Advertisement

Experimental Brain Research

, Volume 236, Issue 8, pp 2399–2410 | Cite as

Shared variance of oculomotor phenotypes in a large sample of healthy young men

  • D. Valakos
  • T. Karantinos
  • I. Evdokimidis
  • N. C. Stefanis
  • D. Avramopoulos
  • N. Smyrnis
Research Article
  • 73 Downloads

Abstract

This study used canonical correlation analysis to investigate patterns of shared variance between parameters measured in seven different occulomotor function tasks, namely the visually guided saccade task, the antisaccade task, the closed-loop smooth-pursuit task, the open-loop smooth-pursuit task, and three active visual fixation tasks. These tasks were performed by 2130 young army recruits. Only a small percentage (1–10%) of shared variance existed between sets of parameters for all oculomotor function tasks measured. The most correlated tasks were the visually guided saccade and the antisaccade. The first common factor correlated with speed of performance between these tasks (latency), while the second and third correlated with accuracy of performance. Better performance in active visual fixation tasks correlated with better performance accuracy (lower error rate) and increased speed (lower latency) in the antisaccade and saccade tasks as well as better performance in the closed-loop smooth-pursuit task (increase in gain and decrease in the rate of unwanted saccades during pursuit). Better performance in the closed-loop smooth-pursuit task (increased gain and decreased number of unwanted saccades) also correlated with increased accuracy and increased speed of performing saccades and antisaccades. Finally, the open-loop fixation task had no correlation with all other oculomotor tasks except for a very weak negative correlation with the closed-loop pursuit task where better performance (increased gain) in one correlated with worse performance (decreased gain) in the other. The results of this analysis showed that a small percentage of variance is shared among different oculomotor function tasks. The structure of this shared variance could be used to derive common oculomotor function indices to study their relation to genetic and other sources of inter-subject variation.

Keywords

Saccades Antisaccades Smooth eye pursuit Fixation Canonical analysis Eye movements 

References

  1. Bargary G, Bosten JM, Goodbourn PT, Lawrance-Owen AJ, Hogg RE, Mollon JD (2017) Individual differences in human eye movements: an oculomotor signature? Vision Res 141:157–169.  https://doi.org/10.1016/j.visres.2017.03.001 CrossRefPubMedGoogle Scholar
  2. Biscaldi M, Fischer B, Stuhr V (1996) Human express saccade makers are impaired at suppressing visually evoked saccades. J Neurophysiol 76:199–214.  https://doi.org/10.1152/jn.1996.76.1.199 CrossRefPubMedGoogle Scholar
  3. Caldani S, Amado I, Bendjemaa N et al (2017) Oculomotricity and neurological soft signs: can we refine the endophenotype? A study in subjects belonging to the spectrum of schizophrenia. Psychiatry Res 256:490–497.  https://doi.org/10.1016/j.psychres.2017.06.013 CrossRefPubMedGoogle Scholar
  4. Chan JL, Koval MJ, Johnston K, Everling S (2017) Neural correlates for task switching in the macaque superior colliculus. J Neurophysiol 118:2156–2170.  https://doi.org/10.1152/jn.00139.2017 CrossRefPubMedGoogle Scholar
  5. Coe BC, Munoz DP (2017) Mechanisms of saccade suppresion revealed in the antisaccade task. Phil Trans R Soc B 372:20160192 doi.  https://doi.org/10.1098/rstb.2016.0192 CrossRefPubMedGoogle Scholar
  6. Constantinidis TS, Smyrnis N, Evdokimidis I, Stefanis NC, Avramopoulos D, Giouzelis I, Stefanis CN (2003) Effects of direction on saccadic performance in relation to lateral preferences. Exp Brain Res 150:443–448.  https://doi.org/10.1007/s00221-003-1454-0 CrossRefPubMedGoogle Scholar
  7. Cornelissen FW, Kimmig H, Schira M et al (2002) Event-related fMRI responses in the human frontal eye fields in a randomized pro- and antisaccade task. Exp Brain Res 145:270–274.  https://doi.org/10.1007/s00221-002-1136-3 CrossRefPubMedGoogle Scholar
  8. Curtis CE, D’Esposito M (2003) Success and failure suppressing reflexive behavior. J Cogn Neurosci 15:409–418.  https://doi.org/10.1162/089892903321593126 CrossRefPubMedGoogle Scholar
  9. Damilou A, Apostolakis S, Thrapsanioti E, Theleritis C, Smyrnis N (2016) Shared and distinct oculomotor function deficits in schizophrenia and obsessive compulsive disorder. Psychophysiology 53:796–805.  https://doi.org/10.1111/psyp.12630 CrossRefPubMedGoogle Scholar
  10. DeSimone JC, Everling S, Heath M (2015) The antisaccade task: visual distractors elicit a location-independent planning ‘cost’. PLoS One 10:e0122345.  https://doi.org/10.1371/journal.pone.0122345 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 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.  https://doi.org/10.1152/jn.00562.2002 CrossRefPubMedGoogle Scholar
  12. Evdokimidis I, Smyrnis N, Constantinidis TS et al (2002) The antisaccade task in a sample of 2,006 young men. I. Normal population characteristics. Exp Brain Res 147:45–52.  https://doi.org/10.1007/s00221-002-1208-4 CrossRefPubMedGoogle Scholar
  13. Everling S, Fischer B (1998) The antisaccade: a review of basic research and clinical studies. Neuropsychologia 36:885–899CrossRefPubMedGoogle Scholar
  14. Everling S, Krappmann P, Flohr H (1997) Cortical potentials preceding pro- and antisaccades in man. Electroencephalogr Clin Neurophysiol 102:356–362CrossRefPubMedGoogle Scholar
  15. Freedman EG, Foxe JJ (2017) Eye movements, sensorimotor adaptation and cerebellar-dependent learning in autism: toward potential biomarkers and subphenotypes. Eur J Neurosci.  https://doi.org/10.1111/ejn.13625 PubMedCrossRefGoogle Scholar
  16. Fukushima K, Fukushima J, Barnes GR (2017) Clinical application of eye movement tasks as an aid to understanding Parkinson’s disease pathophysiology. Exp Brain Res 235:1309–1321.  https://doi.org/10.1007/s00221-017-4916-5 CrossRefPubMedGoogle Scholar
  17. Gaymard B, Rivaud S, Cassarini JF, Dubard T, Rancurel G, Agid Y, Pierrot-Deseilligny C (1998) Effects of anterior cingulate cortex lesions on ocular saccades in humans. Exp Brain Res 120:173–183CrossRefPubMedGoogle Scholar
  18. Gooding DC, Basso MA (2008) The tell-tale tasks: a review of saccadic research in psychiatric patient populations. Brain Cogn 68:371–390.  https://doi.org/10.1016/j.bandc.2008.08.024 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Hatzimanolis A, Bhatnagar P, Moes A et al (2015) Common genetic variation and schizophrenia polygenic risk influence neurocognitive performance in young adulthood. Am J Med Genet B Neuropsychiatr Genet 168B:392–401.  https://doi.org/10.1002/ajmg.b.32323 CrossRefPubMedGoogle Scholar
  20. Kattoulas E, Smyrnis N, Stefanis NC, Avramopoulos D, Stefanis CN, Evdokimidis I (2011a) Predictive smooth eye pursuit in a population of young men: I. Effects of age, IQ, oculomotor and cognitive tasks. Exp Brain Res 215:207–218.  https://doi.org/10.1007/s00221-011-2887-5 CrossRefPubMedGoogle Scholar
  21. Kattoulas E, Evdokimidis I, Stefanis NC, Avramopoulos D, Stefanis CN, Smyrnis N (2011b) Predictive smooth eye pursuit in a population of young men: II. Effects of schizotypy, anxiety and depression. Exp Brain Res 215:219–226.  https://doi.org/10.1007/s00221-011-2888-4 CrossRefPubMedGoogle Scholar
  22. Kattoulas E, Stefanis NC, Avramopoulos D, Stefanis CN, Evdokimidis I, Smyrnis N (2012) Schizophrenia-related RGS4 gene variations specifically disrupt prefrontal control of saccadic eye movements. Psychol Med 42:757–767.  https://doi.org/10.1017/s003329171100167x CrossRefPubMedGoogle Scholar
  23. Kheradmand A, Colpak AI, Zee DS (2016) Eye movements in vestibular disorders. Handb Clin Neurol 137:103–117.  https://doi.org/10.1016/b978-0-444-63437-5.00008-x CrossRefPubMedGoogle Scholar
  24. Krebs RM, Woldorff MG, Tempelmann C et al (2010) High-field FMRI reveals brain activation patterns underlying saccade execution in the human superior colliculus. PLoS One 5:e8691.  https://doi.org/10.1371/journal.pone.0008691 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Kuntsi J, Wood AC, Rijsdijk F et al (2010) Separation of cognitive impairments in attention-deficit/hyperactivity disorder into 2 familial factors. Arch Gen Psychiatry 67:1159–1167.  https://doi.org/10.1001/archgenpsychiatry.2010.139 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Lencer R, Trillenberg P (2008) Neurophysiology and neuroanatomy of smooth pursuit in humans. Brain Cogn 68:219–228.  https://doi.org/10.1016/j.bandc.2008.08.013 CrossRefPubMedGoogle Scholar
  27. Lencer R, Sprenger A, Reilly JL et al (2015) Pursuit eye movements as an intermediate phenotype across psychotic disorders: Evidence from the B-SNIP study. Schizophr Res 169:326–333.  https://doi.org/10.1016/j.schres.2015.09.032 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Mayfrank L, Mobashery M, Kimmig H, Fischer B (1986) The role of fixation and visual attention in the occurrence of express saccades in man. Eur Arch Psychiatry Neurol Sci 235:269–275CrossRefPubMedGoogle Scholar
  29. Pierrot-Deseilligny C, Rivaud S, Gaymard B, Agid Y (1991) Cortical control of reflexive visually-guided saccades. Brain 114(Pt 3):1473–1485CrossRefPubMedGoogle Scholar
  30. Ploner CJ, Gaymard BM, Rivaud-Pechoux S, Pierrot-Deseilligny C (2005) The prefrontal substrate of reflexive saccade inhibition in humans. Biol Psychiatry 57:1159–1165.  https://doi.org/10.1016/j.biopsych.2005.02.017 CrossRefPubMedGoogle Scholar
  31. Rivaud S, Muri RM, Gaymard B, Vermersch AI, Pierrot-Deseilligny C (1994) Eye movement disorders after frontal eye field lesions in humans. Exp Brain Res 102:110–120CrossRefPubMedGoogle Scholar
  32. Smyrnis N (2008) Metric issues in the study of eye movements in psychiatry. Brain Cogn 68:341–358.  https://doi.org/10.1016/j.bandc.2008.08.022 CrossRefPubMedGoogle Scholar
  33. Smyrnis N, Evdokimidis I, Stefanis NC et al (2002) The antisaccade task in a sample of 2,006 young males. II. Effects of task parameters. Exp Brain Res 147:53–63.  https://doi.org/10.1007/s00221-002-1207-5 CrossRefPubMedGoogle Scholar
  34. Smyrnis N, Evdokimidis I, Stefanis NC, Avramopoulos D, Constantinidis TS, Stavropoulos A, Stefanis CN (2003) Antisaccade performance of 1,273 men: effects of schizotypy, anxiety, and depression. J Abnorm Psychol 112:403–414CrossRefPubMedGoogle Scholar
  35. Smyrnis N, Kattoulas E, Evdokimidis I et al (2004) Active eye fixation performance in 940 young men: effects of IQ, schizotypy, anxiety and depression. Exp Brain Res 156:1–10.  https://doi.org/10.1007/s00221-003-1759-z CrossRefPubMedGoogle Scholar
  36. Smyrnis N, Evdokimidis I, Mantas A et al (2007) Smooth pursuit eye movements in 1,087 men: effects of schizotypy, anxiety, and depression. Exp Brain Res 179:397–408.  https://doi.org/10.1007/s00221-006-0797-8 CrossRefPubMedGoogle Scholar
  37. Smyrnis N, Kattoulas E, Stefanis NC, Avramopoulos D, Stefanis CN, Evdokimidis I (2011) Schizophrenia-related neuregulin-1 single-nucleotide polymorphisms lead to deficient smooth eye pursuit in a large sample of young men. Schizophr Bull 37:822–831.  https://doi.org/10.1093/schbul/sbp150 CrossRefPubMedGoogle Scholar
  38. Theleritis C, Evdokimidis I, Smyrnis N (2014) Variability in the decision process leading to saccades: a specific marker for schizophrenia? Psychophysiology 51:327–336.  https://doi.org/10.1111/psyp.12178 CrossRefPubMedGoogle Scholar
  39. Trillenberg P, Sprenger A, Talamo S, Herold K, Helmchen C, Verleger R, Lencer R (2017) Visual and non-visual motion information processing during pursuit eye tracking in schizophrenia and bipolar disorder. Eur Arch Psychiatry Clin Neurosci 267:225–235.  https://doi.org/10.1007/s00406-016-0671-z CrossRefPubMedGoogle Scholar
  40. Vernet M, Quentin R, Chanes L, Mitsumasu A, Valero-Cabre A (2014) Frontal eye field, where art thou? Anatomy, function, and non-invasive manipulation of frontal regions involved in eye movements and associated cognitive operations. Front Integr Neurosci 8:66.  https://doi.org/10.3389/fnint.2014.00066 PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • D. Valakos
    • 1
  • T. Karantinos
    • 1
  • I. Evdokimidis
    • 3
  • N. C. Stefanis
    • 2
  • D. Avramopoulos
    • 4
  • N. Smyrnis
    • 1
    • 2
  1. 1.Laboratory of Cognitive NeuroscienceUniversity Mental Health Research InstituteAthensGreece
  2. 2.Psychiatry Department, Medical School, Eginition HospitalNational and Kapodistrian University of AthensAthensGreece
  3. 3.Neurology Department, Medical School, Eginition HospitalNational and Kapodistrian University of AthensAthensGreece
  4. 4.McKusick-Nathans Institute of Genetic MedicineJohns Hopkins UniversityBaltimoreUSA

Personalised recommendations