Abstract
Peripheral cues induce facilitation with short cue-target intervals and inhibition of return (IOR) with long cue-target intervals. Modulations of facilitation and IOR by continuous displacements of the eye or the cued stimuli are poorly understood. Previously, the retinal coordinates of the cued location were changed by saccadic or smooth pursuit eye movements during the cue-target interval. In contrast, we probed the relevant coordinates for facilitation and IOR by orthogonally varying object motion (stationary, moving) and eye movement (fixation, smooth pursuit). In the pursuit conditions, cue and target were presented during the ongoing eye movement and observers made a saccade to the target. Importantly, we found facilitation and IOR of similar size during smooth pursuit and fixation. The results suggest that involuntary orienting is possible even when attention has to be allocated to the moving target during smooth pursuit. Comparison of conditions with stabilized and moving objects suggest an oculocentric basis for facilitation as well as inhibition. Facilitation and IOR were reduced with objects that moved on the retina both with smooth pursuit and eye fixation.
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Notes
We use the term “retinal” synonymous to “oculocentric”. In keeping with general usage, we oppose this reference frame to “environmental” that is synonymous to “spatial”. We would like to point out that “environmental” is inexact because a head-centric (egocentric) reference frame cannot be ruled out, as the head was fixed. The term “non-retinotopic” would be more exact.
References
Abrams RA, Dobkin RS (1994) Inhibition of return: effects of attentional cuing on eye movement latencies. J Exp Psychol Hum Percept Perfom 20(3):467–477
Abrams RA, Pratt J (2000) Oculocentric coding of inhibited eye movements to recently attended locations. J Exp Psychol Hum Percept Perfom 26(2):776–788
Boman D, Braun D, Hotson J (1996) Stationary and pursuit visual fixation share similar behavior. Vision Res 36(5):751–763
Briand KA, Larrison AL, Sereno AB (2000) Inhibition of return in manual and saccadic response systems. Percept Psychophys 62(8):1512–1524
Cynader M, Berman N (1972) Receptive-field organization of monkey superior colliculus. J Neurophysiol 35(2):187–201
Dassonville P, Schlag J, Schlag-Rey M (1992) The frontal eye field provides the goal of saccadic eye movement. Exp Brain Res 89(2):300–310
Duhamel JR, Bremmer F, BenHamed S, Graf W (1997) Spatial invariance of visual receptive fields in parietal cortex neurons. Nature 389(6653):845–848
Gardner JL, Merriam EP, Movshon JA, Heeger DJ (2008) Maps of visual space in human occipital cortex are retinotopic, not spatiotopic. J Neurosci 28(15):3988–3999
Gilchrist ID, Harvey M (2000) Refixation frequency and memory mechanisms in visual search. Curr Biol 10(19):1209–1212
Hooge IT, Over EA, van Wezel RJ, Frens MA (2005) Inhibition of return is not a foraging facilitator in saccadic search and free viewing. Vision Res 45(14):1901–1908
Hunt AR, Kingstone A (2003) Inhibition of return: dissociating attentional and oculomotor components. J Exp Psychol Hum Percept Perform 29(5):1068–1074
Kerzel D, Ziegler NE (2005) Visual short-term memory during smooth pursuit eye movements. J Exp Psychol Hum Percept Perform 31(2):354–372
Kerzel D, Aivar MP, Ziegler NE, Brenner E (2006) Mislocalization of flashes during smooth pursuit hardly depends on the lighting conditions. Vision Res 46(6–7):1145–1154
Kerzel D, Souto D, Ziegler NE (2008) Effects of attention shifts to stationary objects during steady-state smooth pursuit eye movements. Vision Res 48(7):958–969
Khurana B, Kowler E (1987) Shared attentional control of smooth eye movement and perception. Vision Res 27(9):1603–1618
Kingstone A, Pratt J (1999) Inhibition of return is composed of attentional and oculomotor processes. Percept Psychophys 61(6):1046–1054
Klein R, MacInnes JW (1999) Inhibition of return is a foraging facilitator in visual search. Psychol Sci 10(4):346–352
Klier EM, Wang H, Crawford JD (2001) The superior colliculus encodes gaze commands in retinal coordinates. Nat Neurosci 4(6):627–632
Krauzlis RJ, Miles FA (1996) Initiation of saccades during fixation or pursuit: evidence in humans for a single mechanism. J Neurophysiol 76(6):4175–4179
Madelain L, Krauzlis RJ, Wallman J (2005) Spatial deployment of attention influences both saccadic and pursuit tracking. Vision Res 45(20):2685–2703
Maylor EA, Hockey R (1985) Inhibitory component of externally controlled covert orienting in visual space. J Exp Psychol Hum Percept Perform 11(6):777–787
Muller HJ, von Muhlenen A (1996) Attentional tracking and inhibition of return in dynamic displays. Percept Psychophys 58(2):224–249
Nijhawan R (2002) Neural delays, visual motion and the flash-lag effect. Trends Cogn Sci 6(9):387
Posner MI, Cohen Y (1984) Components of visual orienting. In: Bouma H, Bowhuis D (eds) Attention and performance X. Erlbaum, Hillsdale, pp 531–556
Pouget A, Snyder LH (2000) Computational approaches to sensorimotor transformations. Nat Neurosci 3(Suppl):1192–1198
Pratt J, McAuliffe J (1999) Examining the effect of practice on inhibition of return in static displays. Percept Psychophys 61(4):756–765
Reuter-Lorenz PA, Jha AP, Rosenquist JN (1996) What is inhibited in inhibition of return? J Exp Psychol Hum Percept Perform 22(2):367–378
Riggio L, Kirsner K (1997) The relationship between central cues and peripheral cues in covert visual orientation. Percept Psychophys 59(6):885–899
Ro T, Rafal RD (1999) Components of reflexive visual orienting to moving objects. Percept Psychophys 61(5):826–836
Sapir A, Soroker N, Berger A, Henik A (1999) Inhibition of return in spatial attention: direct evidence for collicular generation. Nat Neurosci 2(12):1053–1054
Sapir A, Hayes A, Henik A, Danziger S, Rafal R (2004) Parietal lobe lesions disrupt saccadic remapping of inhibitory location tagging. J Cogn Neurosci 16(4):503–509
Schlag-Rey M, Schlag J, Dassonville P (1992) How the frontal eye field can impose a saccade goal on superior colliculus neurons. J Neurophysiol 67(4):1003–1005
Schutz AC, Delipetkos E, Braun DI, Kerzel D, Gegenfurtner KR (2007) Temporal contrast sensitivity during smooth pursuit eye movements. J Vis 7(13):3.1–15
Sumner P, Nachev P, Vora N, Husain M, Kennard C (2004) Distinct cortical and collicular mechanisms of inhibition of return revealed with S cone stimuli. Curr Biol 14(24):2259–2263
Taylor TL, Klein RM (2000) Visual and motor effects in inhibition of return. J Exp Psychol Hum Percept Perform 26(5):1639–1656
Theeuwes J (1991) Exogenous and endogenous control of attention: the effect of visual onsets and offsets. Percept Psychophys 49(1):83–90
Tipper C, Kingstone A (2005) Is inhibition of return a reflexive effect? Cognition 97(3):B55–62
Tipper SP, Driver J, Weaver B (1991) Object-centred inhibition of return of visual attention. Q J Exp Psychol A Hum Exp Psychol 43(2):289–298
Tipper SP, Weaver B, Jerreat LM, Burak AL (1994) Object-based and environment-based inhibition of return of visual attention. J Exp Psychol Hum Percept Perform 20(3):478–499
Weaver B, Lupianez J, Watson FL (1998) The effects of practice on object-based, location-based, and static-display inhibition of return. Percept Psychophys 60(6):993–1003
Acknowledgments
We would like to thank Sabine Born, Jeremy Fix and two anonymous reviewers for their helpful comments. We specially thank all the subjects for their tremendous patience. D. K. and D. S. were supported by grant PDFM1-114417 of the Swiss National Science Foundation.
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Souto, D., Kerzel, D. Involuntary cueing effects during smooth pursuit: facilitation and inhibition of return in oculocentric coordinates. Exp Brain Res 192, 25–31 (2009). https://doi.org/10.1007/s00221-008-1555-x
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DOI: https://doi.org/10.1007/s00221-008-1555-x