Experimental Brain Research

, Volume 103, Issue 2, pp 294–310 | Cite as

Independent contributions of the orienting of attention, fixation offset and bilateral stimulation on human saccadic latencies

  • R. Walker
  • R. W. Kentridge
  • J. M. Findlay
Original Paper

Abstract

In a series of experiments we examined the effects of the endogenous orienting of visual attention on human saccade latency. Three separate manipulations were performed: the orienting of visual attention, the prior offset of fixation (gap paradigm) and the bilateral presentation of saccade targets. Each of these manipulations was shown to make an independent contribution to saccade latency. In experiments 1 and 2 subjects were instructed to orient their attention covertly to a location by a verbal pre-cue; targets could appear in the attended hemifield (valid) or in the non-attended hemifield (invalid) together with a no-instruction (neutral) condition. Saccades were made under fixation gap and overlap conditions, to either single targets or two bilaterally presented targets which appeared at equal and opposite eccentricities in both hemifields. The results showed a large increase (cost) of saccade latency to invalid targets and a small non-significant decrease (benefit) of saccade latency to valid targets. The cost associated with invalid targets replicates the “meridian crossing effect” shown in manual reaction time experiments and is consistent with the hemifield inhibition and premotor models of attentional orienting. The use of a “gap” procedure produced a generalised facilitation of saccade latency, which was not modified by the prior orienting of visual attention. The magnitude of the gap effect was similar for saccades made to attended and non-attended stimulis. This suggests that the gap effect may be due to ocular motor disengagement, or a warning signal effect, rather than to the prior disengagement of visual attention. When two targets were presented simultaneously, one in each hemifield, saccade latency was slowed compared with the single target condition. The magnitude of this slowing was unaffected by the prior orienting of visual attention or by the fixation condition. The slowing was examined in more detail in experiment 3, by presenting targets with brief offset delays. The latency increase was maximal if the two targets were presented simultaneously and decreased if the distractor appeared at short intervals (20–80 ms) before or after the saccade target onset. If the non-attended stimulus was presented at greater intervals (160, 240 ms) before the saccade target, then a facilitation effect was observed. This demonstrates that the onset of a distractor in the non-attended hemifield can have both an inhibitory and a facilitatory effect on a saccade production.

Key words

Eye movements Saccade Attention Gap effect Human 

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References

  1. Abrams RA, Jonides J (1988) Programming saccadic eye movements. J Exp Psychol Hum Percept Perform 14(3):428–443Google Scholar
  2. Allport DA (1993) Attention and control: have we been asking the wrong questions? A critical review of twenty-five years. In: Meyer DE, Kornblum S (eds) Attention and performance XIV. MIT Press, Cambridge Mass. pp 183–218Google Scholar
  3. Andersen RA, Essick GK, Siegel RM (1987) Neurons of area 7 activated by both visual stimuli and oculomotor behaviour. Exp Brain Res 67:316–322Google Scholar
  4. Aslin RN, Shea SL (1987) The amplitude and angle of saccades to double-step target displacements. Vision Res 27(11):1925–1942Google Scholar
  5. Becker W (1989) Metrics. In: Wurtz RH, Goldberg ME (eds) The neurobiology of saccadic eye movements. Elsevier Science, OxfordGoogle Scholar
  6. Becker W, Jürgens R (1979) An analysis of the saccadic system by means of double-step stimuli. Vision Res 19:967–983CrossRefPubMedGoogle Scholar
  7. Braun D, Breitmeyer BG (1990) Effects of reappearance of fixated and attended stimuli upon saccadic reaction time. Exp Brain Res 81:318–324Google Scholar
  8. Crawford TJ, Müller HJ (1992) Spatial and temporal effects of spatial attention on human saccadic eye movements. Vision Res 32(2):293–304Google Scholar
  9. Eriksen CW (1990) Attentional search of the visual field. In: Brogan D (ed) Visual search. Taylor and Francis, LondonGoogle Scholar
  10. Eriksen CW, Hoffman JE (1972) Some characteristics of selective attention in visual perception determined by vocal reaction time. Percept Psychophys 11(2):169–171Google Scholar
  11. Findlay JM (1983) Visual information processing for saccadic eye movements. In: Hein A, Jeannerod M (eds) Spatially oriented behavior. Springer, Berlin Heidelberg New York, pp 281–303Google Scholar
  12. Findlay JM (1987) Visual computation and saccadic eye movements. Spat Vis 2:175–189Google Scholar
  13. Findlay JM (1992) Programming of stimulus-elicited saccadic eye movements. In: Rayner K (eds) Eye movements and visual cognition. Springer, Berlin Heidelberg New York, pp 8–30Google Scholar
  14. Findlay JM (1993) Does the attention need to be visual? Commentary on B. Fischer and H. Weber. Behav Brain Sci 16:576–577Google Scholar
  15. Findlay JM, Harris LR (1984) Small saccades to double-stepped targets moving in two dimensions. In: Gale AG, Johnson F (eds) Theoretical and applied aspects of eye movement research. Elsevier Science Amsterdam, pp 71–78Google Scholar
  16. Findlay JM, Brogan D, Wenban-Smith MG (1993) The spatial signal for saccadic eye movements emphasises visual boundaries. Percept Psychophys 53(6):633–641Google Scholar
  17. Fischer B (1987) The preparation of visually guided saccades. Rev Physiol Biochem Pharmacol 106:1–35Google Scholar
  18. Fischer B, Boch R (1983) Saccadic eye movements after extremely short reaction times in the monkey. Brain Res 260:21–26Google Scholar
  19. Fischer B, Breitmeyer B (1987) Mechanisms of visual attention revealed by saccadic eye movements. Neuropsychologia 25(1A):73–83CrossRefPubMedGoogle Scholar
  20. Fischer B, Ramsperger E (1984) Human express saccades: extremely short reaction times of goal directed eye movements. Exp Brain Res 57:191–195Google Scholar
  21. Fischer B, Weber H (1993) Express saccades and visual attention. Behav Brain Sci 16:553–610Google Scholar
  22. Heywood S, Churcher J (1980) Structure of the visual array and saccadic latency: implications for oculomotor control. Q J Exp Psychol 32(2):335–341Google Scholar
  23. Honda H, Findlay JM (1992) Saccades to targets in three dimensional space: dependence of saccadic latency on target location. Precept Psychophys 52(2):167–174Google Scholar
  24. Hughes HC, Zimba LD (1985) Spatial maps of directed visual attention. J Exp Psychol Hum Percept Perform 11(4):409–430Google Scholar
  25. Hughes HC, Zimba LD (1987) Natural boundaries for the spatial spread of directed visual attention. Neuropsychologia 25(1A):5–18Google Scholar
  26. Infante C, Leiva J (1986) Simultaneous unitary neuronal activity in both superior colliculi and its relation to eye movements in the cat. Brain Res 381:390–392Google Scholar
  27. Jonides J, Mack R (1984) On the cost and benefit of cost and benefit. Psychol Bull 96:29–44Google Scholar
  28. Jüttner M, Wolf M (1992) Occurrence of human express saccades depends on stimulus uncertainty and stimulus sequence. Exp Brain Res 89:678–681Google Scholar
  29. Kingstone A, Klein RM (1993a) What are human express saccades? Percept Psychophys 54:260–273Google Scholar
  30. Kingstone A, Klein RM (1993b) Visual offsets facilitate saccadic latency: does predisengagement of visuospatial attention mediate this gap effect? J Exp Psychol Hum Percept Perform 19:(6) 1251–1265CrossRefPubMedGoogle Scholar
  31. Klein R (1980) Does oculomotor readiness mediate cognitive control of visual attention? In: Nickerson RS (ed) Attention and performance VIII. Erlbaum Hillsdale, N.J. pp 259–276Google Scholar
  32. Klein R, Kingstone A, Pontefract A (1992) Orienting of visual attention. In: Rayner K (ed) Eye movements and visual cognition: scene perception and reading. Springer, Berlin Heidelberg New YorkGoogle Scholar
  33. Lévy-Schoen A, Blanc-Garin J (1974) On oculomotor programming and perception. Brain Res 71:443–450PubMedGoogle Scholar
  34. Lynch JC, McLaren JW (1989) Deficits of visual attention and saccadic eye movements after lesions of parietooccipital cortex in monkeys. J Neurophysiol 61(1):74–90Google Scholar
  35. Lynch JC, Graybiel AM, Lobeck LJ (1985) The differential projection of two cytoarchitectonic subregions of the inferior parietal lobule of macaque upon the deep layers of the superior colliculus. J Comp Neurol 235:241–254Google Scholar
  36. Massone LLE (1993) A velocity-based model for control of ocular accades. Department of Physiology, Department of Electrical Engineering and Computer Science, Northwestern University, 303 E. Chicago Avenue, Chicago Ill. 60611, USAGoogle Scholar
  37. McIlwain JT (1986) Point images in the visual system: new interest in an old idea. Trends Neurosci 9(8):354–458Google Scholar
  38. Michard A, Têtard C, Lévy-Schoen A (1974) Attente du signal et temps de réaction oculomoteur. L'Année Psychol 74:387–402Google Scholar
  39. Munoz DP, Wurtz RH (1992) Role of the rostral superior colliculus in active visual fixation and execution of express saccades. J Neurophysiol 67(4):1000–1002Google Scholar
  40. Munoz DP, Pelisson D, Guitton D (1991) Movement of neural activity on the superior colliculus motor map during gaze shifts. Science 251(4999):1358–1360Google Scholar
  41. Ottes FP, Van Gisbergen JAM, Eggermont JJ (1984) Metrics of saccade responses to visual double stimuli: two different modes. Vision Res 24:1169–1179Google Scholar
  42. Posner MI (1980) Orienting of attention. Q J Exp Psychol 32:3–25PubMedGoogle Scholar
  43. Posner MI, Nisssen JM, Ogden WC (1978) Attended and unattended processing modes: the role of set for spatial locations. In: Pick HL, Saltzman BJ (eds) Modes of perceiving and processing information. Erlbaum Hillsdale, N.J.Google Scholar
  44. Posner MI, Walker JA, Friedrich FJ, Rafal RD (1984) Effects of parietal injury on covert orienting of attention. J Neurosci 4(7): 1863–1874Google Scholar
  45. Remington RW (1980) Attention and saccadic eye movements. J Exp Psychol Hum Percept Perform 6:726–744Google Scholar
  46. Reulen JPH, Marcus JT, Koops D, Fries FR de, Tiesinger G, Boshuizen K, Bos JE (1988) Precise recording of eye movements: the IRIS technique. Med Biol Eng Comp 26(1):20–26Google Scholar
  47. Reuter-Lorenz PA, Fendrich R (1992) Oculomotor readiness and covert orienting: differences between central and peripheral precues. Percept Psychophys 52(3):336–344Google Scholar
  48. Reuter-Lorenz PA, Hughes HC, Fendrich R (1991) The reduction of saccadic latency by prior offset of the fixation point: an analysis of the gap effect. Percept Psychophys 49(2):167–175Google Scholar
  49. Rizzolatti G, Camarda R (1987) Neural circuits for spatial attention and unilateral neglect. In: Jeannerod M (ed) Neurophysiological and neuropsychological aspects of spatial neglect. Elsevier Science North-Holland, Amsterdam, pp 151–182Google Scholar
  50. Rizzolatti G, Camarda R, Grupp LA, Pisa M (1974) Inhibitory effects of remote visual stimuli on visual responses of cat superior colliculus: spatial and temporal factors. J Neurophysiol 37:1262–1275Google Scholar
  51. Rizzolatti G, Riggio L, Dascola I, Umiltá C (1987) Reorienting attention across the horizontal and vertical meridians: evidence in favour of a premotor theory of attention. Neuropsychologia 25(1A):31–40Google Scholar
  52. Robinson DA (1972) Eye movements evoked by collicular stimulation in the alert monkey. Vision Res 12:1795–1808CrossRefPubMedGoogle Scholar
  53. Ross LE, Ross SM (1980) Saccade latency and warning signals: effects of auditory and visual stimulus onset and offset. Percept Psychophys 29(5):429–437Google Scholar
  54. Ross SM, Ross LE (1981) Saccade latency and warning signals: effects of auditory and visual stimulus onset and offset. Percept Psychophys 29:429–437Google Scholar
  55. Saslow MG (1967) Effects of components of displacement-step stimuli upon latency for saccadic eye movement. J Opt Soc Am 57(8):1024–1029PubMedGoogle Scholar
  56. Schiller PH, Sandell JH, Maunsell JHR (1987) The effect of frontal eye field and superior colliculus lesions on saccadic latencies in the rhesus monkey. J Neurophysiol 57:1033–1049Google Scholar
  57. Sheliga BM, Riggio I, Rizzolatti G (1994) Orienting attention and eye movements. Exp Brain Res 98:507–522Google Scholar
  58. Shepherd M, Findlay JM, Hockey RJ (1986) The relationship between eye movements and spatial attention. Q J Exp Psychol 38:475–491Google Scholar
  59. Sparks DL, Hartwich-Young R (1989) The deep layers of the superior colliculus. In: Wurtz RH, Goldberg ME (eds) The neurobiology of saccadic eye movements. Elsevier Science, Oxford, pp 213–255Google Scholar
  60. Tam WJ, Stelmach LB (1993) Viewing behaviour: ocular and attentional disengagement. Percept Psychophys 54:211–222PubMedGoogle Scholar
  61. Tassinari G, Aglioti S, Chelazzi L, Marzi CA, Berlucchi G (1987) Distribution in the visual field of the costs of voluntarily allocated attention and of the inhibitory after-effects of covert orienting. Neuropsychologia 25:55–71CrossRefPubMedGoogle Scholar
  62. Umiltá C, Riggio L, Dascola I, Rizzolatti G (1991) Differential effects of central and peripheral cues on the reorienting of spatial attention. Eur J Cognitive Psychol 3(2):247–267Google Scholar
  63. Van Gisbergen JAM, Van Opstal JJ, Tax AAM (1987) Collicular ensemble coding of saccades based on vector stimulation. Neuroscience 21:541–555Google Scholar
  64. Van Opstal JJ, Van Gisbergen JAM (1989) A nonlinear model for collicular spatial interactions underlying the metrical properties of electrically elicited saccades. Biol Cybern 60:171–183Google Scholar
  65. Walker R (1992) Visual attention with implications for unilateral spatial neglect. Ph. D. Thesis, University of DurhamGoogle Scholar
  66. Walker R, Findlay JM, Young AW, Welch J (1991) Disentangling neglect and hemianopia. Neuropsychologia 29(10):1019–1027Google Scholar
  67. Wenban-Smith MG, Findlay JM (1991) Express saccades: Is there a separate population in humans? Exp Brain Res 87:218–222Google Scholar
  68. Yin TCT, Mountcastle VB (1977) Visual input to the visuomotor mechanisms of the monkey's parietal lobe. Science 197:1381–1383Google Scholar

Copyright information

© Springer-Verlag 1995

Authors and Affiliations

  • R. Walker
    • 1
  • R. W. Kentridge
    • 1
  • J. M. Findlay
    • 1
  1. 1.Department of PsychologyUniversity of DurhamDurhamUK

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