Experimental Brain Research

, Volume 232, Issue 12, pp 3949–3963 | Cite as

Oculomotor inhibitory control in express saccade makers

  • Felicity D. A. WolohanEmail author
  • Paul C. Knox
Research Article


Express saccade makers (ESMs) produce high proportions (>30 %) of low-latency (80–130 ms) express saccades in tasks in which such responses are usually suppressed. In addition, high directional error rates on the antisaccade (AS) task suggest a failure of oculomotor inhibitory mechanisms in ESMs. However, the AS task is complex and does not provide a measure of inhibitory processes in isolation. We therefore examined inhibitory control in 25 ESM and 28 non-ESM (‘Norm’) participants, using a minimally delayed oculomotor response (MDOR) task. After a randomised fixation period, a pro-saccade target appeared for 200 or 1,000 ms. Participants were instructed to maintain fixation and saccade to the target position upon target offset. In a control task, they saccaded on target onset. Overall, saccade latency was considerably increased in the MDOR task compared to the control task (354 vs. 170 ms; p < 0.001), and we also observed a latency modulation with display time (200: 399, 1,000: 302 ms; p < 0.001). However, there was no evidence of a difference between groups (p = 0.29). Errors consisted primarily of responses to target onsets and error rates were comparable between the groups (p = 0.33). The overproduction of fast, reflexive responses was still observed in ESMs who generated a higher proportion of their errors within the express latency range (p < 0.001). We confirmed that in the AS task, the ESMs exhibited a higher directional error rate (p = 0.03). These results suggest that the performance ‘deficit’ observed on the AS task in ESMs cannot be attributed to generally weaker inhibitory control.


Saccades Express saccades Antisaccades Inhibitory control Latency 



This study was supported by a project grant from the Leverhulme Trust (RPG329). We are grateful to all the participants who took part in these experiments.


  1. Abroms BD, Gottlob LR, Fillmore MT (2006) Alcohol effects on inhibitory control of attention: distinguishing between intentional and automatic mechanisms. Psychopharmacology 188:324–334PubMedCrossRefGoogle Scholar
  2. Amatya N, Gong Q, Knox PC (2011) Differing proportions of ‘express saccade makers’ in different human populations. Exp Brain Res 210:117–129PubMedCrossRefGoogle Scholar
  3. Bibi R, Edelman J (2009) The influence of motor training on human express saccade production. J Neurophysiol 102:3101–3110PubMedCentralPubMedCrossRefGoogle Scholar
  4. Biscaldi M, Fischer B, Stuhr V (1996) Human express saccade makers are impaired at suppressing visually evoked saccades. J Neurophysiol 76:199–214PubMedGoogle Scholar
  5. Cavegn D, Biscaldi M (1996) Fixation and saccade control in an express-saccade maker. Exp Brain Res 109:101–116PubMedGoogle Scholar
  6. Clementz BA, McDowell JE, Zisook S (1994) Saccadic system functioning among schizophrenia patients and their first-degree biological relatives. J Abnorm Psychol 103:277PubMedCrossRefGoogle Scholar
  7. Crawford T, Parker E, Solis-Trapala I, Mayes J (2011) Is the relationship of prosaccade reaction times and antisaccade errors mediated by working memory? Exp Brain Res 208:385–397PubMedCrossRefGoogle Scholar
  8. Delinte A, Gomez CM, Decostre MF, Crommelinck M, Roucoux A (2002) Amplitude transition function of human express saccades. Neurosci Res 42:21–34PubMedCrossRefGoogle Scholar
  9. Dorris MC, Pare M, Munoz DP (1997) Neuronal activity in monkey superior colliculus related to the initiation of saccadic eye movements. J Neurosci 17:8566–8579PubMedGoogle Scholar
  10. Edelman JA, Keller EL (1996) Activity of visuomotor burst neurons in the superior colliculus accompanying express saccades. J Neurophysiol 76:908–926PubMedGoogle Scholar
  11. Everling S, Fischer B (1998) The antisaccade: a review of basic research and clinical studies. Neuropsychologia 36:885–899PubMedCrossRefGoogle Scholar
  12. Findlay JM (1981) Spatial and temporal factors in the predictive generation of saccadic eye movements. Vis Res 21:347–354PubMedCrossRefGoogle Scholar
  13. Fischer B, Boch R (1983) Saccadic eye movements after extremely short reaction times in the monkey. Brain Res 260:21–26PubMedCrossRefGoogle Scholar
  14. Fischer B, Ramsperger E (1984) Human express saccades: extremely short reaction times of goal directed eye movements. Exp Brain Res 57:191–195PubMedCrossRefGoogle Scholar
  15. Gooding DC, Miller MD, Kwapil TR (2000) Smooth pursuit eye tracking and visual fixation in psychosis-prone individuals. Psychiatry Res 93:41–54PubMedCrossRefGoogle Scholar
  16. Gooding DC, Mohapatra L, Shea HB (2004) Temporal stability of saccadic task performance in schizophrenia and bipolar patients. Psychol Med 349:921–932CrossRefGoogle Scholar
  17. Gottlob LR, Fillmore MT, Abroms BD (2007) Age-group differences in inhibiting an oculomotor response. Aging Neuropsychol Cogn 14:586–593CrossRefGoogle Scholar
  18. Guitton D, Buchtel HA, Douglas RM (1985) Frontal lobe lesions in man cause difficulties in suppressing reflexive glances and in generating goal-directed saccades. Exp Brain Res 58:455–472PubMedCrossRefGoogle Scholar
  19. Hodgson T, Chamberlain M, Parris B, James M, Gutowski N, Husain M et al (2007) The role of the ventrolateral frontal cortex in inhibitory oculomotor control. Brain 130:1525–1537PubMedCrossRefGoogle Scholar
  20. Hommer DW, Clem T, Litman R, Pickar D (1991) Maladaptive anticipatory saccades in schizophrenia. Biol Psychiatry 30:779–794PubMedCrossRefGoogle Scholar
  21. Hutton SB, Ettinger U (2006) The antisaccade task as a research tool in psychopathology: a critical review. Psychophysiology 43:302–313PubMedCrossRefGoogle Scholar
  22. Hutton SB, Joyce EM, Barnes TRE, Kennard C (2002) Saccadic distractibility in first-episode schizophrenia. Neuropsychologia 40(10):1729–1736PubMedCrossRefGoogle Scholar
  23. Kane MJ, Bleckley MK, Conway AR, Engle RW (2001) A controlled-attention view of working-memory capacity. J Exp Psychol Gen 130:169–183PubMedCrossRefGoogle Scholar
  24. Kissler J, Clementz BA (1998) Fixation stability among schizophrenia patients. Neuropsychobiology 38:57–62PubMedCrossRefGoogle Scholar
  25. Knox PC, Razak N (2010) Oculomotor inhibition: shared or separate mechanisms for saccades and smooth pursuit? Soc Neurosci Absts 676:17Google Scholar
  26. Knox PC, Wolohan FDA (2014) Cultural diversity and saccade similarities: culture does not explain saccade latency differences between Chinese and Caucasian participants. PLoS One 9:e94424PubMedCentralPubMedCrossRefGoogle Scholar
  27. Knox PC, Amatya N, Jiang X, Gong Q (2012) Performance deficits in a voluntary saccade task in Chinese “express saccade makers”. PLoS One 7:e47688PubMedCentralPubMedCrossRefGoogle Scholar
  28. Ludwig CJ, Ranson A, Gilchrist ID (2008) Oculomotor capture by transient events: a comparison of abrupt onsets, offsets, motion, and flicker. J Vision 8:1–16CrossRefGoogle Scholar
  29. Minshew NJ, Luna B, Sweeney JA (1999) Oculomotor evidence for neocortical systems but not cerebellar dysfunction in autism. Neurology 52:917–922PubMedCentralPubMedCrossRefGoogle Scholar
  30. Nieman DH, Bour LJ, Linszen DH, Goede J, Koelman JHTM, Gersons BPR et al (2000) Neuropsychological and clinical correlates of antisaccade task performance in schizophrenia. Neurology 54:866–871PubMedCrossRefGoogle Scholar
  31. Oswal A, Ogden M, Carpenter RH (2007) The time course of stimulus expectation in a saccadic decision task. J Neurophysiol 97:2722–2730PubMedCrossRefGoogle Scholar
  32. Pierrot-Deseilligny C, Muri R, Rivaud-Pechoux S, Gaymard B, Ploner CJ (2002) Cortical control of spatial memory in humans: the visuooculomotor model. Ann Neurol 52:10–19PubMedCrossRefGoogle Scholar
  33. Pratt J, Trottier L (2005) Pro-saccades and anti-saccades to onset and offset targets. Vis Res 45:765–774PubMedCrossRefGoogle Scholar
  34. Radant AD, Claypoole K, Wingerson DK, Cowley DS, Roy-Byrne PP (1997) Relationships between neuropsychological and oculomotor measures in schizophrenia patients and normal controls. Biol Psychiatry 42:797–805PubMedCrossRefGoogle Scholar
  35. Reuter B, Kathmann N (2004) Using saccade tasks as a tool to analyze executive dysfunctions in schizophrenia. Acta Psychol 115:255–269CrossRefGoogle Scholar
  36. Reuter B, Rakusan L, Kathmann N (2005) Poor antisaccade performance in schizophrenia: an inhibition deficit? Psychiatry Res 135:1–10PubMedCrossRefGoogle Scholar
  37. Roberts RJ, Hager LD, Heron C (1994) Prefrontal cognitive processes: working memory and inhibition in the antisaccade task. J Exp Psychol Gen 123:374–393CrossRefGoogle Scholar
  38. Ross RG, Hommer DW, Breiger D, Varley C, Radant AD (1994) Eye movement task related to frontal lobe functioning in children with attention deficit disorder. J Am Acad Child Adolesc Psychiatry 33:869–874PubMedCrossRefGoogle Scholar
  39. Ross RG, Harris JG, Olincy A, Radant A, Adler LE, Freedman R (1998) Familial transmission of two independent saccadic abnormalities in schizophrenia. Schizophr Res 30:59–70PubMedCrossRefGoogle Scholar
  40. Ross RG, Harris JG, Olincy A, Radant A (2000) Eye movement task measures inhibition and spatial working memory in adults with schizophrenia, ADHD, and a normal comparison group. Psychiatry Res 95:35–42PubMedCrossRefGoogle Scholar
  41. Saslow MG (1967) Effects of components of displacement step stimuli upon latency for saccadic eye movements. J Opt Soc Am 57:1024–1029PubMedCrossRefGoogle Scholar
  42. Schiller PH, Sandell JH, Maunsell JH (1987) The effect of frontal eye field and superior colliculus lesions on saccadic latencies in the rhesus monkey. J Neurophysiol 57:1033–1049PubMedGoogle Scholar
  43. Stuyven E, Van der Goten K, Vandierendonck A, Claeys K, Crevits L (2000) The effect of cognitive load on saccadic eye movements. Acta Psychol 104:69–85CrossRefGoogle Scholar
  44. Unsworth N, Schrock JC, Engle RW (2004) Working memory capacity and the antisaccade task: individual differences in voluntary saccade control. J Exp Psychol 30:1302–1321Google Scholar
  45. Van Koningsbruggen MG, Rafal RD (2009) Control of oculomotor reflexes: independent effects of strategic and automatic preparation. Exp Brain Res 192:761–768PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Department of Eye and Vision Science, Institute of Ageing and Chronic DiseaseUniversity of LiverpoolLiverpoolUK

Personalised recommendations