopez L, Vizoso C, Holguin SR, Amenedo E, Bara S, Cadaveira F (2005) Modulations of the visual N1 component of event-related potentials by central and peripheral cueing. Clin Neurophysiol 116:807–820

    Article  CAS  PubMed  Google Scholar 

  • Driver J, Noesselt T (2008) Multisensory interplay reveals crossmodal influences on ‘sensory-specific’ brain regions, neural responses, and judgments. Neuron 57:11–23

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eimer M, Driver J (2001) Crossmodal links in endogenous and exogenous spatial attention: evidence from event-related brain potential studies. Neurosci Biobehav Rev 25:497–511.

    Article  CAS  PubMed  Google Scholar 

  • Eimer M, Schröger E (1998) ERP effects of intermodal attention and cross-modal links in spatial attention. Psychophysiology 35:313–327

    Article  CAS  PubMed  Google Scholar 

  • Engel A, Fries P, Singer W (2001) Dynamic predictions: oscillations and synchrony in top-down processing. Nat Rev Neurosci 2:704–716

    Article  CAS  PubMed  Google Scholar 

  • Fawcett IP, Barnes GR, Hillebrand A, Singh KD (2004) The temporal frequency tuning of human visual cortex investigated using synthetic aperture magnetometry. Neuroimage 21:1542–1553.

    Article  PubMed  Google Scholar 

  • Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1:1–47

    Article  CAS  PubMed  Google Scholar 

  • Feng W, Störmer VS, Martinez A, McDonald JJ, Hillyard SA (2014) Sounds activate visual cortex and improve visual discrimination. J Neurosci 34(29):9817–9824

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fuchs S, Andersen SK, Gruber T, Müller MM (2008) Attentional bias of competitive interactions in neuronal networks of early visual processing in the human brain. Neuroimage 41:1086–1101.

    Article  PubMed  Google Scholar 

  • Gander PE, Bosnyak DJ, Roberts LE (2010) Acoustic experience but not attention modifies neural population phase expressed in human primary auditory cortex. Hear Res 269(1–2):81–94

    Article  CAS  PubMed  Google Scholar 

  • Genovese CR, Lazar NA, Nichols T (2002) Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 15:870–878

    Article  PubMed  Google Scholar 

  • Hillyard SA, Hink RF, Schwent VL, Picton TW (1973) Electrical signs of selective attention in the human brain. Science 182(4108):177–180

    Article  CAS  PubMed  Google Scholar 

  • Hillyard SA, Simpson GV, Woods DL, VanVoorhis S, Münte TF (1984) Event-related brain potentials and selective attention to different modalities. In: Reinoso-Suarez F, Ajmone-Marsan C (eds) Cortical integration. Raven Press, New York, pp 395–414

    Google Scholar 

  • Hopfinger JB, West VM (2006) Interactions between endogenous and exogenous attention on cortical visual processing. Neuroimage 31:774–789

    Article  PubMed  Google Scholar 

  • Hötting K, Rösler F, Röder B (2003) Crossmodal and intermodal attention modulate event-related brain potentials to tactile and auditory stimuli. Exp Brain Res 148:26–37

    Article  PubMed  Google Scholar 

  • Jacoby O, Hall SE, Mattingley JB (2012) A crossmodal crossover: opposite effects of visual and auditory perceptual load on steady-state evoked potentials to irrelevant visual stimuli. Neuroimage 61(4): 1050–1058.

    Article  PubMed  Google Scholar 

  • Jervis BW, Nichols MJ, Johnson TE, Allen E, Hudson NR (1983) A fundamental investigation of the composition of auditory evoked potentials. IEEE Trans Biomed Eng 30:43–50

    Article  CAS  PubMed  Google Scholar 

  • Jonides J (1981) Voluntary versus automatic control over the mind’s eye’s movement. Atten Perform IX(9):187–203

    Google Scholar 

  • Kashiwase Y, Matsumiya K, Kuriki I, Shioiri S (2012) Time courses of attentional modulation in neural amplification and synchronization measured with steady-state visual-evoked potentials. J Cogn Neurosci 24(8):1779–1793

    Article  PubMed  Google Scholar 

  • Kastner S, Ungerleider LG (2000) Mechanisms of visual attention in the human cortex. Annu Rev Neurosci 23:315–341

    Article  CAS  PubMed  Google Scholar 

  • Keitel C, Schröger E, Saupe K, Müller MM (2011) Sustained selective intermodal attention modulates processing of language-like stimuli. Exp Brain Res 213(2–3):321–327

    Article  PubMed  Google Scholar 

  • Keitel C, Maess B, Schröger E, Müller MM (2013) Early visual and auditory processing rely on modality-specific attentional resources. Neuroimage 70(C), 240–249.

    Article  PubMed  Google Scholar 

  • Keitel C, Quigley C, Ruhnau P (2014) Stimulus-driven brain oscillations in the alpha range: entrainment of intrinsic rhythms or frequency-following response? J Neurosci 34(31):10137–10140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim YJ, Grabowecky M, Paller KA, Muthu K, Suzuki S (2007) Attention induces synchronization-based response gain in steady-state visual evoked potentials. Nat Neurosci 10:117–125

    Article  CAS  PubMed  Google Scholar 

  • Klein RM (2000) Inhibition of return. Trends Cogn Sci 4:138–147

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Klimesch W, Sauseng P, Hanslmayr S (2007) EEG alpha oscillations: the inhibition-timing hypothesis. Brain Res Rev 53:63–88

    Article  PubMed  Google Scholar 

  • Lakatos P, O’Connell MN, Barczak A, Mills A, Javitt DC, Schroeder CE (2009) The leading sense: supramodal control of neurophysiological context by attention. Neuron 64:419–430

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Landau AN, Esterman M, Robertson LC, Bentin S, Prinzmetal W (2007) Different effects of voluntary and involuntary attention on EEG activity in the gamma band. J Neurosci 27:11986–11990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lopes da Silva FH (1998) Event-related potentials: methodology and quantification. In: Niedermeyer E, Lopes da Silva FH (eds) Electroencephalography: basic principles, clinical applications and related fields, 4th edn. Williams and Wilkins, Baltimore, pp 947–957

  • Luo H, Tian X, Song K, Zhou K, Poeppel D (2013) Neural response phase tracks how listeners learn new acoustic representations. Curr Biol 23:968–974

    Article  CAS  PubMed  Google Scholar 

  • Mäkinen V, Tiitinen H, May P (2005) Auditory event-related responses are generated independently of ongoing brain activity. Neuroimage 24:961–968

    Article  PubMed  Google Scholar 

  • Mathewson KE, Lleras A, Beck DM, Fabiani M, Ro T, Gratton G (2011) Pulsed out of awareness: EEG alpha oscillations represent a pulsed-inhibition of ongoing cortical processing. Front Psychol 2:99

    Article  PubMed  PubMed Central  Google Scholar 

  • McDonald JJ, Teder-Sälejärvi WA, Di Russo F, Hillyard SA (2003) Neural substrates of perceptual enhancement by cross-modal spatial attention. J Cogn Neurosci 15:10–19

    Article  PubMed  Google Scholar 

  • McDonald JJ, Teder-Sälejärvi WA, Di Russo F, Hillyard SA (2005) Neural basis of auditory-induced shifts in visual time-order perception. Nat Neurosci 8:1197–1202

    Article  CAS  PubMed  Google Scholar 

  • McDonald JJ, Störmer VS, Martinez A, Feng W, Hillyard SA (2013) Salient sounds activate human visual cortex automatically. J Neurosci 33:9194–9201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moratti S, Clementz B, Gao Y, Ortiz T, Keil A (2007) Neural mechanisms of evoked oscillations: Stability and interaction with transient events. Hum Brain Mapp 28:1318–1333

    Article  PubMed  Google Scholar 

  • Morgan ST, Hansen JC, Hillyard SA (1996) Selective attention to stimulus location modulates the steady-state visual evoked potential. Proc Natl Acad Sci USA 93:4770–4774

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Müller HJ, Rabbitt PM (1989) Reflexive and voluntary orienting of visual attention: time course of activation and resistance to interruption. J Exp Psychol Hum Percept Perform 15(2):315–330

    Article  PubMed  Google Scholar 

  • Müller MM, Picton TW, Valdes-Sosa P, Riera J, Teder-Sälejärvi WA, Hillyard SA (1998a) Effects of spatial selective attention on the steady-state visual evoked potential in the 20–28 Hz range. Brain Res Cogn Brain Res 6:249–261

    Article  PubMed  Google Scholar 

  • Müller MM, Teder-Sälejärvi W, Hillyard SA (1998b) The time course of cortical facilitation during cued shifts of spatial attention. Nat Neurosci 1:631–634

    Article  PubMed  Google Scholar 

  • Müller MM, Andersen SK, Keil A (2008) Time course of competition for visual processing resources between emotional pictures and foreground task. Cereb Cortex 18(8):1892–1899

    Article  PubMed  Google Scholar 

  • Nakayama K, Mackeben M (1989) Sustained and transient components of focal visual attention. Vis Res 29(11):1631–1647

    Article  CAS  PubMed  Google Scholar 

  • Naue N, Rach S, Struber D, Huster RJ, Zaehle T, Korner U, Herrmann CS (2011) Auditory event-related response in visual cortex modulates subsequent visual responses in humans. J Neurosci 31:7729–7736

    Article  CAS  PubMed  Google Scholar 

  • Nikulin VV, Nolte G, Curio G (2011) A novel method for reliable and fast extractionof neuronal EEG/MEG oscillations on the basis of spatio-spectral decomposition. Neuroimage 55:1528–1535

    Article  PubMed  Google Scholar 

  • Norcia AM, Appelbaum LG, Ales JM, Cottereau BR, Rossion B (2015) The steady-state visual evoked potential in vision research: a review. J Vis 15(6): 4, 1–46.

    Google Scholar 

  • Oostenveld R, Fries P, Maris E, Schoffelen JM (2011) FieldTrip: Open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput Intell Neurosci 2011:156869

    Article  PubMed  Google Scholar 

  • Painter DR, Dux PE, Travis SL, Mattingley JB (2014) Neural responses to target features outside a search array are enhanced during conjunction but not unique-feature search. J Neurosci 34(9):3390–3401

    Article  CAS  PubMed  Google Scholar 

  • Parks NA, Hilimire MR, Corballis PM (2011) Steady-state signatures of visual perceptual load, multimodal distractor filtering, and neural competition. J Cogn Neurosci 23(5):1113–1124

    Article  PubMed  Google Scholar 

  • Peelen MV, Heslenfeld DJ, Theeuwes J (2004) Endogenous and exogenous attention shifts are mediated by the same large-scale neural network. Neuroimage 22:822–830

    Article  PubMed  Google Scholar 

  • Porcu E, Keitel C, Müller MM (2014) Visual, auditory and tactile stimuli compete for early sensory processing capacities within but not between senses. Neuroimage 97:224–235

    Article  PubMed  Google Scholar 

  • Posner MI, Cohen Y (1984) Components of visual orienting. Atten Perform X Control Lang Process 32:531–556.

    Google Scholar 

  • Regan D (1977) Steady-state evoked potentials. J Opt Soc Am 67:1475–1489

    Article  CAS  PubMed  Google Scholar 

  • Regan D (1989) Human brain electrophysiology: evoked potentials and evoked magnetic fields in science and medicine. Elsevier, New York

  • Rosen AC, Rao SM, Caffarra P, Scaglioni A, Bobholz JA, Woodley SJ, Hammeke TA, Cunningham JM, Prieto TE, Binder JR (1999) Neural basis of endogenous and exogenous spatial orienting. A functional MRI study. J Cogn Neurosci 11:135–152

    Article  CAS  PubMed  Google Scholar 

  • Salinas E, Sejnowski TJ (2001) Correlated neuronal activity and the flow of neural information. Nat Rev Neurosci 2:539–550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saupe K, Schröger E, Andersen SK, Müller MM (2009) Neural mechanisms of intermodal sustained selective attention with concurrently presented auditory and visual stimuli. Front Hum Neurosci 3: 58

    Article  PubMed  PubMed Central  Google Scholar 

  • Sauseng P, Klimesch W (2008) What does phase information of oscillatory brain activity tell us about cognitive processes? Neurosci Biobehav Rev 32(5):1001–1013

    Article  PubMed  Google Scholar 

  • Sauseng P, Klimesch W, Gruber WR, Hanslmayr S, Freunberger R, Doppelmayr M (2007) Are event-related potential components generated by phase resetting of brain oscillations? A critical discussion. Neuroscience 146:1435–1444

    Article  CAS  PubMed  Google Scholar 

  • Schroeder CE, Lakatos P, Kajikawa Y, Partan S, Puce A (2008) Neuronal oscillations and visual amplification of speech. Trends Cogn Sci Regul 12:106–113

    Article  Google Scholar 

  • Schyns PG, Thut G, Gross J (2011) Cracking the code of oscillatory activity. Plos Biol 9:e1001064.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Senkowski D, Schneider T, Foxe J, Engel A (2008) Crossmodal binding through neural coherence: implications for multisensory processing. Trends Neurosci 31:401–409

    Article  CAS  PubMed  Google Scholar 

  • Sieben K, Roder B, Hanganu-Opatz IL (2013) Oscillatory entrainment of primary somatosensory cortex encodes visual control of tactile processing. J Neurosci 33:5736–5749

    Article  CAS  PubMed  Google Scholar 

  • Störmer VS, Green JJ, McDonald JJ (2009) Tracking the voluntary control of auditory spatial attention with event-related brain potentials. Psychophysiology 46:357–366

    Article  PubMed  Google Scholar 

  • Störmer VS, Feng W, Martinez A, McDonald JJ, Hillyard SA (2016) Salient, irrelevant sounds reflexively induce alpha rhythm desynchronization in parallel with slow potential shifts in visual cortex. J Cogn Neurosci 28(3):433–445

    Article  PubMed  Google Scholar 

  • Talsma D, Doty T, Strowd R, Woldorff M (2006) Attentional capacity for processing concurrent stimuli is larger across sensory modalities than within a modality. Psychophysiology 43(6):541–549

    Article  PubMed  Google Scholar 

  • Thorne JD, De Vos M, Viola FC, Debener S (2011) Cross-modal phase reset predicts auditory task performance in humans. J Neurosci 31:3853–3861

    Article  CAS  PubMed  Google Scholar 

  • Thorpe SG, Nunez PL, Srinivasan R (2007) Identification of wave-like spatial structure in the SSVEP: comparison of simultaneous EEG and MEG. Stat Med 26(21):3911–3926

    Article  PubMed  Google Scholar 

  • Vialatte F-B, Maurice M, Dauwels J, Cichocki A (2010) Steady-state visually evoked potentials: Focus on essential paradigms and future perspectives. Prog Neurobiol 90(4):418–438

    Article  PubMed  Google Scholar 

  • Wang Y, Ding N, Ahmar N, Xiang J, Poeppel D, Simon JZ (2012) Sensitivity to temporal modulation rate and spectral bandwidth in the human auditory system: MEG evidence. J Neurophysiol 107:2033–2041

    Article  PubMed  Google Scholar 

  • Zhang D, Hong B, Gao X, Gao S, Röder B (2011) Exploring steady-state visual evoked potentials as an index for intermodal and crossmodal spatial attention. Psychophysiology 48:665–675

    Article  PubMed  Google Scholar 

  • Zhu D, Bieger J, Molina GG, Aarts RM (2010) A survey of stimulation methods used in SSVEP-based BCIs. Comput Intell Neurosci 1:702357

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Biological Psychology and Neuropsychology, University of Hamburg, Von-Melle-Park 11, 20146, Hamburg, Germany

    Dan Zhang & Brigitte Röder

  2. Department of Biomedical Engineering, School of Medicine, Tsinghua University, Beijing, 100084, China

    Dan Zhang, Bo Hong & Shangkai Gao

  3. Department of Psychology, School of Social Sciences, Tsinghua University, Beijing, 100084, China

    Dan Zhang

Authors
  1. Dan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bo Hong
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shangkai Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Brigitte Röder
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dan Zhang.

Ethics declarations

Support Funding

The Sino-German Research Training Group CINACS, German Research Foundation (DFG GK 1247/1) and DFG TRR 169/1 Crossmodal Learning, National Key Research and Development Plan of China under Grant No. 2016YFB1001200 and Tsinghua University Initiative Scientific Research Program (2014z21043).

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 3512 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, D., Hong, B., Gao, S. et al. Exploring the temporal dynamics of sustained and transient spatial attention using steady-state visual evoked potentials. Exp Brain Res 235, 1575–1591 (2017). https://doi.org/10.1007/s00221-017-4907-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-017-4907-6

Keywords

Search

Navigation