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Effects of blocked vs. interleaved administration mode on saccade preparatory set revealed using pupillometry

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Abstract

Eye movements have been used extensively to assess information processing and cognitive function. However, significant variability in saccade performance has been observed, which could arise from methodological variations across different studies. For example, prosaccades and antisaccades have been studied using either a blocked or interleaved design, which has a significant influence on error rates and latency. This is problematic as it makes it difficult to compare saccade performance across studies and may limit the ability to use saccades as a behavioural assay to assess neurocognitive function. Thus, the current study examined how administration mode influences saccade related preparatory activity by employing pupil size as a non-invasive proxy for neural activity related to saccade planning and execution. Saccade performance and pupil dynamics were examined in eleven participants as they completed pro- and antisaccades in blocked and interleaved paradigms. Results showed that administration mode significantly modulated saccade performance and preparatory activity. Reaction times were longer for both pro- and antisaccades in the interleaved condition, compared to the blocked condition (p < 0.05). Prosaccade pupil dilations were larger in the interleaved condition (p < 0.05), while antisaccade pupil dilations did not significantly differ between administration modes. Additionally, ROC analysis provided preliminary evidence that pupil size can effectively predict saccade directional errors prior to saccade onset. We propose that task-evoked pupil dilations reflect an increase in preparatory activity for prosaccades and the corresponding cognitive demands associated with interleaved administration mode. Overall, the results highlight the importance that administration mode plays in the design of neurocognitive tasks.

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References

  • Ansari TL, Derakshan N, Richards A (2008) Effects of anxiety on task switching: Evidence from the mixed antisaccade task. Cogn Affect Behav Neurosci 8(3):229–238

    PubMed  Google Scholar 

  • Aston-Jones G, Cohen JD (2005) An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. Annu Rev Neurosci 28:403–450

    CAS  PubMed  Google Scholar 

  • Ayala N, Heath M (2020) Executive dysfunction following a sport-related concussion is independent of task-based symptom burden. J Neurotrauma. https://doi.org/10.1089/neu.2019.6865

    Article  PubMed  Google Scholar 

  • Cherkasova MV, Manoach DS, Intriligator JM, Barton JJ (2002) Antisaccades and task-switching: interactions in controlled processing. Exp Brain Res 144(4):528–537

    PubMed  Google Scholar 

  • Clark JJ (1999) Spatial attention and latencies of saccadic eye movements. Vision Res 39(3):585–602

    CAS  PubMed  Google Scholar 

  • Coe BC, Munoz DP (2017) Mechanisms of saccade suppression revealed in the anti-saccade task. Philos Trans R Soc B: Biol Sci 372(1718):20160192

    Google Scholar 

  • Connolly JD, Goodale MA, Goltz HC, Munoz DP (2005) fMRI activation in the human frontal eye field is correlated with saccadic reaction time. J Neurophysiol 94(1):605–611

    PubMed  Google Scholar 

  • Curtis CE, Connolly JD (2008) Saccade preparation signals in the human frontal and parietal cortices. J Neurophysiol 99(1):133–145

    PubMed  Google Scholar 

  • Dafoe JM, Armstrong IT, Munoz DP (2007) The influence of stimulus direction and eccentricity on pro-and anti-saccades in humans. Exp Brain Res 179(4):563–570

    PubMed  Google Scholar 

  • Dalmaso M, Castelli L, Galfano G (2020) Microsaccadic rate and pupil size dynamics in pro-/anti-saccade preparation: the impact of intermixed vs. blocked trial administration. Psychol Res 84(5):1320–1332

    PubMed  Google Scholar 

  • Derakshan N, Ansari TL, Hansard M, Shoker L, Eysenck MW (2009) Anxiety, inhibition, efficiency, and effectiveness: an investigation using the antisaccade task. Expl psychol 56(1):48

    Google Scholar 

  • DeSimone JC, Weiler J, Aber GS, Heath M (2014) The unidirectional prosaccade switch-cost: correct and error antisaccades differentially influence the planning times for subsequent prosaccades. Vision Res 96:17–24

    PubMed  Google Scholar 

  • DeSouza JF, Menon RS, Everling S (2003) Preparatory set associated with pro-saccades and anti-saccades in humans investigated with event-related FMRI. J Neurophysiol 89:1016–1023 (pmid:12574477)

    PubMed  Google Scholar 

  • Edelman JA, Goldberg ME (2003) Saccade-related activity in the primate superior colliculus depends on the presence of local landmarks at the saccade endpoint. J Neurophysiol 90(3):1728–1736

    PubMed  Google Scholar 

  • Ethridge LE, Brahmbhatt S, Gao Y, Mcdowell JE, Clementz BA (2009) Consider the context: blocked versus interleaved presentation of antisaccade trials. Psychophysiology 46(5):1100–1107

    PubMed  PubMed Central  Google Scholar 

  • Evdokimidis I, Smyrnis N, Constantinidis T, Stefanis N, Avramopoulos D, Paximadis C, Stefanis C (2002) The antisaccade task in a sample of 2006 young men. Exp Brain Res 147(1):45–52

    CAS  PubMed  Google Scholar 

  • Everling S, Munoz DP (2000) Neuronal correlates for preparatory set associated with pro-saccades and anti-saccades in the primate frontal eye field. J Neurosci 20(1):387–400

    CAS  PubMed  PubMed Central  Google Scholar 

  • Everling S, Dorris MC, Munoz DP (1998) Reflex suppression in the anti-saccade task is dependent on prestimulus neural processes. J Neurophysiol 80(3):1584–1589

    CAS  PubMed  Google Scholar 

  • Everling S, Dorris MC, Klein RM, Munoz DP (1999) Role of primate superior colliculus in preparation and execution of anti-saccades and pro-saccades. J Neurosci 19(7):2740–2754

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fischer B, Weber H (1992) Characteristics of “anti” saccades in man. Exp Brain Res 89(2):415–424

    CAS  PubMed  Google Scholar 

  • Ford KA, Goltz HC, Brown MR, Everling S (2005) Neural processes associated with antisaccade task performance investigated with event-related FMRI. J Neurophysiol 94(1):429–440

    PubMed  Google Scholar 

  • Frischen A, Bayliss AP, Tipper SP (2007) Gaze cueing of attention: visual attention, social cognition, and individual differences. Psychol Bull 133(4):694

    PubMed  PubMed Central  Google Scholar 

  • Furlan M, Smith AT, Walker R (2016) An fMRI investigation of preparatory set in the human cerebral cortex and superior colliculus for pro- and anti-saccades. PLoS One 11(7):e0158337. https://doi.org/10.1371/journal.pone.0158337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hallett PE (1978) Primary and secondary saccades to goals defined by instructions. Vis Ress 18:1279–1296

    CAS  Google Scholar 

  • Heath M, Shellington E, Titheridge S, Gill DP, Petrella RJ (2017) A 24-week multi-modality exercise program improves executive control in older adults with a self-reported cognitive complaint: evidence from the antisaccade task. J Alzheimers Dis 56(1):167–183

    PubMed  Google Scholar 

  • Hess EH, Polt JM (1964) Pupil size in relation to mental activity during simple problem-solving. Science 143(3611):1190–1192

    CAS  PubMed  Google Scholar 

  • Hutchison KA, Moffitt CC, Hart K, Hood AV, Watson JM, Marchak FM (2020) Measuring task set preparation versus mind wandering using pupillometry. J Exp Psychol Learn 46(2):280–295

    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. Front Hum Neurosci 5:97

    PubMed  PubMed Central  Google Scholar 

  • Klingner J, Tversky B, Hanrahan P (2011) Effects of visual and verbal presentation on cognitive load in vigilance, memory, and arithmetic tasks. Psychophysiology 48(3):323–332

    PubMed  Google Scholar 

  • Lehmann SJ, Corneil BD (2016) Transient pupil dilation after subsaccadic microstimulation of primate frontal eye fields. J Neurosci 36(13):3765–3776

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mathôt S (2018) Pupillometry: psychology, physiology, and function. J Cognit, 1(1).

  • McDowell JE, Myles-Worsley M, Coon H, Byerley W, Clementz BA (1999) Measuring liability for schizophrenia using optimized antisaccade stimulus parameters. Psychophysiology 36(1):138–141

    CAS  PubMed  Google Scholar 

  • McDowell JE, Brown GG, Paulus M, Martinez A, Stewart SE, Dubowitz DJ, Braff DL (2002) Neural correlates of refixation saccades and antisaccades in normal and schizophrenia subjects. Biol Psychiatr 51(3):216–223

    Google Scholar 

  • Munoz DP, Everling S (2004) Look away: the anti-saccade task and the voluntary control of eye movement. Nat Rev Neurosci 5(3):218–228

    CAS  PubMed  Google Scholar 

  • O’Driscoll GA, Alpert NM, Matthysse SW, Levy DL, Rauch SL, Holzman PS (1995) Functional neuroanatomy of antisaccade eye movements investigated with positron emission tomography. Proc Natl Acad Sci USA 92:925–929 (pmid:7846080)

    PubMed  Google Scholar 

  • Olk B, Kingstone A (2003) Why are antisaccades slower than prosaccades? A novel finding using a new paradigm. NeuroReport 14(1):151–155

    PubMed  Google Scholar 

  • Pierce JE, McCardel JB, McDowell JE (2015) Trial-type probability and task-switching effects on behavioral response characteristics in a mixed saccade task. Exp Brain Res 233(3):959–969

    PubMed  Google Scholar 

  • Pierrot-Deseilligny CH, Rivaud S, Gaymard B, Agid Y (1991) Cortical control of reflexive visually-guided saccades. Brain 114(3):1473–1485

    PubMed  Google Scholar 

  • Pierrot-Deseilligny C, Müri RM, Ploner CJ, Gaymard B, Demeret S, Rivaud-Pechoux S (2003) Decisional role of the dorsolateral prefrontal cortex in ocular motor behaviour. Brain 126(6):1460–1473

    CAS  PubMed  Google Scholar 

  • Rajkowski J, Kubiak P, Aston-Jones G (1994) Locus coeruleus activity in monkey: phasic and tonic changes are associated with altered vigilance. Brain Res Bull 35(5–6):607–616

    CAS  PubMed  Google Scholar 

  • Smyrnis N (2008) Metric issues in the study of eye movements in psychiatry. Brain Cogn 68(3):341–358

    PubMed  Google Scholar 

  • Wang CA, Boehnke SE, White BJ, Munoz DP (2012) Microstimulation of the monkey superior colliculus induces pupil dilation without evoking saccades. J Neurosci 32(11):3629–3636

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J, Tian J, Wang R, Benson V (2013) Increased attentional focus modulates eye movements in a mixed antisaccade task for younger and older adults. PLoS One 8(4):e61566

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang CA, Brien DC, Munoz DP (2015) Pupil size reveals preparatory processes in the generation of pro-saccades and anti-saccades. Eur J Neurosci 41(8):1102–1110

    PubMed  Google Scholar 

  • Winn MB, Wendt D, Koelewijn T, Kuchinsky SE (2018) Best practices and advice for using pupillometry to measure listening effort: An introduction for those who want to get started. Trends Hear 22:2331216518800869

    PubMed  PubMed Central  Google Scholar 

  • Zeligman L, Zivotofsky AZ (2017) Back to basics: The effects of block vs. interleaved trial administration on pro-and anti-saccade performance. PLoS One 12(2):e0172485

    PubMed  PubMed Central  Google Scholar 

Download references

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Authors and Affiliations

  1. Department of Kinesiology, University of Waterloo, 200 University Ave W., Waterloo, ON, N2L 5G1, Canada

    Naila Ayala & Ewa Niechwiej-Szwedo

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  1. Naila Ayala
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  2. Ewa Niechwiej-Szwedo
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Correspondence to Ewa Niechwiej-Szwedo.

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Communicated by Bill J Yates.

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Ayala, N., Niechwiej-Szwedo, E. Effects of blocked vs. interleaved administration mode on saccade preparatory set revealed using pupillometry. Exp Brain Res 239, 245–255 (2021). https://doi.org/10.1007/s00221-020-05967-9

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