Advertisement

Microsaccadic rate and pupil size dynamics in pro-/anti-saccade preparation: the impact of intermixed vs. blocked trial administration

  • Mario Dalmaso
  • Luigi Castelli
  • Giovanni Galfano
Original Article
  • 47 Downloads

Abstract

Prolonged fixation can lead to the generation of tiny and fast eye movements called microsaccades, whose dynamics can be associated with higher cognitive mechanisms. Saccade preparation is also reflected in microsaccadic activity, but the few studies on this topic provided mixed results. For instance, fewer microsaccades have been observed when participants were asked to prepare for an anti-saccade (i.e., a saccade in the opposite direction to the target) as compared to a pro-saccade (i.e., a saccade executed towards a target), but null results have also been reported. In the attempt to shed new light on this topic, two experiments were carried out in which the context of presentation of pro- and anti-saccade trials was manipulated. Pupil size was also recorded, as a further index of cognitive load. In Experiment 1, participants were asked to prepare and perform pro- and anti-saccades in response to a peripheral target, according to a central instruction cue provided at the beginning of each trial (intermixed condition). In Experiment 2, the same task was employed, but pro- and anti-saccade trials were delivered in two distinct blocks (blocked condition). In both experiments, greater saccadic latencies and lower accuracy emerged for anti- than for pro-saccades. However, in the intermixed condition, a lower microsaccadic rate and a greater pupil size emerged when participants prepared for anti- rather than pro-saccades, whereas these differences disappeared in the blocked condition. These results suggest that contextual factors may play a key role in shaping oculomotor dynamics linked to saccade preparation.

Notes

Acknowledgements

This work was funded by the Italian Ministry of Education, University, and Research (Futuro in Ricerca 2012, Grant number RBFR12F0BD to Giovanni Galfano) and by the University of Padova (Bando Giovani Ricercatori 2015 “Assegno Senior”, Grant number GRIC15QDDH to Mario Dalmaso). The authors are grateful to Ralf Engbert for his valuable suggestions on data analysis, to Daniela Toffoletto for her help during data collection, and to two anonymous reviewers for their advice and constructive criticisms on a previous version of the paper.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the studies.

References

  1. Albares, M., Criaud, M., Wardak, C., Nguyen, S. C. T., Ben Hamed, S., & Boulinguez, P. (2011). Attention to baseline: Does orienting visuospatial attention really facilitate target detection? Journal of Neurophysiology, 106, 809–816.CrossRefGoogle Scholar
  2. Antoniades, C., Ettinger, U., Gaymard, B., Gilchrist, I., Kristjánsson, A., Kennard, C., et al. (2013). An internationally standardised antisaccade protocol. Vision Research, 84, 1–5.CrossRefGoogle Scholar
  3. Betta, E., Galfano, G., & Turatto, M. (2007). Microsaccadic response during inhibition of return in a target-target paradigm. Vision Research, 47, 428–436.CrossRefGoogle Scholar
  4. Betta, E., & Turatto, M. (2006). Are you ready? I can tell by looking at your microsaccades. Neuroreport, 17, 1001–1004.CrossRefGoogle Scholar
  5. Cherkasova, M. V., Manoach, D. S., Intriligator, J. M., & Barton, J. J. (2002). Antisaccades and task-switching: Interactions in controlled processing. Experimental Brain Research, 144, 528–537.CrossRefGoogle Scholar
  6. Choe, K. W., Blake, R., & Lee, S. H. (2016). Pupil size dynamics during fixation impact the accuracy and precision of video-based gaze estimation. Vision Research, 118, 48–59.CrossRefGoogle Scholar
  7. Collewijn, H., & Kowler, E. (2008). The significance of microsaccades for vision and oculomotor control. Journal of Vision, 8, 1–21.CrossRefGoogle Scholar
  8. Corneil, B. D., & Munoz, D. P. (2014). Overt responses during covert orienting. Neuron, 82, 1230–1243.CrossRefGoogle Scholar
  9. Costela, F. M., Otero-Millan, J., McCamy, M. B., Macknik, S. L., Troncoso, X. G., & Jazi, A. N., et al. (2014). Fixational eye movement correction of blink-induced gaze position errors. PLoS One, 9, e110889.CrossRefGoogle Scholar
  10. Dalmaso, M., Castelli, L., Scatturin, P., & Galfano, G. (2017). Working memory load modulates microsaccadic rate. Journal of Vision, 17, 1–12.  https://doi.org/10.1167/17.3.6.Google Scholar
  11. Engbert, R., & Kliegl, R. (2003). Microsaccades uncover the orientation of covert attention. Vision Research, 43, 1035–1045.CrossRefGoogle Scholar
  12. Engbert, R., & Kliegl, R. (2004). Microsaccades keep the eyes’ balance during fixation. Psychological Science, 15, 431–436.CrossRefGoogle Scholar
  13. Everling, S., Dorris, M. C., Klein, R. M., & Munoz, D. P. (1999). Role of primate superior colliculus in preparation and execution of anti-saccades and pro-saccades. Journal of Neuroscience, 19, 2740–2754.CrossRefGoogle Scholar
  14. Everling, S., & Fischer, B. (1998). The antisaccade: A review of basic research and clinical findings. Neuropsychologia, 36, 885–899.CrossRefGoogle Scholar
  15. Everling, S., & Munoz, D. P. (2000). Neuronal correlates for preparatory set associated with pro-saccades and anti-saccades in the primate frontal eye field. Journal of Neuroscience, 20, 387–400.CrossRefGoogle Scholar
  16. Gao, X., Yan, H., & Sun, H.-J. (2015). Modulation of microsaccade rate by task difficulty revealed through between- and within-trial comparisons. Journal of Vision, 15, 1–15.  https://doi.org/10.1167/15.3.3.Google Scholar
  17. Gautier, J., Bedell, H. E., Siderov, J., & Waugh, S. J. (2016). Monocular microsaccades are visual-task related. Journal of Vision, 16, 1–16.CrossRefGoogle Scholar
  18. Gilbert, S. J., Spengler, S., Simons, J. S., Steele, J. D., Lawrie, S. M., Frith, C. D., et al. (2006). Functional specialization within rostral prefrontal cortex (area 10): A meta-analysis. Journal of Cognitive Neuroscience, 18, 932–948.CrossRefGoogle Scholar
  19. Hafed, Z. M., Chen, C. Y., & Tian, X. (2015). Vision, perception, and attention through the lens of microsaccades: Mechanisms and implications. Frontiers in Systems Neuroscience, 9, 167.CrossRefGoogle Scholar
  20. Hafed, Z. M., Goffart, L., & Krauzlis, R. J. (2009). A neural mechanism for microsaccade generation in the primate superior colliculus. Science, 323, 940–943.CrossRefGoogle Scholar
  21. Hafed, Z. M., & Ignashchenkova, A. (2013). On the dissociation between microsaccade rate and direction after peripheral cues: Microsaccadic inhibition revisited. Journal of Neuroscience, 33, 16220–16235.CrossRefGoogle Scholar
  22. Hermens, F., Zanker, J. M., & Walker, R. (2010). Microsaccades and preparatory set: A comparison between delayed and immediate, exogenous and endogenous pro-and anti-saccades. Experimental Brain Research, 201, 489–498.CrossRefGoogle Scholar
  23. Hyönä, J., Tommola, J., & Alaja, A. M. (1995). Pupil dilation as a measure of processing load in simultaneous interpretation and other language tasks. Quarterly Journal of Experimental Psychology, 48A, 598–612.CrossRefGoogle Scholar
  24. Jainta, S., Vernet, M., Yang, Q., & Kapoula, Z. (2011). The pupil reflects motor preparation for saccades—Even before the eye starts to move. Frontiers in Human Neuroscience, 5, 97.CrossRefGoogle Scholar
  25. Johnston, K., & Everling, S. (2009). Task-relevant output signals are sent from monkey dorsolateral prefrontal cortex to the superior colliculus during a visuospatial working memory task. Journal of Cognitive Neuroscience, 21, 1023–1038.CrossRefGoogle Scholar
  26. Just, M. A., Carpenter, P. A., & Miyake, A. (2003). Neuroindices of cognitive workload: Neuroimaging, pupillometric and event-related potential studies of brain work. Theoretical Issues in Ergonomics Science, 4, 56–88.CrossRefGoogle Scholar
  27. Kahneman, D., & Beatty, J. (1966). Pupil diameter and load on memory. Science, 154, 1583–1585.CrossRefGoogle Scholar
  28. Kliegl, R., Rolfs, M., Laubrock, J., & Engbert, R. (2009). Microsaccadic modulation of response times in spatial attention tasks. Psychological Research Psychologische Forschung, 73, 136–146.CrossRefGoogle Scholar
  29. Klinger, J., Tversky, B., & Hanrahan, P. (2011). Effects of visual and verbal presentation on cognitive load in vigilance, memory, and arithmetic tasks. Psychophysiology, 48, 323–332.CrossRefGoogle Scholar
  30. Ko, H.-K., Poletti, M., & Rucci, M. (2010). Microsaccades precisely relocate gaze in a high visual acuity task. Nature Neuroscience, 13, 1549–1553.CrossRefGoogle Scholar
  31. Krauzlis, R. J., Goffart, L., & Hafed, Z. M. (2017). Neuronal control of fixation and fixational eye movements. Philosophical Transactions of the Royal Society B: Biological Sciences, 372, 20160205.CrossRefGoogle Scholar
  32. Krejtz, K., Duchowski, A. T., Niedzielska, A., Biele, C., & Krejtz, I. (2018). Eye tracking cognitive load using pupil diameter and microsaccades with fixed gaze. PLoS One, 13, e0203629.CrossRefGoogle Scholar
  33. Lange, E. B., Zweck, F., & Sinn, P. (2017). Microsaccade-rate indicates absorption by music listening. Consciousness and Cognition, 55, 59–78.CrossRefGoogle Scholar
  34. Lisi, M., Bonato, M., & Zorzi, M. (2015). Pupil dilation reveals top-down attentional load during spatial monitoring. Biological Psychology, 112, 39–45.CrossRefGoogle Scholar
  35. Martinez-Conde, S., & Macknik, S. L. (2017). Unchanging visions: The effects and limitations of ocular stillness. Philosophical Transactions of the Royal Society B: Biological Sciences, 372, 20160204.CrossRefGoogle Scholar
  36. Martinez-Conde, S., Macknik, S. L., Troncoso, X. G., & Dyar, T. A. (2006). Microsaccades counteract fading during fixation. Neuron, 49, 297–305.CrossRefGoogle Scholar
  37. Martinez-Conde, S., Otero-Millan, J., & Macknik, S. L. (2013). The impact of microsaccades on vision: Towards a unified theory of saccadic function. Nature Reviews Neuroscience, 14, 83–96.CrossRefGoogle Scholar
  38. Mathôt, S., Fabius, J., Van Heusden, E., & Van der Stigchel, S. (2018). Safe and sensible preprocessing and baseline correction of pupil-size data. Behavior Research Methods, 50, 94–106.CrossRefGoogle Scholar
  39. McCamy, M. B., Macknik, S. L., & Martinez-Conde, S. (2014). Different fixational eye movements mediate the prevention and the reversal of visual fading. Journal of Physiology, 592, 4381–4394.CrossRefGoogle Scholar
  40. McCamy, M. B., Otero-Millan, J., Di Stasi, L. L., Macknik, S. L., & Martinez-Conde, S. (2014). Highly informative natural scene regions increase microsaccade production during visual scanning. Journal of Neuroscience, 34, 2956–2966.CrossRefGoogle Scholar
  41. Miyake, A., & Shah, P. (Eds.). (1999). Models of working memory: Mechanisms of active maintenance and executive control. Cambridge: Cambridge University Press.Google Scholar
  42. Munoz, D. P., & Everling, S. (2004). Look away: The anti-saccade task and the voluntary control of eye movement. Nature Reviews Neuroscience, 5, 218–228.CrossRefGoogle Scholar
  43. Nyström, M., Hooge, I., & Andersson, R. (2016). Pupil size influences the eye-tracker signal during saccades. Vision Research, 121, 95–103.CrossRefGoogle Scholar
  44. Otero-Millan, J., Macknik, S. L., Serra, A., Leigh, R. J., & Martinez-Conde, S. (2011). Triggering mechanisms in microsaccade and saccade generation: A novel proposal. Annals of the New York Academy of Sciences, 1233, 107–116.CrossRefGoogle Scholar
  45. Pastukhov, A., & Braun, J. (2010). Rare but precious: Microsaccades are highly informative about attentional allocation. Vision Research, 50, 1173–1184.CrossRefGoogle Scholar
  46. Peel, T. R., Hafed, Z. M., Dash, S., Lomber, S. G., & Corneil, B. D. (2016). A causal role for the cortical frontal eye fields in microsaccade deployment. PLoS Biology, 14, e1002531.CrossRefGoogle Scholar
  47. Pierce, J. E., McCardel, J. B., & McDowell, J. E. (2015). Trial-type probability and task-switching effects on behavioral response characteristics in a mixed saccade task. Experimental Brain Research, 233, 959–969.CrossRefGoogle Scholar
  48. Piquado, T., Isaacowitz, D., & Wingfield, A. (2010). Pupillometry as a measure of cognitive effort in younger and older adults. Psychophysiology, 47, 560–569.CrossRefGoogle Scholar
  49. Poletti, M., & Rucci, M. (2016). A compact field guide to the study of microsaccades: Challenges and functions. Vision Research, 118, 83–97.CrossRefGoogle Scholar
  50. Privitera, C. M., Carney, T., Klein, S., & Aguilar, M. (2014). Analysis of microsaccades and pupil dilation reveals a common decisional origin during visual search. Vision Research, 95, 43–50.CrossRefGoogle Scholar
  51. Richer, F., & Beatty, J. (1985). Pupillary dilations in movement preparation and execution. Psychophysiology, 22, 204–207.CrossRefGoogle Scholar
  52. Rolfs, M. (2009). Microsaccades: Small steps on a long way. Vision Research, 49, 2415–2441.CrossRefGoogle Scholar
  53. Rolfs, M., Engbert, R., & Kliegl, R. (2005). Cross- modal coupling of oculomotor control and spatial attention in vision and audition. Experimental Brain Research, 166, 427–439.CrossRefGoogle Scholar
  54. Rolfs, M., Kliegl, R., & Engbert, R. (2008). Toward a model of microsaccade generation: The case of microsaccadic inhibition. Journal of Vision, 8, 1–23.CrossRefGoogle Scholar
  55. Schaeffer, D. J., Chi, L., Krafft, C. E., Li, Q., Schwarz, N. F., & McDowell, J. E. (2015). Individual differences in working memory moderate the relationship between prosaccade latency and anti- saccade error rate. Psychophysiology, 52, 605–608.CrossRefGoogle Scholar
  56. Shen, K., Bezgin, G., Selvam, R., McIntosh, A. R., & Ryan, J. D. (2016). An anatomical interface between memory and oculomotor systems. Journal of Cognitive Neuroscience, 28, 1772–1783.CrossRefGoogle Scholar
  57. Siegenthaler, E., Costela, F. M., McCamy, M. B., Di Stasi, L. L., Otero-Millan, J., Sonderegger, A., et al. (2014). Task difficulty in mental arithmetic affects microsaccadic rates and magnitudes. European Journal of Neuroscience, 39, 287–294.CrossRefGoogle Scholar
  58. Sirois, S., & Brisson, J. (2014). Pupillometry. Interdisciplinary Reviews: Cognitive Science, 5, 679–692.Google Scholar
  59. Theeuwes, J., Olivers, C. N., & Chizk, C. L. (2005). Remembering a location makes the eyes curve away. Psychological Science, 16, 196–199.CrossRefGoogle Scholar
  60. Unsworth, N., & Robison, M. K. (2018). Tracking working memory maintenance with pupillometry. Attention, Perception, & Psychophysics, 80, 461–484.CrossRefGoogle Scholar
  61. Valsecchi, M., Betta, E., & Turatto, M. (2007). Visual oddballs induce prolonged microsaccadic inhibition. Experimental Brain Research, 177, 196–208.CrossRefGoogle Scholar
  62. Valsecchi, M., & Turatto, M. (2009). Microsaccadic responses in a bimodal oddball task. Psychological Research Psychologische Forschung, 73, 23–33.CrossRefGoogle Scholar
  63. van der Wel, P., & van Steenbergen, H. (2018). Pupil dilation as an index of effort in cognitive control tasks: A review. Psychonomic Bulletin and Review (in press).  https://doi.org/10.3758/s13423-018-1432-y.
  64. Wang, C. A., Blohm, G., Huang, J., Boehnke, S. E., & Munoz, D. P. (2017). Multisensory integration in orienting behavior: Pupil size, microsaccades, and saccades. Biological Psychology, 129, 36–44.CrossRefGoogle Scholar
  65. Wang, C. A., Boehnke, S. E., White, B. J., & Munoz, D. P. (2012). Microstimulation of the monkey superior colliculus induces pupil dilation without evoking saccades. Journal of Neuroscience, 32, 3629–3636.CrossRefGoogle Scholar
  66. Wang, C. A., Brien, D. C., & Munoz, D. P. (2015). Pupil size reveals preparatory processes in the generation of pro-saccades and anti-saccades. European Journal of Neuroscience, 41, 1102–1110.CrossRefGoogle Scholar
  67. Wardak, C., Ramanoël, S., Guipponi, O., Boulinguez, P., & Ben Hamed, S. B. (2012). Proactive inhibitory control varies with task context. European Journal of Neuroscience, 36, 3568–3579.CrossRefGoogle Scholar
  68. Watanabe, M., Matsuo, Y., Zha, L., Munoz, D. P., & Kobayashi, Y. (2013). Fixational saccades reflect volitional action preparation. Journal of Neurophysiology, 110, 522–535.CrossRefGoogle Scholar
  69. Xue, L., Huang, D., Wang, T., Hu, Q., Chai, X., Li, L., et al. (2017). Dynamic modulation of the perceptual load on microsaccades during a selective spatial attention task. Scientific Reports, 7, 16496.CrossRefGoogle Scholar
  70. Zeligman, L., & Zivotofsky, A. Z. (2017). Back to basics: The effects of block vs. interleaved trial administration on pro-and anti-saccade performance. PLoS ONE, 12, e0172485.CrossRefGoogle Scholar
  71. Zhou, X., & Constantinidis, C. (2017). Fixation target representation in prefrontal cortex during the antisaccade task. Journal of Neurophysiology, 117, 2152–2162.CrossRefGoogle Scholar
  72. Zuber, B. L., Stark, L., & Cook, G. (1965). Microsaccades and the velocity-amplitude relationship for saccadic eye movements. Science, 150, 1459–1460.CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Developmental and Social PsychologyUniversity of PadovaPaduaItaly

Personalised recommendations