Abstract
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.
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References
Berger A, Henik A, Rafal R (2005) Competition between endogenous and exogenous orienting of visual attention. J Exp Psychol Gen 134(2):207–221
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):648–663
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):1015–1034
Danziger S, Kingstone A (1999) Unmasking the inhibition of return phenomenon. Percept Psychophys 61:1024–1037
Danziger S, Fenrich R, Rafal RD (1997) Inhibitory tagging of locations in the blind field of hemianopic patients. Conscious Cogn 6:291–307
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 15:95–111
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 Francisco
Dorris MC, Klein RM, Everling S, Munoz DP (2002) Contribution of the primate superior colliculus to inhibition of return. J Cogn Neurosci 14:1256–1263
Dukewich KR (2009) Reconceptualizing inhibition of return as habituation of the orienting response. Psychon Bull Rev 16(2):238–251
Eimer M (1994) An ERP study on visual spatial priming with peripheral onsets. Psychophysiology 31:154–163
Fecteau JH, Munoz DP (2005) Correlates of capture of attention and inhibition of return across stages of visual processing. J Cogn Neurosci 17:1714–1727
Fuchs M, Drenckhahn R (1998) An improved boundary element method for realistic volume-conductor modeling. IEEE Trans Biomed Eng 45:980–997
Godijn R, Theeuwes J (2002) Oculomotor capture and inhibition of return: evidence for an oculomotor suppression account of IOR. Psychol Res 66:234–246
Godijn R, Theeuwes J (2004) The relationship between inhibition of return and saccade trajectory deviations. J Exp Psychol Hum Percept Perform 30:538–554
Greenwood PM, Goff WR (1987) Modification of median nerve somatic evoked potentials by prior median nerve, peroneal nerve, and auditory stimulation. Electroencephalogr Clin Neurophysiol 68:295–302
Handy TC, Jha AP, Mangun GR (1999) Promoting novelty in vision: Inhibition of return modulates perceptual-level processing. Psychol Sci 10:157–161
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 219–235
Hopfinger JB, Mangun GR (1998) Reflexive attention modulates processing of visual stimuli in human extrastriate cortex. Psychol Sci 9:441–447
Hopfinger JB, Mangun GR (2001) Tracking the influence of reflexive attention on sensory and cognitive processing. Cogn Affect Behavior Neurosci 1:56–65
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 30:10–22
Ivanoff J, Klein RM (2001) The presence of a nonresponding effector increases inhibition of return. Psychonom Bull Rev 8:307–314
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):908–919
Kingstone A, Pratt J (1999) Inhibition of return is composed of attentional and oculomotor process. Percept Psychophys 61:1046–1054
Kiss I, Pisio C, Francois A, Schopflocher D (1998) Central executive function in working memory: event-related brain potential studies. Cogn Brain Res 6:235–247
Klein RM (2000) Inhibition of return. Trends Cogn Sci 4:138–147
Klein RM (2004) Orienting and inhibition of return. In: Gazzaniga MS (ed) The new cognitive neurosciences, 3rd edn. MIT Press, Cambridge
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 45–64
Klein RM, Dick B (2002) Temporal dynamics of reflexive attention shifts: a dual-stream rapid serial visual presentation exploration. Psychol Sci 13:176–179
Klein RM, MacInnes WJ (1999) Inhibition of return is a foraging facilitator in visual search. Psych Sci 10:346–352
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 Diego
Lepsien J, Pollmann S (2002) Covert reorienting and inhibition of return: an event-related fMRI study. J Cogn Neurosci 14:127–144
Lupiáñez J (2010) Inhibition of Return. In Nobre AC, Coull JT (eds) Attention and Time. Oxford University Press, Oxford, UK, pp. 17–34
Lupiáñez J, Milán EG, Tornay FJ, Madrid E, Tudela R (1997) Does IOR occur in discrimination tasks? Yes, it does, but later. Percept Psychophys 59:1241–1254
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):447–457
Lupiáñez J, Klein RM, Bartolomeo P (2006) Inhibition of return: twenty years after. Cogn Neuropsychol 23(7):1003–1014
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 16:1262–1271
McDonald JJ, Ward LM, Kiehl KA (1999) An event-related brain potential study of inhibition of return. Percept Psychophys 61:1411–1423
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 35:575–587
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 18:49–65
Posner MI, Cohen Y (1984) Components of visual orienting. In: Bouma H, Bouwhuis DG (eds) Attention and performance X. Erlbaum, Hillsdale, pp 531–556
Posner MI, Rafal RD, Choate LS, Vaughan J (1985) Inhibition of return: Neural basis and function. Cogn Neuropsychol 2:211–228
Prime DJ, Ward LM (2004) Inhibition of return from stimulus to response. Psychol Sci 15:272–276
Prime DJ, Ward LM (2006) Cortical expressions of inhibition of return. Brain Res 1072:161–174
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):308–323
Reuter-Lorenz PA, Jha AP, Rosenquist JN (1996) What is inhibited in inhibition of return? J Exp Psycho Hum Percept Perform 22:367–378
Ro T, Pratt J, Rafal RD (2000) Inhibition of return in saccadic eye movements. Exp Brain Res 130:264–268
Simson R, Ritter W, Vaughan HG Jr (1985) Effects of expectation on negative potentials during visual processing. Electroencephalogr Clin Neurophysiol 62:25–31
Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. Thieme, New York
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 25:55–71
Theeuwes J (1991) Exogenous and endogenous control of attention: the effect of visual onsets and offsets. Percept Psychophys 49(1):83–90
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 79:171–178
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 23:1522–1532
Tucker DM (1993) Spatial sampling of head electrical fields: the geodesic sensor net. Electroenceph Clin Neurophysiol 87:154–163
Wascher E, Tipper SP (2004) Revealing effects of noninformative spatial cues: an EEG study of inhibition of return. Psychophysiol 41:716–728
Woldorff MG (1993) Distortion of ERP averages due to overlap from temporally adjacent ERPs: analysis and correction. Psychophysics 22:54–62
Xu P, Tian Y, Chen H, Yao D (2007) Lp norm iterative sparse solution for EEG source localization. IEEE Trans Biomed Eng 54:400–409
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):2051–2067
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 2108–2111
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 26:173–184
Yin G, Zhang J, Tian Y, Yao D (2009) A multi-component decomposition algorithm for event-related potentials. J Neurosci Methods 178(1):219–227
Acknowledgments
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).
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Appendix
Calculation of the Amplitude Weight Centre (AWC)
In order to compare the differences among the scalp topologies of different moments or different subjects, we utilized the amplitude weight centre (AWC) technique (Yao et al. 2005). In this paper, we define a local AWC of an electrode with its N neighbor electrodes to characterize the topology distribution in the region of interest (ROI). In the current work, ROI is defined as the scalp area enclosing the electrodes with the positive/negative maximum potential.
The local AWC at moment t is defined as follows:
where A n (t) is the potential at the nth electrode in the ROI (\( x_{n} ,y_{n} ,z_{n} \)) represents the coordinates of the nth electrode, and N is the number of electrodes consisting of the ROI (in this work, N = 11).
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Tian, Y., Klein, R.M., Satel, J. et al. Electrophysiological Explorations of the Cause and Effect of Inhibition of Return in a Cue–Target Paradigm. Brain Topogr 24, 164–182 (2011). https://doi.org/10.1007/s10548-011-0172-3
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DOI: https://doi.org/10.1007/s10548-011-0172-3