Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Look away: the anti-saccade task and the voluntary control of eye movement

Nature Reviews Neuroscience volume 5, pages 218–228 (2004)Cite this article

Key Points

  • The anti-saccade task, in which subjects are required to make a saccadic eye movement away from a target, rather than towards it, is a useful task for investigating the voluntary and flexible control of movement. Anti-saccades have a longer latency than pro-saccades and subjects are more likely to make errors on anti-saccade trials. These errors usually consist of a rapid saccade to the target, which is often corrected within a short latency by a second saccade away from the target. Two processes are needed for the anti-saccade task: suppression of the automatic pro-saccade, and inversion of the stimulus vector into the correct saccade vector.

  • Monkeys and humans perform similarly on this task. In electrophysiological studies of monkeys doing the anti-saccade task, saccade neurons in the superior colliculus (SC) and frontal eye fields (FEF) seem to be inhibited before the target appears, to suppress the automatic pro-saccade. This is proposed to prevent activity in these neurons from crossing a threshold that would allow a saccade to be initiated. The suppression could arise from several sources, including other neurons in the FEF and SC, the supplementary eye fields, the dorsolateral prefrontal cortex (DLPFC) and the substantia nigra pars reticulata.

  • The generation of the anti-saccade requires vector inversion and a build-up of activity in a different set of saccade neurons. Monkey electrophysiology studies indicate that vector inversion involves the lateral intraparietal area and/or the FEF.

  • In humans, functional imaging and event-related potential (ERP) studies have been used to study the anti-saccade task. These studies have identified differences in brain activity between pro-saccades and anti-saccades that are consistent with data from electrophysiological studies in monkeys.

  • Young children struggle to perform the anti-saccade task, apparently because they have difficulty in suppressing the automatic pro-saccade. This might relate to the protracted maturation of the frontal lobes, which have been proposed to mediate top-down inhibition of saccade neurons. Patients with lesions of the DLPFC have a similar deficit in performance. By contrast, lesions of the FEF impair the ability of patients to generate the anti-saccade.

  • A number of clinical conditions affect performance on the anti-saccade task. Patients with schizophrenia show increased error rates and prolonged reaction times. Patients with attention-deficit hyperactivity disorder struggle to suppress the automatic pro-saccade but do not show delays in reaction times, whereas those with Parkinson's disease have significantly increased reaction times and also an increased error rate. Tourette's syndrome causes an increase in reaction time with no increase in error rate, possibly because these patients generate increased top-down inhibition as a consequence of adapting to the disorder. All of these findings can be interpreted in the context of an 'accumulator model' of saccade generation.

Abstract

The anti-saccade task has emerged as an important task for investigating the flexible control that we have over behaviour. In this task, participants must suppress the reflexive urge to look at a visual target that appears suddenly in the peripheral visual field and must instead look away from the target in the opposite direction. A crucial step involved in performing this task is the top-down inhibition of a reflexive, automatic saccade. Here, we describe recent neurophysiological evidence demonstrating the presence of this inhibitory function in single-cell activity in the frontal eye fields and superior colliculus. Patients diagnosed with various neurological and/or psychiatric disorders that affect the frontal lobes or basal ganglia find it difficult to suppress the automatic pro-saccade, revealing a deficit in top-down inhibition.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: The anti-saccade task.
Figure 2: Discharges recorded from a fixation neuron (FN) and a saccade neuron (SN) in frontal eye field and superior colliculus when a monkey performs the pro-saccade and anti-saccade tasks in the gap condition.
Figure 3: Activity of individual saccade neurons in the frontal eye field and superior colliculus.
Figure 4: An accumulator model can be used to represent the accumulation of saccade activity in the brain on anti-saccade trials.

Similar content being viewed by others

References

  1. Hallett, P. E. Primary and secondary saccades to goals defined by instructions. Vision Res. 18, 1279–1296 (1978). This study introduced the anti-saccade task.

    Article  CAS  PubMed  Google Scholar 

  2. Amador, N., Schlag-Rey, M. & Schlag, J. Primate antisaccades. I. Behavioral characteristics. J. Neurophysiol. 80, 1775–1786 (1998).

    Article  CAS  PubMed  Google Scholar 

  3. Bell, A. H., Everling, S. & Munoz, D. P. Influence of stimulus eccentricity and direction on characteristics of pro- and antisaccades in non-human primates. J. Neurophysiol. 84, 2595–2604 (2000).

    Article  CAS  PubMed  Google Scholar 

  4. Fischer, B. & Weber, H. Effects of stimulus conditions on the performance of antisaccades in man. Exp. Brain Res. 116, 191–200 (1997).

    Article  CAS  PubMed  Google Scholar 

  5. Munoz, D. P., Broughton, J. R., Goldring, J. E. & Armstrong, I. T. Age-related performance of human subjects on saccadic eye movement tasks. Exp. Brain Res. 121, 391–400 (1998).

    Article  CAS  PubMed  Google Scholar 

  6. Hallett, P. E. & Adams, B. D. The predictability of saccadic latency in a novel voluntary oculomotor task. Vision Res. 20, 329–339 (1980).

    Article  CAS  PubMed  Google Scholar 

  7. Dorris, M. C. & Munoz, D. P. A neural correlate for the gap effect on saccadic reaction times in monkey. J. Neurophysiol. 73, 2558–2562 (1995).

    Article  CAS  PubMed  Google Scholar 

  8. Forbes, K. & Klein, R. M. The magnitude of the fixation offset effect with endogenously and exogenously controlled saccades. J. Cogn. Neurosci. 8, 344–352 (1996).

    Article  CAS  PubMed  Google Scholar 

  9. Fischer, B. & Weber, H. Express saccades and visual attention. Behav. Brain Sci. 16, 553–610 (1993).

    Article  Google Scholar 

  10. Fischer, B. & Boch, R. Saccadic eye movements after extremely short reaction times in the monkey. Brain Res. 260, 21–26 (1983).

    Article  CAS  PubMed  Google Scholar 

  11. Pare, M. & Munoz, D. P. Saccadic reaction time in the monkey: advanced preparation of oculomotor programs is primarily responsible for express saccade occurrence. J. Neurophysiol. 76, 3666–3681 (1996).

    Article  CAS  PubMed  Google Scholar 

  12. Hess, W. R., Burgi, S. & Bucher, V. Motor function of tectal and tegmental area. Monatsschr. Psychiatr. Neurol. 112, 1–52 (1946).

    Article  CAS  PubMed  Google Scholar 

  13. Carpenter, R. H. S. in Eye Movements: Cognition and Visual Perception (eds Fischer, D. F. & Monty, R. A.) 237–246 (Erlbaum, Hillsdale, New Jersey, 1981).

    Google Scholar 

  14. Edelman, J. A. & Keller, E. L. Activity of visuomotor burst neurons in the superior colliculus accompanying express saccades. J. Neurophysiol. 76, 908–926 (1996).

    Article  CAS  PubMed  Google Scholar 

  15. Dorris, M. C., Pare, M. & Munoz, D. P. Neuronal activity in monkey superior colliculus related to the initiation of saccadic eye movements. J. Neurosci. 17, 8566–8579 (1997). This paper shows that the level of pretarget activation of saccade neurons in the superior colliculus is negatively correlated with saccadic reaction times.

    Article  CAS  PubMed  Google Scholar 

  16. Sparks, D., Rohrer, W. H. & Zhang, Y. The role of the superior colliculus in saccade initiation: a study of express saccades and the gap effect. Vision Res. 40, 2763–2777 (2000).

    Article  CAS  PubMed  Google Scholar 

  17. Fischer, B., Gezeck, S. & Hartnegg, K. On the production and correction of involuntary prosaccades in a gap antisaccade task. Vision Res. 40, 2211–2217 (2000).

    Article  CAS  PubMed  Google Scholar 

  18. Everling, S., Dorris, M. C. & Munoz, D. P. Reflex suppression in the anti-saccade task is dependent on prestimulus neural processes. J. Neurophysiol. 80, 1584–1589 (1998). This study demonstrates that errors in the anti-saccade task are associated with a high level of pretarget excitation of saccade neurons in the primate superior colliculus.

    Article  CAS  PubMed  Google Scholar 

  19. Luce, R. D. Response Times: Their Role in Inferring Elementary Mental Organization (Oxford Univ. Press, Oxford, 1986).

    Google Scholar 

  20. Carpenter, R. H. & Williams, M. L. Neural computation of log likelihood in control of saccadic eye movements. Nature 377, 59–62 (1995). An experimental study that supports the accumulator model of saccade initiation.

    Article  CAS  PubMed  Google Scholar 

  21. Ratcliff, R. A diffusion model account of response time and accuracy in a brightness discrimination task: fitting real data and failing to fit fake but plausible data. Psychon. Bull. Rev. 9, 278–291 (2002).

    Article  PubMed  Google Scholar 

  22. Trappenberg, T. P., Dorris, M. C., Munoz, D. P. & Klein, R. M. A model of saccade initiation based on the competitive integration of exogenous and endogenous signals in the superior colliculus. J. Cogn. Neurosci. 13, 256–271 (2001).

    Article  CAS  PubMed  Google Scholar 

  23. Hanes, D. P. & Schall, J. D. Neural control of voluntary movement initiation. Science 274, 427–430 (1996).

    Article  CAS  PubMed  Google Scholar 

  24. Gold, J. I. & Shadlen, M. N. Representation of a perceptual decision in developing oculomotor commands. Nature 404, 390–394 (2000).

    Article  CAS  PubMed  Google Scholar 

  25. Ratcliff, R., Cherian, A. & Segraves, M. A comparison of macaque behavior and superior colliculus neuronal activity to predictions from models of two-choice decisions. J. Neurophysiol. 90, 1392–1407 (2003).

    Article  PubMed  Google Scholar 

  26. Pare, M. & Hanes, D. P. Controlled movement processing: superior colliculus activity associated with countermanded saccades. J. Neurosci. 23, 6480–6489 (2003).

    Article  CAS  PubMed  Google Scholar 

  27. Everling, S., Dorris, M. C., Klein, R. M. & Munoz, D. P. Role of primate superior colliculus in preparation and execution of anti-saccades and pro-saccades. J. Neurosci. 19, 2740–2754 (1999).

    Article  CAS  PubMed  Google Scholar 

  28. Everling, S. & Munoz, D. P. Neuronal correlates for preparatory set associated with pro-saccades and anti-saccades in the primate frontal eye field. J. Neurosci. 20, 387–400 (2000). References 27 and 28 show differences in the activity of neurons in the superior colliculus and FEF between pro-saccades and anti-saccades.

    Article  CAS  PubMed  Google Scholar 

  29. Funahashi, S., Chafee, M. V. & Goldman-Rakic, P. S. Prefrontal neuronal activity in rhesus monkeys performing a delayed anti-saccade task. Nature 365, 753–756 (1993).

    Article  CAS  PubMed  Google Scholar 

  30. Desouza, J. F., Iversen, S. D. & Everling, S. Preparatory set activity associated with pro-saccades and anti-saccades within the primate prefrontal cortex. Soc. Neurosci. Abstr. 33, 661.10 (2003).

    Google Scholar 

  31. Gottlieb, J. & Goldberg, M. E. Activity of neurons in the lateral intraparietal area of the monkey during an antisaccade task. Nature Neurosci. 2, 906–912 (1999).

    Article  CAS  PubMed  Google Scholar 

  32. Zhang, M. & Barash, S. Neuronal switching of sensorimotor transformations for antisaccades. Nature 408, 971–975 (2000).

    Article  CAS  PubMed  Google Scholar 

  33. Zhang, M. & Barash, S. Persistent LIP activity in memory-antisaccades: working memory for a sensorimotor transformation. J. Neurophysiol. 91, 1424–1441 (2004). References 32 and 33 describe paradoxical visual responses in LIP neurons in an anti-saccade task.

    Article  PubMed  Google Scholar 

  34. Toth, L. J. & Assad, J. A. Dynamic coding of behaviourally relevant stimuli in parietal cortex. Nature 415, 165–168 (2002).

    Article  CAS  PubMed  Google Scholar 

  35. Olson, C. R. & Gettner, S. N. Neuronal activity related to rule and conflict in macaque supplementary eye field. Physiol. Behav. 77, 663–670 (2002).

    Article  CAS  PubMed  Google Scholar 

  36. Schlag-Rey, M., Amador, N., Sanchez, H. & Schlag, J. Antisaccade performance predicted by neuronal activity in the supplementary eye field. Nature 390, 398–401 (1997). The first study to contrast the activity of SEF neurons between pro-saccade and anti-saccade trials.

    Article  CAS  PubMed  Google Scholar 

  37. Amador, N., Schlag-Rey, M. & Schlag, J. Primate antisaccade II. Supplementary eye field neuronal activity predicts correct performance. J. Neurophysiol. 26 Nov 2003 [epub ahead of print].

  38. Sato, T. R. & Schall, J. D. Effects of stimulus-response compatibility on neural selection in frontal eye field. Neuron 38, 637–648 (2003). This study demonstrates that visual selection and saccade selection are different processes in the FEF.

    Article  CAS  PubMed  Google Scholar 

  39. Schiller, P. H., True, S. D. & Conway, J. L. Deficits in eye movements following frontal eye-field and superior colliculus ablations. J. Neurophysiol. 44, 1175–1189 (1980).

    Article  CAS  PubMed  Google Scholar 

  40. Munoz, D. P. & Schall, J. D. in The Superior Colliculus: New Approaches for Studying Sensorimotor Integration (eds Hall, W. C. & Moschovakis, A.) 55–82 (CRC, Boca Raton, Florida, 2003).

    Google Scholar 

  41. Munoz, D. P. & Istvan, P. J. Lateral inhibitory interactions in the intermediate layers of the monkey superior colliculus. J. Neurophysiol. 79, 1193–1209 (1998).

    Article  CAS  PubMed  Google Scholar 

  42. Munoz, D. P. & Wurtz, R. H. Saccade-related activity in monkey superior colliculus. I. Characteristics of burst and buildup cells. J. Neurophysiol. 73, 2313–2333 (1995).

    Article  CAS  PubMed  Google Scholar 

  43. Dias, E. C. & Bruce, C. J. Physiological correlate of fixation disengagement in the primate's frontal eye field. J. Neurophysiol. 72, 2532–2537 (1994).

    Article  CAS  PubMed  Google Scholar 

  44. Saslow, M. G. Effects of components of displacement-step stimuli upon latency of saccadic eye movements. J. Opt. Soc. Am. 57, 1024–1029 (1967).

    Article  CAS  PubMed  Google Scholar 

  45. Mayfrank, L., Mobashery, M., Kimmig, H. & Fischer, B. The role of fixation and visual attention in the occurrence of express saccades in man. Eur. Arch. Psychiatry Neurol. Sci. 235, 269–275 (1986).

    Article  CAS  PubMed  Google Scholar 

  46. Munoz, D. P. & Corneil, B. D. Evidence for interactions between target selection and visual fixation for saccade generation in humans. Exp. Brain Res. 103, 168–173 (1995).

    Article  CAS  PubMed  Google Scholar 

  47. Weber, H. & Fischer, B. Gap duration and location of attention focus modulate the occurrence of left/right asymmetries in the saccadic reaction times of human subjects. Vision Res. 35, 987–998 (1995).

    Article  CAS  PubMed  Google Scholar 

  48. Scudder, C. A., Kaneko, C. S. & Fuchs, A. F. The brainstem burst generator for saccadic eye movements: a modern synthesis. Exp. Brain Res. 142, 439–462 (2002).

    Article  PubMed  Google Scholar 

  49. Moschovakis, A. K., Scudder, C. A. & Highstein, S. M. The microscopic anatomy and physiology of the mammalian saccadic system. Prog. Neurobiol. 50, 133–254 (1996). An authorative review of the neurophysiology and anatomy of the saccadic eye movement system.

    Article  CAS  PubMed  Google Scholar 

  50. Everling, S., Pare, M., Dorris, M. C. & Munoz, D. P. Comparison of the discharge characteristics of brain stem omnipause neurons and superior colliculus fixation neurons in monkey: implications for control of fixation and saccade behavior. J. Neurophysiol. 79, 511–528 (1998).

    Article  CAS  PubMed  Google Scholar 

  51. Evinger, C., Kaneko, C. R. & Fuchs, A. F. Activity of omnipause neurons in alert cats during saccadic eye movements and visual stimuli. J. Neurophysiol. 47, 827–844 (1982).

    Article  CAS  PubMed  Google Scholar 

  52. King, W. M., Precht, W. & Dieringer, N. Afferent and efferent connections of cat omnipause neurons. Exp. Brain Res. 38, 395–403 (1980).

    Article  CAS  PubMed  Google Scholar 

  53. Schlag, J. & Schlag-Rey, M. Unit activity related to spontaneous saccades in frontal dorsomedial cortex of monkey. Exp. Brain Res. 58, 208–211 (1985).

    Article  CAS  PubMed  Google Scholar 

  54. Schlag, J. & Schlag-Rey, M. Evidence for a supplementary eye field. J. Neurophysiol. 57, 179–200 (1987).

    Article  CAS  PubMed  Google Scholar 

  55. Shook, B. L., Schlag-Rey, M. & Schlag, J. Direct projection from the supplementary eye field to the nucleus raphe interpositus. Exp. Brain Res. 73, 215–218 (1988).

    Article  CAS  PubMed  Google Scholar 

  56. Munoz, D. P. & Fecteau, J. H. Vying for dominance: dynamic interactions control visual fixation and saccadic initiation in the superior colliculus. Prog. Brain Res. 140, 3–19 (2002).

    Article  PubMed  Google Scholar 

  57. Meredith, M. A. & Ramoa, A. S. Intrinsic circuitry of the superior colliculus: pharmacophysiological identification of horizontally oriented inhibitory interneurons. J. Neurophysiol. 79, 1597–1602 (1998).

    Article  CAS  PubMed  Google Scholar 

  58. Huerta, M. F., Krubitzer, L. A. & Kaas, J. H. Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys. II. Cortical connections. J. Comp. Neurol. 265, 332–361 (1987).

    Article  CAS  PubMed  Google Scholar 

  59. Shook, B. L., Schlag-Rey, M. & Schlag, J. Primate supplementary eye field: I. Comparative aspects of mesencephalic and pontine connections. J. Comp. Neurol. 301, 618–642 (1990).

    Article  CAS  PubMed  Google Scholar 

  60. Goldman, P. S. & Nauta, W. J. Autoradiographic demonstration of a projection from prefrontal association cortex to the superior colliculus in the rhesus monkey. Brain Res. 116, 145–149 (1976).

    Article  CAS  PubMed  Google Scholar 

  61. Leichnetz, G. R., Spencer, R. F., Hardy, S. G. & Astruc, J. The prefrontal corticotectal projection in the monkey; an anterograde and retrograde horseradish peroxidase study. Neuroscience 6, 1023–1041 (1981).

    Article  CAS  PubMed  Google Scholar 

  62. Selemon, L. D. & Goldman-Rakic, P. S. Common cortical and subcortical targets of the dorsolateral prefrontal and posterior parietal cortices in the rhesus monkey: evidence for a distributed neural network subserving spatially guided behavior. J. Neurosci. 8, 4049–4068 (1988).

    Article  CAS  PubMed  Google Scholar 

  63. Asaad, W. F., Rainer, G. & Miller, E. K. Neural activity in the primate prefrontal cortex during associative learning. Neuron 21, 1399–1407 (1998).

    Article  CAS  PubMed  Google Scholar 

  64. White, I. M. & Wise, S. P. Rule-dependent neuronal activity in the prefrontal cortex. Exp. Brain Res. 126, 315–335 (1999).

    Article  CAS  PubMed  Google Scholar 

  65. Asaad, W. F., Rainer, G. & Miller, E. K. Task-specific neural activity in the primate prefrontal cortex. J. Neurophysiol. 84, 451–459 (2000).

    Article  CAS  PubMed  Google Scholar 

  66. Hikosaka, O., Takikawa, Y. & Kawagoe, R. Role of the basal ganglia in the control of purposive saccadic eye movements. Physiol. Rev. 80, 953–978 (2000).

    Article  CAS  PubMed  Google Scholar 

  67. Hikosaka, O. & Wurtz, R. H. Visual and oculomotor functions of monkey substantia nigra pars reticulata. II. Visual responses related to fixation of gaze. J. Neurophysiol. 49, 1254–1267 (1983).

    Article  CAS  PubMed  Google Scholar 

  68. Handel, A. & Glimcher, P. W. Quantitative analysis of substantia nigra pars reticulata activity during a visually guided saccade task. J. Neurophysiol. 82, 3458–3475 (1999).

    Article  CAS  PubMed  Google Scholar 

  69. Hikosaka, O. & Wurtz, R. H. Visual and oculomotor functions of monkey substantia nigra pars reticulata. IV. Relation of substantia nigra to superior colliculus. J. Neurophysiol. 49, 1285–1301 (1983).

    Article  CAS  PubMed  Google Scholar 

  70. Lynch, J. C., Graybiel, A. M. & Lobeck, L. J. The differential projection of two cytoarchitectonic subregions of the inferior parietal lobule of macaque upon the deep layers of the superior colliculus. J. Comp. Neurol. 235, 241–254 (1985).

    Article  CAS  PubMed  Google Scholar 

  71. Colby, C. L., Duhamel, J. R. & Goldberg, M. E. Visual, presaccadic, and cognitive activation of single neurons in monkey lateral intraparietal area. J. Neurophysiol. 76, 2841–2852 (1996).

    Article  CAS  PubMed  Google Scholar 

  72. Gnadt, J. W. & Andersen, R. A. Memory related motor planning activity in posterior parietal cortex of macaque. Exp. Brain Res. 70, 216–220 (1988).

    CAS  PubMed  Google Scholar 

  73. Everling, S., Krappmann, P. & Flohr, H. Cortical potentials preceding pro- and antisaccades in man. Electroencephalogr. Clin. Neurophysiol. 102, 356–362 (1997).

    Article  CAS  PubMed  Google Scholar 

  74. Evdokimidis, I., Liakopoulos, D., Constantinidis, T. S. & Papageorgiou, C. Cortical potentials with antisaccades. Electroencephalogr. Clin. Neurophysiol. 98, 377–384 (1996).

    Article  CAS  PubMed  Google Scholar 

  75. Klein, C., Heinks, T., Andresen, B., Berg, P. & Moritz, S. Impaired modulation of the saccadic contingent negative variation preceding antisaccades in schizophrenia. Biol. Psychiatry 47, 978–990 (2000).

    Article  CAS  PubMed  Google Scholar 

  76. Everling, S., Spantekow, A., Krappmann, P. & Flohr, H. Event-related potentials associated with correct and incorrect responses in a cued antisaccade task. Exp. Brain Res. 118, 27–34 (1998).

    Article  CAS  PubMed  Google Scholar 

  77. O'Driscoll, G. A. et al. Functional neuroanatomy of antisaccade eye movements investigated with positron emission tomography. Proc. Natl Acad. Sci. USA 92, 925–929 (1995).

    Article  CAS  PubMed  Google Scholar 

  78. Paus, T., Petrides, M., Evans, A. C. & Meyer, E. Role of the human anterior cingulate cortex in the control of oculomotor, manual, and speech responses: a positron emission tomography study. J. Neurophysiol. 70, 453–469 (1993).

    Article  CAS  PubMed  Google Scholar 

  79. Sweeney, J. A. et al. Positron emission tomography study of voluntary saccadic eye movements and spatial working memory. J. Neurophysiol. 75, 454–468 (1996).

    Article  CAS  PubMed  Google Scholar 

  80. Doricchi, F. et al. Neural control of fast-regular saccades and antisaccades: an investigation using positron emission tomography. Exp. Brain Res. 116, 50–62 (1997).

    Article  CAS  PubMed  Google Scholar 

  81. Connolly, J. D., Goodale, M. A., Desouza, J. F., Menon, R. S. & Vilis, T. A comparison of frontoparietal fMRI activation during anti-saccades and anti-pointing. J. Neurophysiol. 84, 1645–1655 (2000).

    Article  CAS  PubMed  Google Scholar 

  82. Connolly, J. D., Goodale, M. A., Menon, R. S. & Munoz, D. P. Human fMRI evidence for the neural correlates of preparatory set. Nature Neurosci. 5, 1345–1352 (2002). An important demonstration that frontal areas and not parietal areas carry preparatory signals for anti-saccades.

    Article  CAS  PubMed  Google Scholar 

  83. Desouza, J. F., Menon, R. S. & Everling, S. Preparatory set associated with pro-saccades and anti-saccades in humans investigated with event-related FMRI. J. Neurophysiol. 89, 1016–1023 (2003). Strong fMRI evidence that differences between pro-saccades and anti-saccades originate from differences in preparatory activity and not motor activity.

    Article  PubMed  Google Scholar 

  84. Curtis, C. E. & D'Esposito, M. Success and failure suppressing reflexive behavior. J. Cogn. Neurosci. 15, 409–418 (2003).

    Article  PubMed  Google Scholar 

  85. Leigh, R. J. & Kennard, C. Using saccades as a research tool in the clinical neurosciences. Brain 7 Nov 2003 (doi 10.1093/brain/awh035). A recent review covering the usefulness of saccadic motor tasks in clinical studies.

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

    Article  CAS  PubMed  Google Scholar 

  87. Fischer, B., Biscaldi, M. & Gezeck, S. On the development of voluntary and reflexive components in human saccade generation. Brain Res. 754, 285–297 (1997).

    Article  CAS  PubMed  Google Scholar 

  88. Luna, B. et al. Maturation of widely distributed brain function subserves cognitive development. Neuroimage 13, 786–793 (2001).

    Article  CAS  PubMed  Google Scholar 

  89. Klein, C. & Foerster, F. Development of prosaccade and antisaccade task performance in participants aged 6 to 26 years. Psychophysiology 38, 179–189 (2001).

    Article  CAS  PubMed  Google Scholar 

  90. Fukushima, J., Hatta, T. & Fukushima, K. Development of voluntary control of saccadic eye movements. I. Age-related changes in normal children. Brain Dev. 22, 173–180 (2000).

    Article  CAS  PubMed  Google Scholar 

  91. Fuster, J. M. The Prefrontal Cortex: Anatomy, Physiology, and Neuropsychology of the Frontal Lobe (Raven, New York, 1997).

    Google Scholar 

  92. Guitton, D., Buchtel, H. A. & Douglas, R. M. Frontal lobe lesions in man cause difficulties in suppressing reflexive glances and in generating goal-directed saccades. Exp. Brain Res. 58, 455–472 (1985). A seminal study showing that patients with frontal lobe lesions have high error rates in an anti-saccade task.

    Article  CAS  PubMed  Google Scholar 

  93. Pierrot-Deseilligny, C., Rivaud, S., Gaymard, B. & Agid, Y. Cortical control of reflexive visually-guided saccades. Brain 114, 1473–1485 (1991).

    Article  PubMed  Google Scholar 

  94. Pierrot-Deseilligny, C. et al. Decisional role of the dorsolateral prefrontal cortex in ocular motor behaviour. Brain 126, 1460–1473 (2003).

    Article  CAS  PubMed  Google Scholar 

  95. Walker, R., Husain, M., Hodgson, T. L., Harrison, J. & Kennard, C. Saccadic eye movement and working memory deficits following damage to human prefrontal cortex. Neuropsychologia 36, 1141–1159 (1998).

    Article  CAS  PubMed  Google Scholar 

  96. Pierrot-Deseilligny, C., Ploner, C. J., Muri, R. M., Gaymard, B. & Rivaud-Pechoux, S. Effects of cortical lesions on saccadic eye movements in humans. Ann. NY Acad. Sci. 956, 216–229 (2002).

    Article  PubMed  Google Scholar 

  97. Gaymard, B., Ploner, C. J., Rivaud, S., Vermersch, A. I. & Pierrot-Deseilligny, C. Cortical control of saccades. Exp. Brain Res. 123, 159–163 (1998).

    Article  CAS  PubMed  Google Scholar 

  98. Gaymard, B., Ploner, C. J., Rivaud-Pechoux, S. & Pierrot-Deseilligny, C. The frontal eye field is involved in spatial short-term memory but not in reflexive saccade inhibition. Exp. Brain Res. 129, 288–301 (1999).

    Article  CAS  PubMed  Google Scholar 

  99. Davidson, M. C., Everling, S. L. A. & Munoz, D. P. Comparison of pro- and anti-saccades in primates. III. Reversible activation/inactivation of frontal eye field and superior colliculus. Soc. Neurosci. Abstr. 25, 147.9 (1999).

    Google Scholar 

  100. Broerse, A., Crawford, T. J. & den Boer, J. A. Parsing cognition in schizophrenia using saccadic eye movements: a selective overview. Neuropsychologia 39, 742–756 (2001).

    Article  CAS  PubMed  Google Scholar 

  101. Crawford, T. J., Haeger, B., Kennard, C., Reveley, M. A. & Henderson, L. Saccadic abnormalities in psychotic patients. I. Neuroleptic-free psychotic patients. Psychol. Med. 25, 461–471 (1995).

    Article  CAS  PubMed  Google Scholar 

  102. Crawford, T. J. et al. Abnormal saccadic distractibility in patients with schizophrenia: a 99mTc-HMPAO SPET study. Psychol. Med. 26, 265–277 (1996).

    Article  CAS  PubMed  Google Scholar 

  103. Rosse, R. B., Schwartz, B. L., Kim, S. Y. & Deutsch, S. I. Correlation between antisaccade and Wisconsin Card Sorting Test performance in schizophrenia. Am. J. Psychiatry 150, 333–335 (1993).

    Article  CAS  PubMed  Google Scholar 

  104. McDowell, J. E. et al. Neural correlates of refixation saccades and antisaccades in normal and schizophrenia subjects. Biol. Psychiatry 51, 216–223 (2002).

    Article  PubMed  Google Scholar 

  105. Barkley, R. A. Behavioral inhibition, sustained attention, and executive functions: constructing a unifying theory of ADHD. Psychol. Bull. 121, 65–94 (1997).

    Article  PubMed  Google Scholar 

  106. Munoz, D. P., Armstrong, I. T., Hampton, K. A. & Moore, K. D. Altered control of visual fixation and saccadic eye movements in attention-deficit hyperactivity disorder. J. Neurophysiol. 90, 503–514 (2003).

    Article  PubMed  Google Scholar 

  107. Lezak, M. D. Neuropsychological Assessment (Oxford Univ. Press, Oxford, 1995).

    Google Scholar 

  108. Chan, F., Armstrong, I. T., Pari, G., Riopelle, R. J. & Munoz, D. P. Saccadic eye movement tasks reveal deficits in automatic response inhibition in Parkinson's disease. Neuropsychologia (in the press).

  109. Chen, Y. F., Chen, T. & Tsai, T. T. Analysis of volition latency on antisaccadic eye movements. Med. Eng. Phys. 21, 555–562 (1999).

    Article  CAS  PubMed  Google Scholar 

  110. Briand, K. A., Strallow, D., Hening, W., Poizner, H. & Sereno, A. B. Control of voluntary and reflexive saccades in Parkinson's disease. Exp. Brain Res. 129, 38–48 (1999).

    Article  CAS  PubMed  Google Scholar 

  111. Fukushima, J., Fukushima, K., Miyasaka, K. & Yamashita, I. Voluntary control of saccadic eye movement in patients with frontal cortical lesions and parkinsonian patients in comparison with that in schizophrenics. Biol. Psychiatry 36, 21–30 (1994).

    Article  CAS  PubMed  Google Scholar 

  112. Vidailhet, M. et al. Eye movements in parkinsonian syndromes. Ann. Neurol. 35, 420–426 (1994).

    Article  CAS  PubMed  Google Scholar 

  113. LeVasseur, A. L., Flanagan, J. R., Riopelle, R. J. & Munoz, D. P. Control of volitional and reflexive saccades in Tourette's syndrome. Brain 124, 2045–2058 (2001).

    Article  CAS  PubMed  Google Scholar 

  114. Leigh, R. & Zee, D. The Neurology of Eye Movements (Oxford Univ. Press, Oxford, 1999).

    Google Scholar 

  115. Sparks, D. L. The brainstem control of saccadic eye movements. Nature Rev. Neurosci. 3, 952–964 (2002).

    Article  CAS  Google Scholar 

  116. Wurtz, R. H. & Goldberg, M. E. The Neurobiology of Saccadic Eye Movements (Elsevier, Amsterdam, 1989).

    Google Scholar 

  117. Maunsell, J. H. & Newsome, W. T. Visual processing in monkey extrastriate cortex. Annu. Rev. Neurosci. 10, 363–401 (1987).

    Article  CAS  PubMed  Google Scholar 

  118. Andersen, R. A. Multimodal integration for the representation of space in the posterior parietal cortex. Philos. Trans. R. Soc. Lond. B 352, 1421–1428 (1997).

    Article  CAS  Google Scholar 

  119. Colby, C. L. & Goldberg, M. E. Space and attention in parietal cortex. Annu. Rev. Neurosci. 22, 319–349 (1999).

    Article  CAS  PubMed  Google Scholar 

  120. Pare, M. & Wurtz, R. H. Progression in neuronal processing for saccadic eye movements from parietal cortex area LIP to superior colliculus. J. Neurophysiol. 85, 2545–2562 (2001).

    Article  CAS  PubMed  Google Scholar 

  121. Ferraina, S., Pare, M. & Wurtz, R. H. Comparison of cortico-cortical and cortico-collicular signals for the generation of saccadic eye movements. J. Neurophysiol. 87, 845–858 (2002).

    Article  PubMed  Google Scholar 

  122. Schall, J. D. Visuomotor areas of the frontal lobe. Cereb. Cortex 12, 527–638 (1997). A comprehensive review of the possible roles of different areas in the frontal lobe in visually guided movements.

    Article  Google Scholar 

  123. Dias, E. C. & Segraves, M. A. Muscimol-induced inactivation of monkey frontal eye field: effects on visually and memory-guided saccades. J. Neurophysiol. 81, 2191–2214 (1999).

    Article  CAS  PubMed  Google Scholar 

  124. Rivaud, S., Muri, R. M., Gaymard, B., Vermersch, A. I. & Pierrot-Deseilligny, C. Eye movement disorders after frontal eye field lesions in humans. Exp. Brain Res. 102, 110–120 (1994).

    Article  CAS  PubMed  Google Scholar 

  125. Sommer, M. A. & Tehovnik, E. J. Reversible inactivation of macaque frontal eye field. Exp. Brain Res. 116, 229–249 (1997).

    Article  CAS  PubMed  Google Scholar 

  126. Coe, B., Tomihara, K., Matsuzawa, M. & Hikosaka, O. Visual and anticipatory bias in three cortical eye fields of the monkey during an adaptive decision-making task. J. Neurosci. 22, 5081–5090 (2002).

    Article  CAS  PubMed  Google Scholar 

  127. Stuphorn, V., Taylor, T. L. & Schall, J. D. Performance monitoring by the supplementary eye field. Nature 408, 857–860 (2000).

    Article  CAS  PubMed  Google Scholar 

  128. Segraves, M. A. & Goldberg, M. E. Functional properties of corticotectal neurons in the monkey's frontal eye field. J. Neurophysiol. 58, 1387–1419 (1987).

    Article  CAS  PubMed  Google Scholar 

  129. Sommer, M. A. & Wurtz, R. H. Composition and topographic organization of signals sent from the frontal eye field to the superior colliculus. J. Neurophysiol. 83, 1979–2001 (2000).

    Article  CAS  PubMed  Google Scholar 

  130. Stanton, G. B., Goldberg, M. E. & Bruce, C. J. Frontal eye field efferents in the macaque monkey: II. Topography of terminal fields in midbrain and pons. J. Comp Neurol. 271, 493–506 (1988).

    Article  CAS  PubMed  Google Scholar 

  131. Munoz, D. P., Dorris, M. C., Pare, M. & Everling, S. On your mark, get set: brainstem circuitry underlying saccadic initiation. Can. J. Physiol. Pharmacol. 78, 934–944 (2000).

    Article  CAS  PubMed  Google Scholar 

  132. Gandhi, N. J. & Keller, E. L. Spatial distribution and discharge characteristics of superior colliculus neurons antidromically activated from the omnipause region in monkey. J. Neurophysiol. 78, 2221–2225 (1997).

    Article  CAS  PubMed  Google Scholar 

  133. Segraves, M. A. Activity of monkey frontal eye field neurons projecting to oculomotor regions of the pons. J. Neurophysiol. 68, 1967–1985 (1992).

    Article  CAS  PubMed  Google Scholar 

  134. Alexander, G. E., DeLong, M. R. & Strick, P. L. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu. Rev. Neurosci. 9, 357–381 (1986).

    Article  CAS  PubMed  Google Scholar 

  135. Nakahara, H., Doya, K. & Hikosaka, O. Parallel cortico-basal ganglia mechanisms for acquisition and execution of visuomotor sequences — a computational approach. J. Cogn. Neurosci. 13, 626–647 (2001).

    Article  CAS  PubMed  Google Scholar 

  136. Hallett, M. Physiology of basal ganglia disorders: an overview. Can. J. Neurol. Sci. 20, 177–183 (1993).

    Article  CAS  PubMed  Google Scholar 

  137. Kornblum, S., Hasbroucq, T. & Osman, A. Dimensional overlap: cognitive basis for stimulus-response compatibility — a model and taxonomy. Psychol. Rev. 97, 253–270 (1990).

    Article  CAS  PubMed  Google Scholar 

  138. Wise, S. P. & Murray, E. A. Arbitrary associations between antecedents and actions. Trends Neurosci. 23, 271–276 (2000).

    Article  CAS  PubMed  Google Scholar 

  139. Duncan, J. in Attention and Performance VI (ed. Dornic, S.) 49–61 (Erlbaum, Hillsdale, New Jersey, 1977).

    Google Scholar 

  140. Hommel, B. & Prinz, W. Theoretical Issues in Stimulus-Response Compatibility (Elsevier, Amsterdam, Holland, 1997).

    Book  Google Scholar 

  141. Proctor, R. W. & Reeve, T. G. Stimulus-Response Compatibility: An Integrated Perspective (Elsevier, Amsterdam, Holland, 1990).

    Google Scholar 

  142. Simon, J. R. Reactions toward the source of stimulation. J. Exp. Psychol. 81, 174–176 (1969).

    Article  CAS  PubMed  Google Scholar 

  143. Simon, J. R. & Berbaum, K. Effect of conflicting cues on information processing: the 'Stroop effect' vs. the 'Simon effect'. Acta Psychol. (Amst.) 73, 159–170 (1990).

    Article  CAS  Google Scholar 

  144. Riehle, A., Kornblum, S. & Requin, J. Neuronal coding of stimulus-response association rules in the motor cortex. Neuroreport 5, 2462–2464 (1994).

    Article  CAS  PubMed  Google Scholar 

  145. Zhang, J., Riehle, A., Requin, J. & Kornblum, S. Dynamics of single neuron activity in monkey primary motor cortex related to sensorimotor transformation. J. Neurosci. 17, 2227–2246 (1997).

    Article  CAS  PubMed  Google Scholar 

  146. Crammond, D. J. & Kalaska, J. F. Modulation of preparatory neuronal activity in dorsal premotor cortex due to stimulus-response compatibility. J. Neurophysiol. 71, 1281–1284 (1994).

    Article  CAS  PubMed  Google Scholar 

  147. Stroop, J. R. Studies of interference in serial verbal reactions. J. Exp. Psychol. 18, 643–662 (1935).

    Article  Google Scholar 

  148. Glaser, M. O. & Glaser, W. R. Time course analysis of the Stroop phenomenon. J. Exp. Psychol. Hum. Percept. Perform. 8, 875–894 (1982).

    Article  CAS  PubMed  Google Scholar 

  149. MacLeod, C. M. Half a century of research on the Stroop effect: an integrative review. Psychol. Bull. 109, 163–203 (1991).

    Article  CAS  PubMed  Google Scholar 

  150. Eriksen, B. A. & Eriksen, C. W. Effects of noise letters upon the identification of a target letter in a nonsearch task. Percept. Psychophys. 16, 143–149 (1974).

    Article  Google Scholar 

Download references

Acknowledgements

D.P.M. is supported by the Canadian Institutes of Health Research and the Canada Research Chair Program. S.E. is supported by the National Alliance for Research on Schizophrenia and Depression, CIHR and the EJLB Foundation. J. Fecteau and J. Connolly commented on an earlier version of the manuscript.

Author information

Authors and Affiliations

  1. Department of Physiology, Centre for Neuroscience Studies, CIHR Group in Sensory Motor Systems, Queen's University, Kingston, K7L 3N6, Ontario, Canada

    Douglas P. Munoz

  2. Departments of Physiology & Pharmacology and Psychology, University of Western Ontario, London, N6A 5C1, Ontario, Canada

    Stefan Everling

  3. Robarts Research Institute, PO Box 5015, 100 Perth Drive, London, N6A 5K8, Ontario, Canada

    Stefan Everling

Authors
  1. Douglas P. Munoz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stefan Everling
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Douglas P. Munoz.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Related links

Related links

DATABASES

OMIM

attention-deficit hyperactivity disorder

Parkinson disease

schizophrenia

Tourette's syndrome

Glossary

SACCADIC EYE MOVEMENT

A rapid eye movement (with speeds of up to 800 degrees per second) that brings the point of maximal visual acuity — the fovea — to the image of interest.

VISUAL GRASP REFLEX

Flexive orienting response towards a novel visual stimulus.

FRONTAL EYE FIELD

An area in the frontal lobe that receives visual inputs and produces movements of the eye.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Munoz, D., Everling, S. Look away: the anti-saccade task and the voluntary control of eye movement. Nat Rev Neurosci 5, 218–228 (2004). https://doi.org/10.1038/nrn1345

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrn1345

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing