Skip to main content
Log in

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

  • Original Article
  • Published:
Psychological Research Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Notes

  1. Some authors reported that, in video-based eye-tracking systems, changes in pupil size can influence the computation of eye-gaze direction, leading to potential artefactual results (e.g., Choe, Blake, & Lee, 2016; Nyström, Hooge, & Andersson, 2016). However, Gautier, Bedell, Siderov and Waugh (2016; Appendix C)—who recorded pupil size and microsaccades through an EyeLink 1000—concluded that pupil size is unlikely to affect microsaccade detection.

References

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Betta, E., Galfano, G., & Turatto, M. (2007). Microsaccadic response during inhibition of return in a target-target paradigm. Vision Research, 47, 428–436.

    Article  PubMed  Google Scholar 

  • Betta, E., & Turatto, M. (2006). Are you ready? I can tell by looking at your microsaccades. Neuroreport, 17, 1001–1004.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Collewijn, H., & Kowler, E. (2008). The significance of microsaccades for vision and oculomotor control. Journal of Vision, 8, 1–21.

    Article  PubMed  Google Scholar 

  • Corneil, B. D., & Munoz, D. P. (2014). Overt responses during covert orienting. Neuron, 82, 1230–1243.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Engbert, R., & Kliegl, R. (2003). Microsaccades uncover the orientation of covert attention. Vision Research, 43, 1035–1045.

    Article  PubMed  Google Scholar 

  • Engbert, R., & Kliegl, R. (2004). Microsaccades keep the eyes’ balance during fixation. Psychological Science, 15, 431–436.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Everling, S., & Fischer, B. (1998). The antisaccade: A review of basic research and clinical findings. Neuropsychologia, 36, 885–899.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Gautier, J., Bedell, H. E., Siderov, J., & Waugh, S. J. (2016). Monocular microsaccades are visual-task related. Journal of Vision, 16, 1–16.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hafed, Z. M., Goffart, L., & Krauzlis, R. J. (2009). A neural mechanism for microsaccade generation in the primate superior colliculus. Science, 323, 940–943.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Kahneman, D., & Beatty, J. (1966). Pupil diameter and load on memory. Science, 154, 1583–1585.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Ko, H.-K., Poletti, M., & Rucci, M. (2010). Microsaccades precisely relocate gaze in a high visual acuity task. Nature Neuroscience, 13, 1549–1553.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lange, E. B., Zweck, F., & Sinn, P. (2017). Microsaccade-rate indicates absorption by music listening. Consciousness and Cognition, 55, 59–78.

    Article  PubMed  Google Scholar 

  • Lisi, M., Bonato, M., & Zorzi, M. (2015). Pupil dilation reveals top-down attentional load during spatial monitoring. Biological Psychology, 112, 39–45.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Martinez-Conde, S., Macknik, S. L., Troncoso, X. G., & Dyar, T. A. (2006). Microsaccades counteract fading during fixation. Neuron, 49, 297–305.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Miyake, A., & Shah, P. (Eds.). (1999). Models of working memory: Mechanisms of active maintenance and executive control. Cambridge: Cambridge University Press.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Nyström, M., Hooge, I., & Andersson, R. (2016). Pupil size influences the eye-tracker signal during saccades. Vision Research, 121, 95–103.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Pastukhov, A., & Braun, J. (2010). Rare but precious: Microsaccades are highly informative about attentional allocation. Vision Research, 50, 1173–1184.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Piquado, T., Isaacowitz, D., & Wingfield, A. (2010). Pupillometry as a measure of cognitive effort in younger and older adults. Psychophysiology, 47, 560–569.

    Article  PubMed  PubMed Central  Google Scholar 

  • Poletti, M., & Rucci, M. (2016). A compact field guide to the study of microsaccades: Challenges and functions. Vision Research, 118, 83–97.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Richer, F., & Beatty, J. (1985). Pupillary dilations in movement preparation and execution. Psychophysiology, 22, 204–207.

    Article  PubMed  Google Scholar 

  • Rolfs, M. (2009). Microsaccades: Small steps on a long way. Vision Research, 49, 2415–2441.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Rolfs, M., Kliegl, R., & Engbert, R. (2008). Toward a model of microsaccade generation: The case of microsaccadic inhibition. Journal of Vision, 8, 1–23.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Sirois, S., & Brisson, J. (2014). Pupillometry. Interdisciplinary Reviews: Cognitive Science, 5, 679–692.

    Google Scholar 

  • Theeuwes, J., Olivers, C. N., & Chizk, C. L. (2005). Remembering a location makes the eyes curve away. Psychological Science, 16, 196–199.

    Article  PubMed  Google Scholar 

  • Unsworth, N., & Robison, M. K. (2018). Tracking working memory maintenance with pupillometry. Attention, Perception, & Psychophysics, 80, 461–484.

    Article  Google Scholar 

  • Valsecchi, M., Betta, E., & Turatto, M. (2007). Visual oddballs induce prolonged microsaccadic inhibition. Experimental Brain Research, 177, 196–208.

    Article  PubMed  Google Scholar 

  • Valsecchi, M., & Turatto, M. (2009). Microsaccadic responses in a bimodal oddball task. Psychological Research Psychologische Forschung, 73, 23–33.

    Article  PubMed  Google Scholar 

  • 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.

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Watanabe, M., Matsuo, Y., Zha, L., Munoz, D. P., & Kobayashi, Y. (2013). Fixational saccades reflect volitional action preparation. Journal of Neurophysiology, 110, 522–535.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou, X., & Constantinidis, C. (2017). Fixation target representation in prefrontal cortex during the antisaccade task. Journal of Neurophysiology, 117, 2152–2162.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zuber, B. L., Stark, L., & Cook, G. (1965). Microsaccades and the velocity-amplitude relationship for saccadic eye movements. Science, 150, 1459–1460.

    Article  PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mario Dalmaso.

Ethics declarations

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.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dalmaso, M., Castelli, L. & Galfano, G. Microsaccadic rate and pupil size dynamics in pro-/anti-saccade preparation: the impact of intermixed vs. blocked trial administration. Psychological Research 84, 1320–1332 (2020). https://doi.org/10.1007/s00426-018-01141-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00426-018-01141-7

Navigation