Abstract
Visual selective attention can be achieved into bottom-up and top-down attention. Different selective attention tasks involve different attention control ways. The pop-out task requires more bottom-up attention, whereas the search task involves more top-down attention. P300, which is the positive potential generated by the brain in the latency of 300 ~ 600 ms after stimulus, reflects the processing of attention. There is no consensus on the P300 source. The aim of present study is to study the source of P300 elicited by different visual selective attention. We collected thirteen participants’ P300 elicited by pop-out and search tasks with event-related potentials (ERP). We collected twenty-six participants’ activation brain regions in pop-out and search tasks with functional magnetic resonance imaging (fMRI). And we analyzed the sources of P300 using the ERP and fMRI integration with high temporal resolution and high spatial resolution. ERP results indicated that the pop-out task induced larger P300 than the search task. P300 induced by the two tasks distributed at frontal and parietal lobes, with P300 induced by the pop-out task mainly at the parietal lobe and that induced by the search task mainly at the frontal lobe. Further ERP and fMRI integration analysis showed that neural difference sources of P300 were the right precentral gyrus, left superior frontal gyrus (medial orbital), left middle temporal gyrus, left rolandic operculum, right postcentral gyrus, and left angular gyrus. Our study suggests that the frontal and parietal lobes contribute to the P300 component of visual selective attention.
Similar content being viewed by others
Data Availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Allen JJ (2002) The role of psychophysiology in clinical assessment: ERPs in the evaluation of memory. Psychophysiology 39(3):261–280. https://doi.org/10.1017/s0048577201393034
Bachiller A, Romero S, Molina V, Alonso JF, Mananas MA, Poza J, Hornero R (2015) Auditory P3a and P3b neural generators in schizophrenia: an adaptive sLORETA P300 localization approach. Schizophr Res 169(1–3):318–325. https://doi.org/10.1016/j.schres.2015.09.028
Bae KY, Kim DW, Im CH, Lee SH (2011) Source imaging of P300 auditory evoked potentials and clinical correlations in patients with posttraumatic stress disorder. Prog Neuropsychopharmacol Biol Psychiatry 35(8):1908–1917. https://doi.org/10.1016/j.pnpbp.2011.08.002
Barcelo F, Cooper PS (2018) An information theory account of late frontoparietal ERP positivities in cognitive control. Psychophysiology 55(3):1–19. https://doi.org/10.1111/psyp.12814
Bledowski C, Prvulovic D, Goebel R, Zanella FE, Linden DE (2004) Attentional systems in target and distractor processing: a combined ERP and fMRI study. Neuroimage 22(2):530–540. https://doi.org/10.1016/j.neuroimage.2003.12.034
Bledowski C, Cohen Kadosh K, Wibral M, Rahm B, Bittner RA, Hoechstetter K, Scherg M, Maurer K, Goebel R, Linden DE (2006) Mental chronometry of working memory retrieval: a combined functional magnetic resonance imaging and event-related potentials approach. J Neurosci 26(3):821–829. https://doi.org/10.1523/JNEUROSCI.3542-05.2006
Blundon EG, Rumak SP, Ward LM (2017) Sequential search asymmetry: behavioral and psychophysiological evidence from a dual oddball task. PLoS ONE 12(3):1–31. https://doi.org/10.1371/journal.pone.0173237
Bore JC, Yi C, Li P, Li F, Harmah DJ, Si Y, Guo D, Yao D, Wan F, Xu P (2019) Sparse EEG source localization using LAPPS: least absolute l-P (0<p<1) penalized solution. IEEE Trans Biomed Eng 66(7):1927–1939. https://doi.org/10.1109/tbme.2018.2881092
Botvinik-Nezer R, Salomon T, Schonberg T (2020) Enhanced bottom-up and reduced top-down fMRI activity is related to long-lasting nonreinforced behavioral change. Cereb Cortex 30(3):858–874. https://doi.org/10.1093/cercor/bhz132
Buschman TJ, Miller EK (2007) Top-down versus bottom-up control of attention in the prefrontal and posterior parietal cortices. Science 315(5820):1860–1862. https://doi.org/10.1126/science.1138071
Chen CC, Kuo JC, Wang WJ (2019) Distinguishing the visual working memory training and practice effects by the effective connectivity during n-back tasks: a DCM of ERP study. Front Behav Neurosci 13:1–12. https://doi.org/10.3389/fnbeh.2019.00084
Clark VP, Fannon S, Lai S, Benson R, Bauer L (2000) Responses to rare visual target and distractor stimuli using event-related fMRI. J Neurophysiol 83(5):3133–3139. https://doi.org/10.1152/jn.2000.83.5.3133
Constantinidis C, Steinmetz MA (2005) Posterior parietal cortex automatically encodes the location of salient stimuli. J Neurosci 25(1):233–238. https://doi.org/10.1523/Jneurosci.3379-04.2005
Corbetta M, Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3(3):201–215. https://doi.org/10.1038/nrn755
Dallmer-Zerbe I, Popp F, Lam AP, Philipsen A, Herrmann CS (2020) Transcranial alternating current stimulation (tACS) as a tool to modulate P300 amplitude in attention deficit hyperactivity disorder (ADHD): preliminary findings. Brain Topogr 33(2):191–207. https://doi.org/10.1007/s10548-020-00752-x
de la Salle S, Shah D, Choueiry J, Bowers H, McIntosh J, Carroll B, Ilivitsky V, Knott V (2021) N-methyl-D-aspartate receptor antagonism modulates P300 event-related potentials and associated activity in salience and central executive networks. Pharmacol Biochem Behav 211:1–12. https://doi.org/10.1016/j.pbb.2021.173287
Desimone R, Duncan J (1995) Neural mechanisms of selective visual attention. Annu Rev Neurosci 18:193–222. https://doi.org/10.1146/annurev.ne.18.030195.001205
Duncan J, Humphreys G (1992) Beyond the search surface: visual search and attentional engagement. J Exp Psychol Hum Percept Perform 18(2):578–588. https://doi.org/10.1037//0096-1523.18.2.578
Ehlers MR, Lopez Herrero C, Kastrup A, Hildebrandt H (2015) The P300 in middle cerebral artery strokes or hemorrhages: outcome predictions and source localization. Clin Neurophysiol 126(8):1532–1538. https://doi.org/10.1016/j.clinph.2014.10.151
Eimer M (2014) The neural basis of attentional control in visual search. Trends Cogn Sci 18(10):526–535. https://doi.org/10.1016/j.tics.2014.05.005
Failing M, Theeuwes J (2018) Selection history: how reward modulates selectivity of visual attention. Psychon Bull Rev 25(2):514–538. https://doi.org/10.3758/s13423-017-1380-y
Fan LX, Zhang L, Diao LT, Xu MS, Chen RY, Zhang XM (2021) Bottom-up perceptual salience and top-down retro-cues concurrently determine state in visual working memory. Quart J Exp Psychol 74(3):459–470. https://doi.org/10.1177/1747021820966264
Faro HKC, Machado DGD, Bortolotti H, do Nascimento PHD, Moioli RC, Elsangedy HM, Fontes EB (2020) Influence of judo experience on neuroelectric activity during a selective attention task. Front Psychol 10:1–17. https://doi.org/10.3389/fpsyg.2019.02838
Fonken YM, Kam JWY, Knight RT (2020) A differential role for human hippocampus in novelty and contextual processing: Implications for P300. Psychophysiology 57(7):1–13. https://doi.org/10.1111/psyp.13400
Fujii Y, Morita H, Takeda Y (2021) The similarity between target and nontarget affects different processing stages depending on stimulus feature dimensions: an ERP study. Jpn Psychol Res. https://doi.org/10.1111/jpr.12362
Gazzaley A, Nobre AC (2012) Top-down modulation: bridging selective attention and working memory. Trends Cogn Sci 16(2):129–135. https://doi.org/10.1016/j.tics.2011.11.014
Giesbrecht B, Woldorff MG, Song AW, Mangun GR (2003) Neural mechanisms of top-down control during spatial and feature attention. Neuroimage 19(3):496–512. https://doi.org/10.1016/s1053-8119(03)00162-9
Green JJ, Conder JA, McDonald JJ (2008) Lateralized frontal activity elicited by attention-directing visual and auditory cues. Psychophysiology 45(4):579–587. https://doi.org/10.1111/j.1469-8986.2008.00657.x
Gur RE, Turetsky BI, Loughead J, Snyder W, Kohler C, Elliott M, Pratiwadi R, Ragland JD, Bilker WB, Siegel SJ, Kanes SJ, Arnold SE, Gur RC (2007) Visual attention circuitry in schizophrenia investigated with oddball event-related functional magnetic resonance imaging. Am J Psychiatry 164(3):442–449. https://doi.org/10.1176/ajp.2007.164.3.442
Hiebel H, Ischebeck A, Brunner C, Nikolaev AR, Hofler M, Korner C (2018) Target probability modulates fixation-related potentials in visual search. Biol Psychol 138:199–210. https://doi.org/10.1016/j.biopsycho.2018.09.007
Hopfinger JB, Woldorff MG, Fletcher EM, Mangun GR (2001) Dissociating top-down attentional control from selective perception and action. Neuropsychologia 39(12):1277–1291. https://doi.org/10.1016/s0028-3932(01)00117-8
Horn H, Syed N, Lanfermann H, Maurer K, Dierks T (2003) Cerebral networks linked to the event-related potential P300. Eur Arch Psychiatry Clin Neurosci 253(3):154–159. https://doi.org/10.1007/s00406-003-0419-4
Horwitz B, Poeppel D (2002) How can EEG/MEG and fMRI/PET data be combined? Hum Brain Mapp 17(1):1–3. https://doi.org/10.1002/hbm.10057
Huster RJ, Debener S, Eichele T, Herrmann CS (2012) Methods for simultaneous EEG-fMRI: an introductory review. J Neurosci 32(18):6053–6060. https://doi.org/10.1523/JNEUROSCI.0447-12.2012
Josephs O, Henson RN (1999) Event-related functional magnetic resonance imaging: modelling, inference and optimization. Philos Trans R Soc Lond B Biol Sci 354(1387):1215–1228. https://doi.org/10.1098/rstb.1999.0475
Katsuki F, Constantinidis C (2014) Bottom-up and top-down attention: different processes and overlapping neural systems. Neuroscientist 20(5):509–521. https://doi.org/10.1177/1073858413514136
Kiehl KA, Liddle PF (2001) An event-related functional magnetic resonance imaging study of an auditory oddball task in schizophrenia. Schizophr Res 48(2–3):159–171. https://doi.org/10.1016/s0920-9964(00)00117-1
Kok A (2001) On the utility of P3 amplitude as a measure of processing capacity. Psychophysiology 38(3):557–577. https://doi.org/10.1017/s0048577201990559
Kong G, Fougnie D (2019) Visual search within working memory. J Exp Psychol Gen 148(10):1688–1700. https://doi.org/10.1037/xge0000555
Lamy D, Zoaris L (2009) Task-irrelevant stimulus salience affects visual search. Vis Res 49(11):1472–1480. https://doi.org/10.1016/j.visres.2009.03.007
Lavie N, Tsal Y (1994) Perceptual load as a major determinant of the locus of selection in visual-attention. Percept Psychophys 56(2):183–197. https://doi.org/10.3758/Bf03213897
Lee J, Shomstein S (2014) Reward-based transfer from bottom-up to top-down search tasks. Psychol Sci 25(2):466–475. https://doi.org/10.1177/0956797613509284
Lei X, Xu P, Luo C, Zhao J, Zhou D, Yao D (2011) fMRI functional networks for EEG source imaging. Hum Brain Mapp 32(7):1141–1160. https://doi.org/10.1002/hbm.21098
Lei X, Hu J, Yao D (2012) Incorporating FMRI functional networks in EEG source imaging: a Bayesian model comparison approach. Brain Topogr 25(1):27–38. https://doi.org/10.1007/s10548-011-0187-9
Li L, Gratton C, Yao D, Knight RT (2010) Role of frontal and parietal cortices in the control of bottom-up and top-down attention in humans. Brain Res 1344:173–184. https://doi.org/10.1016/j.brainres.2010.05.016
Li L, Gratton C, Fabiani M, Knight RT (2013) Age-related frontoparietal changes during the control of bottom-up and top-down attention: an ERP study. Neurobiol Aging 34(2):477–488. https://doi.org/10.1016/j.neurobiolaging.2012.02.025
Liang W-K, Wang MS (2009) Source reconstruction of brain electromagnetic fields—source iteration of minimum norm (SIMN). Neuroimage 47(4):1301–1311. https://doi.org/10.1016/j.neuroimage.2009.03.079
Luck SJ, Hillyard SA (1990) Electrophysiological evidence for parallel and serial processing during visual search. Percept Psychophys 48(6):603–617. https://doi.org/10.3758/bf03211606
Luck SJ, Hillyard SA (1994) Electrophysiological correlates of feature analysis during visual search. Psychophysiology 31(3):291–308. https://doi.org/10.1111/j.1469-8986.1994.tb02218.x
Luck SJ, Woodman GF, Vogel EK (2000) Event-related potential studies of attention. Trends Cogn Sci 4(11):432–440. https://doi.org/10.1016/s1364-6613(00)01545-x
Moores KA, Clark CR, Hadfield JL, Brown GC, Taylor DJ, Fitzgibbon SP, Lewis AC, Weber DL, Greenblatt R (2003) Investigating the generators of the scalp recorded visuo-verbal P300 using cortically constrained source localization. Hum Brain Mapp 18(1):53–77. https://doi.org/10.1002/hbm.10073
Mudabbir MAM, Mundlamuri RC, Mariyappa N, Kumar RA, Velmurugan J, Bhargava GK, Suvarna A, Shivashankar N, Raghavendra K, Asranna A, Thennarasu K, Jamuna R, Dawn BR, Saini J, Sinha S (2021) P300 in mesial temporal lobe epilepsy and its correlation with cognition—a MEG based prospective case-control study. Epilepsy Behav 114:1–7. https://doi.org/10.1016/j.yebeh.2020.107619
Mulert C, Jager L, Schmitt R, Bussfeld P, Pogarell O, Moller HJ, Juckel G, Hegerl U (2004) Integration of fMRI and simultaneous EEG: towards a comprehensive understanding of localization and time-course of brain activity in target detection. Neuroimage 22(1):83–94. https://doi.org/10.1016/j.neuroimage.2003.10.051
Nakamura-Palacios EM, de Almeida Benevides MC, Zago-Gomes MdP, Dias de Oliveira RW, de Vasconcellos VF, Passos de Castro LN, da Silva MC, Ramos PA, Fregni F (2012) Auditory event-related potentials (P3) and cognitive changes induced by frontal direct current stimulation in alcoholics according to Lesch alcoholism typology. Int J Neuropsychopharmacol 15(5):601–616. https://doi.org/10.1017/s1461145711001040
Nothdurft H-C (2006) Salience and target selection in visual search. Vis Cogn 14(4–8):514–542. https://doi.org/10.1080/13506280500194162
Pergher V, Tournoy J, Schoenmakers B, Van Hulle MM (2019) P300, gray matter volume and individual characteristics correlates in healthy elderly. Front Aging Neurosci. https://doi.org/10.3389/fnagi.2019.00104
Pinto JDG, Papesh MH, Hout MC (2020) The detail is in the difficulty: challenging search facilitates rich incidental object encoding. Mem Cognit 48(7):1214–1233. https://doi.org/10.3758/s13421-020-01051-3
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
Riddle J, Hwang K, Cellier D, Dhanani S, D’Esposito M (2019) Causal evidence for the role of neuronal oscillations in top-down and bottom-up attention. J Cogn Neurosci 31(5):768–779. https://doi.org/10.1162/jocn_a_01376
Rizer W, Aday JS, Carlson JM (2018) Changes in prefrontal cortex near infrared spectroscopy activity as a function of difficulty in a visual P300 paradigm. J near Infrared Spectrosc 26(4):222–228. https://doi.org/10.1177/0967033518791320
Sabeti M, Katebi SD, Rastgar K, Azimifar Z (2016) A multi-resolution approach to localize neural sources of P300 event-related brain potential. Comput Methods Programs Biomed 133:155–168. https://doi.org/10.1016/j.cmpb.2016.05.013
Sani I, Stemmann H, Caron B, Bullock D, Stemmler T, Fahle M, Pestilli F, Freiwald WA (2021) The human endogenous attentional control network includes a ventro-temporal cortical node. Nat Commun 12(1):1–16. https://doi.org/10.1038/s41467-020-20583-5
Silver MA, Kastner S (2009) Topographic maps in human frontal and parietal cortex. Trends Cogn Sci 13(11):488–495. https://doi.org/10.1016/j.tics.2009.08.005
Sklar AL, Coffman BA, Haas G, Ghuman A, Cho R, Salisbury DF (2020a) Inefficient visual search strategies in the first-episode schizophrenia spectrum. Schizophr Res 224:126–132. https://doi.org/10.1016/j.schres.2020.09.015
Sklar AL, Coffman BA, Salisbury DF (2020b) Localization of early-stage visual processing deficits at schizophrenia spectrum illness onset using magnetoencephalography. Schizophr Bull 46(4):955–963. https://doi.org/10.1093/schbul/sbaa010
Soltani M, Knight RT (2000) Neural origins of the P300. Crit Rev Neurobiol 14(3–4):199–224
Strobel A, Debener S, Sorger B, Peters JC, Kranczioch C, Hoechstetter K, Engel AK, Brocke B, Goebel R (2008) Novelty and target processing during an auditory novelty oddball: a simultaneous event-related potential and functional magnetic resonance imaging study. Neuroimage 40(2):869–883. https://doi.org/10.1016/j.neuroimage.2007.10.065
Tadel F, Bock E, Niso G, Mosher JC, Cousineau M, Pantazis D, Leahy RM, Baillet S (2019) MEG/EEG group analysis with brainstorm. Front Neurosci 13:1–21. https://doi.org/10.3389/fnins.2019.00076
Treisman AM, Gelade G (1980) A feature-integration theory of attention. Cogn Psychol 12(1):97–136. https://doi.org/10.1016/0010-0285(80)90005-5
Trinka E, Unterrainer J, Staffen W, Loscher NW, Ladurner G (2000) Delayed visual P3 in unilateral thalamic stroke. Eur J Neurol 7(5):517–522. https://doi.org/10.1046/j.1468-1331.2000.t01-1-00117.x
Uhrig S, Mittag G, Moller S, Voigt-Antons JN (2019) Neural correlates of speech quality dimensions analyzed using electroencephalography (EEG). J Neural Eng 16(3):1–19. https://doi.org/10.1088/1741-2552/aaf122
Verleger R, Heide W, Butt C, Kompf D (1994) Reduction of P3b in patients with temporo-parietal lesions. Brain Res Cogn Brain Res 2(2):103–116. https://doi.org/10.1016/0926-6410(94)90007-8
Volpe U, Mucci A, Bucci P, Merlotti E, Galderisi S, Maj M (2007) The cortical generators of P3a and P3b: a LORETA study. Brain Res Bull 73(4–6):220–230. https://doi.org/10.1016/j.brainresbull.2007.03.003
Wei X, Ni XL, Liu JY, Lang HY, Zhao R, Dai T, Qin W, Jia W, Fang P (2020) Simulation study on the spatiotemporal difference of complex neurodynamics between P3a and P3b. Complexity 2020:1–11. https://doi.org/10.1155/2020/2796809
Weigl M, Pham HH, Mecklinger A, Rosburg T (2020) The effect of shared distinctiveness on source memory: an event-related potential study. Cogn Affect Behav Neurosci 20(5):1027–1040. https://doi.org/10.3758/s13415-020-00817-1
Woldorff MG, Hazlett CJ, Fichtenholtz HM, Weissman DH, Dale AM, Song AW (2004) Functional parcellation of attentional control regions of the brain. J Cogn Neurosci 16(1):149–165. https://doi.org/10.1162/089892904322755638
Woodman GF (2010) A brief introduction to the use of event-related potentials in studies of perception and attention. Atten Percept Psychophys 72(8):2031–2046. https://doi.org/10.3758/APP.72.8.2031
Wright JM, Krekelberg B (2014) Transcranial direct current stimulation over posterior parietal cortex modulates visuospatial localization. J vis 14(9):1–15. https://doi.org/10.1167/14.9.5
Wronka E, Kaiser J, Coenen AM (2012) Neural generators of the auditory evoked potential components P3a and P3b. Acta Neurobiol Exp 72(1):51–64
Wu GS, Tang XC, Gan RP, Zeng JH, Hu YG, Xu LH, Wei YN, Tang YY, Chen T, Li CB, Wang JJ, Zhang TH (2022) Temporal and time-frequency features of auditory oddball response in distinct subtypes of patients at clinical high risk for psychosis. Eur Arch Psychiatry Clin Neurosci 272(3):449–459. https://doi.org/10.1007/s00406-021-01316-1
Xu G, Zhang Y, Hou H, Yan W (2006) Event-related potential studies of attention to shape under different stimuli tasks. Conf Proc IEEE Eng Med Biol Soc. https://doi.org/10.1109/IEMBS.2006.260902
Yan CG, Wang XD, Zuo XN, Zang YF (2016) DPABI: Data processing & analysis for (resting-state) brain imaging. Neuroinformatics 14(3):339–351. https://doi.org/10.1007/s12021-016-9299-4
Yang FC, Dokovna LB, Burwell RD (2022) Functional differentiation of dorsal and ventral posterior parietal cortex of the rat: Implications for controlled and stimulus-driven attention. Cereb Cortex 32(9):1787–1803. https://doi.org/10.1093/cercor/bhab308
Yoshiura T, Zhong J, Shibata DK, Kwok WE, Shrier DA, Numaguchi Y (1999) Functional MRI study of auditory and visual oddball tasks. NeuroReport 10(8):1683–1688. https://doi.org/10.1097/00001756-199906030-00011
Zhang DD, Lin YQ, Jing YM, Feng CL, Gu RL (2019) The dynamics of belief updating in human cooperation: findings from inter-brain ERP hyperscanning. Neuroimage 198:1–12. https://doi.org/10.1016/j.neuroimage.2019.05.029
Zhou L, Wang GH, Nan C, Wang HL, Liu ZC, Bai HP (2019) Abnormalities in P300 components in depression: an ERP-sLORETA study. Nord J Psychiatry 73(1):1–8. https://doi.org/10.1080/08039488.2018.1478991
Acknowledgements
This work was supported by the National Nature Science Foundation of China [Grant Number 62176045]; the Programme of Introducing Talents of Discipline to Universities (the 111 project) [Grant Number B12027], and the Fundamental Research Funds for the Central Universities [ZYGX2020FRJH014].
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflicts of interest to declare that are relevant to the content of this article.
Ethical Approval
The study was approved by the Ethics Committee of the University of Electronic Science and Technology of China. The study was performed in accordance with the ethical standards as the Declaration of Helsinki.
Additional information
Handling Editor: Micah M. Murray.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zhang, Q., Luo, C., Ngetich, R. et al. Visual Selective Attention P300 Source in Frontal-Parietal Lobe: ERP and fMRI Study. Brain Topogr 35, 636–650 (2022). https://doi.org/10.1007/s10548-022-00916-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10548-022-00916-x