Brain Topography

, Volume 24, Issue 2, pp 164–182 | Cite as

Electrophysiological Explorations of the Cause and Effect of Inhibition of Return in a Cue–Target Paradigm

  • Yin Tian
  • Raymond M. Klein
  • Jason Satel
  • Peng Xu
  • Dezhong Yao
Original Paper


Facilitation and inhibition of return (IOR) are, respectively, faster and slower responses to a peripherally cued target. In a spatially uninformative peripheral cueing task, facilitation is normally observed when the interval between the cue and target stimulus, the stimulus onset asynchrony (SOA), is shorter than 250 ms, while IOR is normally observed when an SOA greater than 250 ms is used. Since Posner and Cohen’s (Attention and performance X, 1984) seminal study, IOR has become an actively investigated component of orienting. In this study, using ERPs and the source localization algorithm, LORETA, we seek to examine the brain mechanisms involved in IOR by localizing the different stages of processing after the appearance of a cue that captures attention exogenously. Unlike previous ERP investigations of IOR, this study analyzes the neural activity (via EEG) produced in response to the cue, prior to the appearance of the target. Neural activations were approximately divided into three stages. In the early stage (110–240 ms), involved activations are in the prefrontal cortex, the bilateral intraparietal cortex, and the contralateral occipito-temporal cortex. In the middle stage (240–350 ms), activations are primarily found in the frontal cortex and the parietal cortex. In the late stage (350–650 ms), the main activations are in the occipito-parietal cortex, but unlike in the early stage, the activation areas have shifted to the hemisphere ipsilateral to the cued location. These findings indicate that IOR is related to both attentional and motor response processes and suggest that the time course of initial facilitation and IOR is concurrent and mediated by two neural networks. Building upon our results, electrophysiological, electroencephalographic, and behavioral results in the literature and extending previous spatial theories of IOR, we propose here a spatio-temporal theory of IOR based upon post-cue dynamics.


Event-related potentials (ERPs) Facilitation Inhibition of return (IOR) Low-resolution electromagnetic tomography (LORETA) Spatially uninformative peripheral cue (SUPC) 



We would like to thank Zhiguo Wang for his help in preparing this manuscript, and also thank Dr. Juan Lupiáñez for his many constructive comments. Funding: This work was supported by the National Nature Science Foundation of China (Grant Numbers 60736029, 60701015), the 863 Project 2009AA02Z301, and the PCSIRT project. Yin Tian was also supported by CPSF (No.20100481379) and PSF of UESTC (No.20100013).


  1. Berger A, Henik A, Rafal R (2005) Competition between endogenous and exogenous orienting of visual attention. J Exp Psychol Gen 134(2):207–221PubMedCrossRefGoogle Scholar
  2. Berlucchi G, Chelazzi L, Tassinari G (2000) Volitional covert orienting to a peripheral cue does not suppress cue-induced inhibition of return. J Cogn Neurosci 12(4):648–663PubMedCrossRefGoogle Scholar
  3. Chica AB, Lupianez J, Bartolomeo P (2006) Dissociating inhibition of return from endogenous orienting of spatial attention: evidence from detection and discrimination tasks. Cogn Neuropsychol 23(7):1015–1034PubMedCrossRefGoogle Scholar
  4. Danziger S, Kingstone A (1999) Unmasking the inhibition of return phenomenon. Percept Psychophys 61:1024–1037PubMedCrossRefGoogle Scholar
  5. Danziger S, Fenrich R, Rafal RD (1997) Inhibitory tagging of locations in the blind field of hemianopic patients. Conscious Cogn 6:291–307CrossRefGoogle Scholar
  6. Di Russo F, Martinez A, Sereno MI, Pitzalis S, Hillyard SA (2001) Cortical sources of the early components of the visual evoked potential. Hum Brain Map 15:95–111CrossRefGoogle Scholar
  7. Dorris MC, Taylor TL, Klein RM, Munoz DP (1998). Neural correlate of inhibition of return (IOR): visual and motor preparatory signals in the monkey superior colliculus (SC). In: Ann Meet Cogn Neurosci Soc, San FranciscoGoogle Scholar
  8. Dorris MC, Klein RM, Everling S, Munoz DP (2002) Contribution of the primate superior colliculus to inhibition of return. J Cogn Neurosci 14:1256–1263PubMedCrossRefGoogle Scholar
  9. Dukewich KR (2009) Reconceptualizing inhibition of return as habituation of the orienting response. Psychon Bull Rev 16(2):238–251PubMedCrossRefGoogle Scholar
  10. Eimer M (1994) An ERP study on visual spatial priming with peripheral onsets. Psychophysiology 31:154–163PubMedCrossRefGoogle Scholar
  11. Fecteau JH, Munoz DP (2005) Correlates of capture of attention and inhibition of return across stages of visual processing. J Cogn Neurosci 17:1714–1727PubMedCrossRefGoogle Scholar
  12. Fuchs M, Drenckhahn R (1998) An improved boundary element method for realistic volume-conductor modeling. IEEE Trans Biomed Eng 45:980–997PubMedCrossRefGoogle Scholar
  13. Godijn R, Theeuwes J (2002) Oculomotor capture and inhibition of return: evidence for an oculomotor suppression account of IOR. Psychol Res 66:234–246PubMedCrossRefGoogle Scholar
  14. Godijn R, Theeuwes J (2004) The relationship between inhibition of return and saccade trajectory deviations. J Exp Psychol Hum Percept Perform 30:538–554PubMedCrossRefGoogle Scholar
  15. Greenwood PM, Goff WR (1987) Modification of median nerve somatic evoked potentials by prior median nerve, peroneal nerve, and auditory stimulation. Electroencephalogr Clin Neurophysiol 68:295–302PubMedCrossRefGoogle Scholar
  16. Handy TC, Jha AP, Mangun GR (1999) Promoting novelty in vision: Inhibition of return modulates perceptual-level processing. Psychol Sci 10:157–161CrossRefGoogle Scholar
  17. Hopfinger J (2005). Electrophysiology of reflexive attention. In: Itti L, Rees G, Tsotsos J (eds) Encyclopedia on the neurobiology of attention. Elsevier Academic Press, Amsterdam, pp 219–235Google Scholar
  18. Hopfinger JB, Mangun GR (1998) Reflexive attention modulates processing of visual stimuli in human extrastriate cortex. Psychol Sci 9:441–447CrossRefGoogle Scholar
  19. Hopfinger JB, Mangun GR (2001) Tracking the influence of reflexive attention on sensory and cognitive processing. Cogn Affect Behavior Neurosci 1:56–65CrossRefGoogle Scholar
  20. Iragui VJ, Kutas M, Mitchiner MR, Hillyard SA (1993) Effects of aging on event-related brain potentials and reaction times in an auditory oddball task. Psychophysiology 30:10–22PubMedCrossRefGoogle Scholar
  21. Ivanoff J, Klein RM (2001) The presence of a nonresponding effector increases inhibition of return. Psychonom Bull Rev 8:307–314CrossRefGoogle Scholar
  22. Ivanoff J, Klein RM (2006) Inhibition of return: Sensitivity and criterion as a function of response time. J Exp Psychol Hum Percept Perform 32(4):908–919PubMedCrossRefGoogle Scholar
  23. Kingstone A, Pratt J (1999) Inhibition of return is composed of attentional and oculomotor process. Percept Psychophys 61:1046–1054PubMedCrossRefGoogle Scholar
  24. Kiss I, Pisio C, Francois A, Schopflocher D (1998) Central executive function in working memory: event-related brain potential studies. Cogn Brain Res 6:235–247CrossRefGoogle Scholar
  25. Klein RM (2000) Inhibition of return. Trends Cogn Sci 4:138–147PubMedCrossRefGoogle Scholar
  26. Klein RM (2004) Orienting and inhibition of return. In: Gazzaniga MS (ed) The new cognitive neurosciences, 3rd edn. MIT Press, CambridgeGoogle Scholar
  27. Klein RM (2005) On the role of endogenous orienting in the inhibitory aftermath of exogenous orienting. In: Mayr U, Awh E, Keele S (eds) Developing Individuality in the human brain: A tribute to Michael Posner. APA Books, Washington, pp 45–64CrossRefGoogle Scholar
  28. Klein RM, Dick B (2002) Temporal dynamics of reflexive attention shifts: a dual-stream rapid serial visual presentation exploration. Psychol Sci 13:176–179PubMedCrossRefGoogle Scholar
  29. Klein RM, MacInnes WJ (1999) Inhibition of return is a foraging facilitator in visual search. Psych Sci 10:346–352CrossRefGoogle Scholar
  30. Klein RM, Taylor TL (1994) Categories of cognitive inhibition with reference to attention. In: Dagenbach D, Car TH (eds) Inhibitory processes in attention, memory, and language. Academic Press, San DiegoGoogle Scholar
  31. Lepsien J, Pollmann S (2002) Covert reorienting and inhibition of return: an event-related fMRI study. J Cogn Neurosci 14:127–144PubMedCrossRefGoogle Scholar
  32. Lupiáñez J (2010) Inhibition of Return. In Nobre AC, Coull JT (eds) Attention and Time. Oxford University Press, Oxford, UK, pp. 17–34Google Scholar
  33. Lupiáñez J, Milán EG, Tornay FJ, Madrid E, Tudela R (1997) Does IOR occur in discrimination tasks? Yes, it does, but later. Percept Psychophys 59:1241–1254PubMedCrossRefGoogle Scholar
  34. Lupiáñez J, Decaix C, Sieroff E, Chokron S, Milliken B, Bartolomeo P (2004) Independent effects of endogenous and exogenous spatial cueing: inhibition of return at endogenously attended target locations. Exp Brain Res 159(4):447–457PubMedCrossRefGoogle Scholar
  35. Lupiáñez J, Klein RM, Bartolomeo P (2006) Inhibition of return: twenty years after. Cogn Neuropsychol 23(7):1003–1014PubMedCrossRefGoogle Scholar
  36. Mayer AR, Seidenberg M, Dorflinger JM, Rao SM (2005) An event-related fMRI study of exogenous orienting: supporting evidence for the cortical basis of inhibition of return? J Cogn Neurosci 16:1262–1271CrossRefGoogle Scholar
  37. McDonald JJ, Ward LM, Kiehl KA (1999) An event-related brain potential study of inhibition of return. Percept Psychophys 61:1411–1423PubMedCrossRefGoogle Scholar
  38. Noesselt T, Hillyard SA, Woldorff MG, Schoenfeld A, Hagner T, Jancke L, Tempelmann C, Hinrichs H, Heinze HJ (2002) Delayed striate cortical activation during spatial attention. Neuron 35:575–587PubMedCrossRefGoogle Scholar
  39. Pascual-Marqui RD, Michel CM, Lehmann D (1994) Low resolution electromagnetic tomography: a new method for localizing electrical activity in the brain. Int J Psychophysiol 18:49–65PubMedCrossRefGoogle Scholar
  40. Posner MI, Cohen Y (1984) Components of visual orienting. In: Bouma H, Bouwhuis DG (eds) Attention and performance X. Erlbaum, Hillsdale, pp 531–556Google Scholar
  41. Posner MI, Rafal RD, Choate LS, Vaughan J (1985) Inhibition of return: Neural basis and function. Cogn Neuropsychol 2:211–228CrossRefGoogle Scholar
  42. Prime DJ, Ward LM (2004) Inhibition of return from stimulus to response. Psychol Sci 15:272–276PubMedCrossRefGoogle Scholar
  43. Prime DJ, Ward LM (2006) Cortical expressions of inhibition of return. Brain Res 1072:161–174PubMedCrossRefGoogle Scholar
  44. Rafal R, Davies J, Lauder J (2006) Inhibitory tagging at subsequently fixated locations: generation of “inhibition of return” without saccade inhibition. Vis Cogn 13(3):308–323CrossRefGoogle Scholar
  45. Reuter-Lorenz PA, Jha AP, Rosenquist JN (1996) What is inhibited in inhibition of return? J Exp Psycho Hum Percept Perform 22:367–378CrossRefGoogle Scholar
  46. Ro T, Pratt J, Rafal RD (2000) Inhibition of return in saccadic eye movements. Exp Brain Res 130:264–268PubMedCrossRefGoogle Scholar
  47. Simson R, Ritter W, Vaughan HG Jr (1985) Effects of expectation on negative potentials during visual processing. Electroencephalogr Clin Neurophysiol 62:25–31PubMedCrossRefGoogle Scholar
  48. Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. Thieme, New YorkGoogle Scholar
  49. Tassinari G, Aglioti S, Chelazzi L, Marzi CA, Berlucchi G (1987) Distribution in the visual field of the costs of voluntarily associated attention and of the inhibitory after-effects of covert orienting. Neuropsychologia 25:55–71PubMedCrossRefGoogle Scholar
  50. Theeuwes J (1991) Exogenous and endogenous control of attention: the effect of visual onsets and offsets. Percept Psychophys 49(1):83–90PubMedCrossRefGoogle Scholar
  51. Tian Y, Yao D (2008) A study on the neural mechanism of inhibition of return by the event-related potential in the Go/Nogo task. Biol Psychol 79:171–178PubMedCrossRefGoogle Scholar
  52. Tipper SP, Rafal RD, Reuter-Lorenz PA, Starrveldt Y, Ro T, Egly R, Danziger S, Weaver B (1997) Object based facilitation and inhibition from visual orienting in the human split. J Exp Psychol Hum Percept Perform 23:1522–1532PubMedCrossRefGoogle Scholar
  53. Tucker DM (1993) Spatial sampling of head electrical fields: the geodesic sensor net. Electroenceph Clin Neurophysiol 87:154–163PubMedCrossRefGoogle Scholar
  54. Wascher E, Tipper SP (2004) Revealing effects of noninformative spatial cues: an EEG study of inhibition of return. Psychophysiol 41:716–728CrossRefGoogle Scholar
  55. Woldorff MG (1993) Distortion of ERP averages due to overlap from temporally adjacent ERPs: analysis and correction. Psychophysics 22:54–62Google Scholar
  56. Xu P, Tian Y, Chen H, Yao D (2007) Lp norm iterative sparse solution for EEG source localization. IEEE Trans Biomed Eng 54:400–409PubMedCrossRefGoogle Scholar
  57. Xu P, Tian Y, Lei X, Hu X, Yao D (2008) Equivalent charge source model based iterative maximum neighbor weight for sparse EEG source localization, annals of biomedical engineering. Ann Biomed Eng 36(12):2051–2067PubMedCrossRefGoogle Scholar
  58. Yao D, He B (1998) The Laplacian weighted minimum norm estimate of three dimensional equivalent charge distribution in the brain. In: Proc Annu Int Conf IEEE Engineering in Medicine and Biology Society, pp 2108–2111Google Scholar
  59. Yao D, Wang L, Oostenveld R, Nielsen KD, Arendt-Nielsen L, Chen A (2005) A comparative study of different references for EEG spectral mapping: the issue of the neutral reference and the use of the infinity reference. Physiol Meas 26:173–184PubMedCrossRefGoogle Scholar
  60. Yin G, Zhang J, Tian Y, Yao D (2009) A multi-component decomposition algorithm for event-related potentials. J Neurosci Methods 178(1):219–227PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  1. 1.Key Laboratory for NeuroInformation of Ministry of Education, School of Life Science and TechnologyUniversity of Electronic Science and Technology of ChinaChengDuChina
  2. 2.Department of PsychologyDalhousie UniversityHalifaxCanada
  3. 3.College of Bio-informationChongQing University of Posts and TelecommunicationsChongQingChina

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