Experimental Brain Research

, 169:369

Shortening and prolongation of saccade latencies following microsaccades

Research Article

Abstract

When the eyes fixate at a point in a visual scene, small saccades rapidly shift the image on the retina. The effect of these microsaccades on the latency of subsequent large-scale saccades may be twofold. First, microsaccades are associated with an enhancement of visual perception. Their occurrence during saccade target perception could, thus, decrease saccade latencies. Second, microsaccades are likely to indicate activity in fixation-related oculomotor neurons. These represent competitors to saccade-related cells in the interplay of gaze holding and shifting. Consequently, an increase in saccade latencies would be expected after microsaccades. Here, we present evidence for both aspects of microsaccadic impact on saccade latency. In a delayed response task, participants made saccades to visible or memorized targets. First, microsaccade occurrence up to 50 ms before target disappearance correlated with 18 ms (or 8%) faster saccades to memorized targets. Second, if microsaccades occurred shortly (i.e., <150 ms) before a saccade was required, mean saccadic reaction time in visual and memory trials was increased by about 40 ms (or 16%). Hence, microsaccades can have opposite consequences for saccade latencies, pointing at a differential role of these fixational eye movements in the preparation of saccade motor programs.

Keywords

Fixational eye movements Memory-guided saccades Visually guided saccades 

References

  1. Bair W, O’Keefe LP (1998) The influence of fixational eye movements on the response of neurons in area MT of the macaque. Vis Neurosci 15:779–786PubMedCrossRefGoogle Scholar
  2. Brainard DH (1997) The Psychophysics Toolbox. Spat Vis 10:433–436PubMedCrossRefGoogle Scholar
  3. Bruce CJ, Friedman HR, Kraus MS, Stanton GB (2004) The primate frontal eye field. In: Chalupa LM, Werner JS (eds) The visual neurosciences, vol 2. MIT Press, Cambridge, MA, pp 1428–1448Google Scholar
  4. Cornelissen FW, Peters EM, Palmer J (2002) The Eyelink Toolbox: Eye tracking with MATLAB and the Psychophysics Toolbox. Behav Res Methods Instrum Comput 34:613–617PubMedGoogle Scholar
  5. Ditchburn RW (1980) The function of small saccades. Vision Res 20:271–272PubMedCrossRefGoogle Scholar
  6. Ditchburn RW, Ginsborg BL (1953) Involuntary eye movements during fixation. J Physiol 119:1–17PubMedGoogle Scholar
  7. Engbert R, Kliegl R (2003) Microsaccades uncover the orientation of covert attention. Vision Res 43:1035–1045PubMedCrossRefGoogle Scholar
  8. Engbert R (2005) Microsaccades: a microcosm for research on oculomotor control, attention, and visual perception. Prog Brain Res (in press)Google Scholar
  9. Friedman HR, Burman DD, Russo GS, Dias EC, Stanton GB, Shi D, Bruce CJ (1997) Neuronal activity in primate frontal eye field during memory-guided saccades. Abstr Soc Neurosci 24:522Google Scholar
  10. Galfano G, Betta E, Turatto M (2004) Inhibition of return in microsaccades. Exp Brain Res 159:400–404PubMedCrossRefGoogle Scholar
  11. Gandhi NJ, Keller EL (1999) Comparison of saccades perturbed by stimulation of the rostral superior colliculus, the caudal superior colliculus, and the omnipause neuron region. J Neurophysiol 82:3236–3253PubMedGoogle Scholar
  12. Gerrits HJM, Vendrik AJH (1974) The influence of stimulus movements on perception in parafoveal stabilized vision. Vision Res 14:175–180PubMedCrossRefGoogle Scholar
  13. Krauskopf J, Cornsweet TN, Riggs LA (1960) Analysis of eye movements during monocular and binocular fixation. J Opt Soc Am 50:572–578PubMedGoogle Scholar
  14. Krauzlis RJ, Basso MA, Wurtz RH (1997) Shared motor error for multiple eye movements. Science 276:1693–1695PubMedCrossRefGoogle Scholar
  15. Laubrock J, Engbert R, Kliegl R (2005) Microsaccade dynamics during covert attention. Vision Res 45:721–730PubMedCrossRefGoogle Scholar
  16. Leopold DA, Logothetis NK (1998) Microsaccades differentially modulate neural activity in the striate and extrastriate visual cortex. Exp Brain Res 123:341–345PubMedCrossRefGoogle Scholar
  17. Lord MP (1951) Measurement of binocular eye movements of subjects in the sitting position. Br J Ophthalmol 35:21–30PubMedCrossRefGoogle Scholar
  18. Martinez-Conde S, Macknik SL, Hubel DH (2000) Microsaccadic eye movements and firing of single cells in the striate cortex of macaque monkeys. Nat Neurosci 3:251–258PubMedCrossRefGoogle Scholar
  19. Martinez-Conde S, Macknik SL, Hubel DH (2002) The function of bursts of spikes during visual fixation in the awake primate lateral geniculate nucleus and primary visual cortex. Proc Natl Acad Sci USA 99:13920–13925PubMedCrossRefGoogle Scholar
  20. Martinez-Conde S, Macknik SL, Hubel DH (2004) The role of fixational eye movements in visual perception. Nat Rev Neurosci 5:229–240PubMedCrossRefGoogle Scholar
  21. Munoz DP, Fecteau JH (2002) Vying for dominance: Dynamic interactions control visual fixation and saccadic initiation in the superior colliculus. Prog Brain Res 140:3–19PubMedCrossRefGoogle Scholar
  22. Munoz DP, Guitton D (1991) Control of orienting gaze shifts by the tectoreticulospinal system in the head-free cat II. Sustained discharges during motor preparation and fixation. J Neurophysiol 66:1624–1641PubMedGoogle Scholar
  23. Munoz DP, Istvan PJ (1998) Lateral inhibitory interactions in the intermediate layers of the monkey superior colliculus. J Neurophysiol 79:1193–1209PubMedGoogle Scholar
  24. Munoz DP, Wurtz RH (1993a) Fixation cells in monkey superior colliculus. I. Characteristics of cell discharge. J Neurophysiol 70:559–575PubMedGoogle Scholar
  25. Munoz DP, Wurtz RH (1993b) Fixation cells in monkey superior colliculus. II. Reversible activation and deactivation. J Neurophysiol 70:576–589PubMedGoogle Scholar
  26. Munoz DP, Wurtz RH (1995a) Saccade-related activity in monkey superior colliculus. I. Characteristics of burst and buildup cells. J Neurophysiol 73:2313–2333PubMedGoogle Scholar
  27. Munoz DP, Wurtz RH (1995b) Saccade-related activity in monkey superior colliculus. II. Spread of activity during saccades. J Neurophysiol 73:2334–2348PubMedGoogle Scholar
  28. Munoz DP, Dorris MC, Paré M, Everling S (2000) On your mark get set: Brainstem circuitry underlying saccadic initiation. Can J Physiol Pharmacol 78:934–944PubMedCrossRefGoogle Scholar
  29. Pelli DG (1997) The VideoToolbox software for visual psychophysics: Transforming numbers into movies. Spat Vis 10:437–442PubMedCrossRefGoogle Scholar
  30. Ratliff F, Riggs LA (1950) Involuntary motions of the eye during monocular fixation. J Exp Psychol 40:687–701PubMedCrossRefGoogle Scholar
  31. Robinson DA (1972) Eye movements evoked by collicular stimulation in the alert monkey. Vision Res 12:1795–1808PubMedCrossRefGoogle Scholar
  32. Rolfs M, Engbert R, Kliegl R (2004) Microsaccade orientation supports attentional enhancement opposite a peripheral cue. Psychol Sci 15:705–707PubMedCrossRefGoogle Scholar
  33. Rolfs M, Engbert R, Kliegl R (2005) Crossmodal coupling of oculomotor control and spatial attention in vision and audition. Exp Brain Res 166:427–439PubMedCrossRefGoogle Scholar
  34. Schall JD, Morel A, King DJ, Bullier J (1995) Topography of visual cortex connections with frontal eye field in macaque: Convergence and segregation of processing streams. J Neurosci 15:4464–4487PubMedGoogle Scholar
  35. Scudder CA, Kaneko CRS, Fuchs AF (2002) The brainstem burst generator for saccadic eye movements: A modern synthesis. Exp Brain Res 142:439–462PubMedCrossRefGoogle Scholar
  36. Snodderly DM, Kagan I, Gur M (2001) Selective activation of visual cortex neurons by fixational eye movements: Implications for neural coding. Vis Neurosci 18:259–277PubMedCrossRefGoogle Scholar
  37. Sparks DL (2002) The brainstem control of saccadic eye movements. Nat Rev Neurosci 3:952–964PubMedCrossRefGoogle Scholar
  38. Sparks DL, Holland R, Guthrie BL (1976) Size and distribution of movement fields in the monkey superior colliculus. Brain Res 113:21–34PubMedCrossRefGoogle Scholar
  39. Supèr H, van der Togt C, Spekreijse H, Lamme VAF (2004) Correspondence of presaccadic activity in the monkey primary visual cortex with saccadic eye movements. Proc Natl Acad Sci USA 101:3230–3235PubMedCrossRefGoogle Scholar
  40. Wurtz RH, Goldberg ME (1972) Activity of superior colliculus in behaving monkey. III. Cells discharging before eye movements. J Neurophysiol 35:575–586PubMedGoogle Scholar
  41. Zuber BL, Stark L, Cook G (1965) Microsaccades and the velocity–amplitude relationship for saccadic eye movements. Science 150:1459–1460PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Martin Rolfs
    • 1
  • Jochen Laubrock
    • 1
  • Reinhold Kliegl
    • 1
  1. 1.Department of Cognitive PsychologyUniversity of PotsdamPotsdamGermany

Personalised recommendations