Abstract
Inhibition of return (IOR) is a bias against reorienting attention to a previously cued location. In this study, using single-pulse transcranial magnetic stimulation (TMS), we show that the human frontal eye fields (FEF) play a crucial role in the generation of IOR. When TMS was applied over the right FEF at a time interval after a visual cue but shortly before the target, IOR was modulated in the hemifield ipsilateral to the TMS such that responses to a previously cued target were no longer slower than responses to uncued targets. Control TMS over the superior parietal lobule, as well as TMS of the FEF shortly after the cue but well before the target, had no influence on IOR. We further show that the FEF is involved with visual selection as responses to targets appearing contralateral to the TMS of the FEF, but not the control site, were delayed. These results suggest that the FEF produces IOR by biasing attention and eye movements away from a previously attended location and facilitating target detection at novel locations.
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References
Abrams RA, Dobkin RS (1994) Inhibition of return: effects of attentional cuing on eye movement latencies. J Exp Psychol Hum Percept Perform 20:467–477
Andersen RA, Snyder LH, Bradley DC, Xing J (1997) Multimodal representation of space in the posterior parietal cortex and its use in planning movements. Annu Rev Neurosci 20:303–330
Bruce CJ, Goldberg ME (1985) Primate frontal eye fields. I. Single neurons discharging before saccades. J Neurophysiol 53:603–635
Cadwell J (1990) Principles of magnetoelectric stimulation. In: Chokroverty S (ed) Magnetic stimulation in clinical neurophysiology. Butterworth, Boston, pp 13–32
Chelazzi L, Biscaldi M, Corbetta M, Peru A, Tassinari G, Berlucchi G (1995) Oculomotor activity and visual spatial attention. Behav Brain Res 71:81–88
Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M, Cohen LG (1997) Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 48:1398–1403
Collie A, Maruff P, Yucel M, Danckert J, Currie J (2000) Spatiotemporal distribution of facilitation and inhibition of return arising from the reflexive orienting of covert attention. J Exp Psychol Hum Percept Perform 26:1733–1745
Corbetta M, Akbudak E, Conturo T, Snyder A, Ollinger J, Drury H, Linenweber M, Petersen S, Raichle M, Van Essen D, Shulman G (1998) A common network of functional areas for attention and eye movements. Neuron 21:761–773
Danziger S, Fendrich R, Rafal RD (1997) Inhibitory tagging of locations in the blind field of hemianopic patients. Conscious Cogn 6:291–307
Dorris MC, Everling S, Klein R, Munoz DP (1998) Neural correlate of inhibition of return (IOR): visual and motor preparatory signals in the monkey superior colliculus (SC). Soc Neurosci Abstr 24:417
Dorris MC, Everling S, Klein R, Munoz DP (2002) Contribution of the primate superior colliculus to inhibition of return. J Cogn Neurosci 14:1256–1263
Driver J, Mattingley JB (1998) Parietal neglect and visual awareness. Nat Neurosci 1:17–22
Fox P, Ingham R, George MS, Mayberg H, Ingham J, Roby J, Martin C, Jerabek P (1997) Imaging human intra-cerebral connectivity by PET during TMS. Neuroreport 8:2787–2791
Groh JM, Sparks DL (1996) Saccades to somatosensory targets. I. Behavioral characteristics. J Neurophysiol 75:412–427
Grosbras M-H, Paus T (2002) Transcranial magnetic stimulation of the human frontal eye field: effects on visual perception and attention. J Cogn Neurosci 14:1109–1120
Handy TC, Jha AP, Mangun GR (1999) Promoting novelty in vision: inhibition of return modulates perceptual-level processing. Psych Sci 10:157–161
Henik A, Rafal R, Rhodes D (1994) Endogenously generated and visually guided saccades after lesions of the human frontal eye fields. J Cogn Neurosci 6:400–411
Jonides J, Mack R (1984) On the cost and benefit of cost and benefit. Psych Bull 96:29–42
Kingstone A, Pratt J (1999) Inhibition of return is composed of attentional and oculomotor processes. Percept Psychophys 61:1046–1054
Klein R (1988) Inhibitory tagging system facilitates visual search. Nature 334:430–431
Klein R (2000) Inhibition of return: what, where, when, why and how. Trends Cogn Sci 4:138–147
Klein RM, MacInnes WJ (1999) Inhibition of return is a foraging facilitator in visual search. Psych Sci 10:346–352
Kosslyn SM, Pascual-Leone A, Felician O, Camposano S, Keenan JP, Thompson WL, Ganis G, Sukel KE, Alpert NM (1999) The role of area 17 in visual imagery: convergent evidence from PET and rTMS [see comments]. Science 284:167–170
Kustov AA, Robinson DL (1996) Shared neural control of attentional shifts and eye movements. Nature 384:74–77
Lepsien J, Pollmann S (2002) Covert reorienting and inhibition of return: an event-related fMRI study. J Cogn Neurosci 14:127–144
Luna B, Thulborn KR, Strojwas MH, McCurtain BJ, Berman RA, Genovese CR, Sweeney JA (1998) Dorsal cortical regions subserving visually guided saccades in humans: an fMRI study. Cereb Cortex 8:40–47
Lupianez J, Milan EG, Tornay FJ, Madrid E, Tudela P (1997) Does IOR occur in discrimination tasks? Yes, it does, but later. Percept Psychophys 59:1241–1254
Maruff P, Yucel M, Danckert J, Stuart G, Currie J (1999) Facilitation and inhibition arising from the exogenous orienting of covert attention depends on the temporal properties of spatial cues and targets. Neuropsychologia 37:731–744
Moore T, Fallah M (2001) Control of eye movements and spatial attention. Proc Natl Acad Sci USA 98:1273–1276
Nobre AC, Sebestyen GN, Gitelman DR, Mesulam MM, Frackowiak RS, Frith CD (1997) Functional localization of the system for visuospatial attention using positron emission tomography. Brain 120:515–533
Nobre AC, Gitelman DR, Dias EC, Mesulam MM (2000) Covert visual spatial orienting and saccades: overlapping neural systems. Neuroimage 11:210–216
Paus T (1996) Location and function of the human frontal eye-field: a selective review. Neuropsychologia 34:475–483
Paus T, Jech R, Thompson CJ, Comeau R, Peters T, Evans AC (1997) Transcranial magnetic stimulation during positron emission tomography: a new method for studying connectivity of the human cerebral cortex. J Neurosci 17:3178–3184
Posner MI, Boies SJ (1971) Components of attention. Psych Rev 78:391–408
Posner MI, Cohen Y (1984) Components of visual orienting. In: Bouma H, Bouwhuis D (eds) Attention and performance X. Erlbaum, Hillsdale, pp 531–556
Posner MI, Rafal RD, Choate L, Vaughn J (1985) Inhibition of return: neural basis and function. Cogn Neuropsych 2:211–228
Pratt J, Abrams RA (1999) Inhibition of return in discrimination tasks. J Exp Psychol Hum Percept Perform 25:229–242
Rafal RD (1994) Neglect. Curr Opin Neurobiol 4:2312–2316
Rafal RD, Posner MI, Friedman JH, Inhoff AW, Bernstein E (1988) Orienting of visual attention in progressive supranuclear palsy. Brain 111:267–280
Rafal RD, Calabresi P, Brennan C, Sciolto T (1989) Saccade preparation inhibits reorienting to recently attended locations. J Exp Psychol Hum Percept Perform 15:673–685
Rafal RD, Egly R, Rhodes D (1994) Effects of inhibition of return on voluntary and visually guided saccades. Can J Exp Psych 48:284–300
Rafal RD, Machado L, Ro T, Ingle H (2000) Looking forward to looking: saccade preparation and the control of midbrain visuomotor reflexes. In: Monsell S, Driver J (eds) Attention and performance XVIII. MIT Press, Cambridge
Rizzolatti G, Riggio L, Dascola I, Umilta C (1987) Reorienting attention across the horizontal and vertical meridians: evidence in favor of a premotor theory of attention. Neuropsychologia 25:30–36
Ro T, Henik A, Machado L, Rafal R (1997) Transcranial magnetic stimulation of the prefrontal cortex delays contralateral endogenous saccades. J Cogn Neurosci 9:433–440
Ro T, Cheifet S, Ingle H, Shoup R, Rafal R (1999) Localization of the human frontal eye fields and motor hand area with transcranial magnetic stimulation and magnetic resonance imaging. Neuropsychologia 37:225–231
Ro T, Farnè A, Chang E (2002) Locating the human frontal eye fields with transcranial magnetic stimulation. J Clin Exp Neuropsychol 24:930–940
Sapir A, Soroker N, Berger A, Henik A (1999) Inhibition of return in spatial attention: direct evidence for collicular generation. Nat Neurosci 2:1053–1054
Schall JD, Thompson KG (1999) Neural selection and control of visually guided eye movements. Annu Rev Neurosci 22:241–259
Sparks DA (1989) The deep layers of the superior colliculus. In: Wurtz R, Goldberg M (eds) The Neurobiology of Saccadic Eye Movements. Elsevier Science Publishers BV, Amsterdam, pp 283–313
Spence C, Lloyd D, McGlone F, Nicholls ME, Driver J (2000) Inhibition of return is supramodal: a demonstration between all possible pairings of vision, touch, and audition. Exp Brain Res 134:42–48
Tassinari G, Aglioti S, Chelazzi L, Peru A, Berlucchi G (1994) Do peripheral non-informative cues induce early facilitation of target detection? Vision Res 34:179–189
Taylor TL, Klein RM (1998) On the causes and effects of inhibition of return. Psychonom Bull Review 5:625–643
Taylor TL, Klein RM (2000) Visual and motor effects in inhibition of return. J Exp Psychol Hum Percept Perform 26:1639–1656
Tipper SP, Weaver B, Jerreat LM, Burak AL (1994) Object- and environment-based inhibition of return of visual attention. J Exp Psychol Hum Percept Perform 20:478–499
Tipper SP, Rafal RD, Reuter-Lorenz P, Starrveldt Y, Ro T, Egly R, Danziger S, Weaver B (1997) Object-based facilitation and inhibition from visual orienting in the human split-brain. J Exp Psychol Hum Percept Perform 23:1522–1532
Acknowledgements
We thank Bob Rafal and Ayelet Sapir for helpful comments on earlier drafts of this manuscript and John Ashburner for assistance with SPM99 and Matlab. This research was supported by the US PHS and the Human Frontiers Science Program.
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Ro, T., Farnè, A. & Chang, E. Inhibition of return and the human frontal eye fields. Exp Brain Res 150, 290–296 (2003). https://doi.org/10.1007/s00221-003-1470-0
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DOI: https://doi.org/10.1007/s00221-003-1470-0