Skip to main content

Disrupting saccadic updating: visual interference prior to the first saccade elicits spatial errors in the secondary saccade in a double-step task

Experimental Brain Research volume 233, pages 1893–1905 (2015)Cite this article

Abstract

When we explore the visual environment around us, we produce sequences of very precise eye movements aligning the objects of interest with the most sensitive part of the retina for detailed visual processing. A copy of the impending motor command, the corollary discharge, is sent as soon as the first saccade in a sequence is ready to monitor the next fixation location and correctly plan the subsequent eye movement. Neurophysiological investigations have shown that chemical interference with the corollary discharge generates a distinct pattern of spatial errors on sequential eye movements, with similar results also from clinical and TMS studies. Here, we used saccadic inhibition to interfere with the temporal domain of the first of two subsequent saccades during a standard double-step paradigm. In two experiments, we report that the temporal interference on the primary saccade led to a specific error in the final landing position of the second saccade that was consistent with previous lesion and neurophysiological studies, but without affecting the spatial characteristics of the first eye movement. On the other hand, single-step saccades were differently influence by the flash, with a general undershoot, more pronounced for larger saccadic amplitude. These findings show that a flashed visual transient can disrupt saccadic updating in a double-step task, possibly due to the mismatch between the planned and the executed saccadic eye movement.

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

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  • Atsma J, Maij F, Corneil BD, Medendorp P (2014) No evidence for peri-saccadic mislocalization on suddenly cancelled saccades. J Neurosci 34(16):5497–5504

    Article  CAS  PubMed  Google Scholar 

  • Bahcall D, Kowler E (1999) Illusory shifts in visual direction accompany adaptation of saccadic eye movements. Nature 400:864–866

    Article  CAS  PubMed  Google Scholar 

  • Becker W, Jürgens R (1979) An analysis of the saccadic system by means of double-step stimuli. Vis Res 19:967–983

    Article  CAS  PubMed  Google Scholar 

  • Benevento LA, Fallon JH (1975) The ascending projections of the superior colliculus in the rhesus monkey (Macaca mulatta). J Comp Neurol 160(3):339–361

    Article  CAS  PubMed  Google Scholar 

  • Bompas A, Sumner P (2011) Saccadic inhibition reveals the timing of automatic and voluntary signals in the human brain. J Neurosci 31:12501–12512

    Article  CAS  PubMed  Google Scholar 

  • Buonocore A, McIntosh RD (2008) Saccadic inhibition underlies the remote distractor effect. Exp Brain Res 191:117–122

    Article  PubMed  Google Scholar 

  • Buonocore A, McIntosh RD (2012) Modulation of saccadic inhibition by distractor size and location. Vis Res 69:32–41

    Article  PubMed  Google Scholar 

  • Buonocore A, McIntosh RD (2013) Attention modulates saccadic inhibition magnitude. Q J Exp Psychol (Hove) 66(6):1051–1059

    Article  Google Scholar 

  • Collins T, Rolfs M, Deubel H, Cavanagh P (2009) Post-saccadic location judgments reveal remapping of saccade targets to non-foveal locations. J Vis 9(5):29.1–29.9

    Article  Google Scholar 

  • Donaldson IM (2000) The functions of the proprioceptors of the eye muscles. Philos Trans R Soc Lond B Biol Sci 355(1404):1685–1754

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Duhamel JR, Goldberg ME, Fitzgibbon EJ, Sirigu A, Grafman J (1992) Saccadic dysmetria in a patient with a right frontoparietal lesion. The importance of corollary discharge for accurate spatial behaviour. Brain 115:1387–1402

    Article  PubMed  Google Scholar 

  • Edelman JA, Xu KZ (2009) Inhibition of voluntary saccadic eye movement commands by abrupt visual onsets. J Neurophysiol 101:1222–1234

    Article  PubMed Central  PubMed  Google Scholar 

  • Findlay JM, Walker R (1999) A model of saccade generation based on parallel processing and competitive inhibition. Behav Brain Sci 22:661–675

    CAS  PubMed  Google Scholar 

  • Goldman-Rakic PS, Porrino LJ (1985) The primate mediodorsal (MD) nucleus and its projection to the frontal lobe. J Comp Neurol 242:535–560

    Article  CAS  PubMed  Google Scholar 

  • Grantyn A (1989) How visual inputs to the ponto-bulbar reticular formation are used in the synthesis of premotor signals during orienting. Prog Brain Res 80:159–170

    Article  CAS  PubMed  Google Scholar 

  • Guillaume A (2012) Saccadic inhibition is accompanied by large and complex amplitude modulations when induced by visual backward masking. J Vis 12(6):5

    Article  PubMed  Google Scholar 

  • Guthrie BL, Porter JD, Sparks DL (1983) Corollary discharge provides accurate eye position information to the oculomotor system. Science 221:1193–1195

    Article  CAS  PubMed  Google Scholar 

  • Hamker FH, Zirnsak M, Ziesche A, Lappe M (2011) Computational models of spatial updating in peri-saccadic perception. Phil Trans R Soc B 366:554–571

    Article  PubMed Central  PubMed  Google Scholar 

  • Heide W, Blankenburg M, Zimmermann E, Kömpf D (1995) Cortical control of double-step saccades: implications for spatial orientation. Ann Neurol 38:739–748

    Article  CAS  PubMed  Google Scholar 

  • Joiner W, Fitzgibbon E, Wurtz R (2010) Amplitudes and directions of individual saccades can be adjusted by corollary discharge. J Vis 10(2):22.1–22.12

    Article  Google Scholar 

  • Katschmarsky S, Cairney S, Maruff P, Wilson PH, Currie J (2001) The ability to execute saccades on the basis of efference copy: impairments in double-step saccade performance in children with developmental co-ordination disorder. Exp Brain Res 136(1):73–78

    Article  CAS  PubMed  Google Scholar 

  • Lewis RF, Zee DS, Hayman MR, Tamargo RJ (2001) Oculomotor function in the rhesus monkey after deafferentation of the extraocular muscles. Exp Brain Res 141(3):349–358

    Article  CAS  PubMed  Google Scholar 

  • Lynch J, Hoover J, Strick P (1994) Input to the primate frontal eye field from the substantia nigra, superior colliculus, and dentate nucleus demonstrated by transneuronal transport. Exp Brain Res 100:181–186

    Article  CAS  PubMed  Google Scholar 

  • McIntosh RD, Buonocore A (2014) Saccadic inhibition can cause the remote distractor effect, but the remote distractor effect may not be a useful concept. J Vis 14(5):15

    Article  PubMed  Google Scholar 

  • Medendorp WP (2011) Spatial constancy mechanisms in motor control. Phil Trans R Soc Lond B Biol Sci 366:476–491

    Article  Google Scholar 

  • Melcher D (2007) Predictive remapping of visual features precedes saccadic eye movements. Nat Neurosci 10:903–907

    Article  CAS  PubMed  Google Scholar 

  • Melcher D (2011) Visual stability. Philos Trans R Soc Lond B Biol Sci 366:468–475

    Article  PubMed Central  PubMed  Google Scholar 

  • Melcher D, Colby CL (2008) Trans-saccadic perception. Trends Cogn Sci 12:466–473

    Article  PubMed  Google Scholar 

  • Melcher D, Morrone MC (2003) Spatiotopic integration of visual motion across saccadic eye movements. Nat Neurosci 6:877–881

    Article  CAS  PubMed  Google Scholar 

  • Morris AP, Chambers CD, Mattingley JB (2007) Parietal stimulation destabilizes spatial updating across saccadic eye movements. Proc Natl Acad Sci USA 104(21):9069–9074

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Munoz DP, Wurtz RH (1993a) Fixation cells in monkey superior colliculus. I. Characteristics of cell discharge. J Neurophysiol 70:559–575

    CAS  PubMed  Google Scholar 

  • Munoz DP, Wurtz RH (1993b) Fixation cells in monkey superior colliculus. II. Reversible activation and deactivation. J Neurophysiol 70:576–589

    CAS  PubMed  Google Scholar 

  • Olivier E, Dorris MC, Munoz DP (1999) Lateral interactions in the superior colliculus, not an extended fixation zone, can account for the remote distractor effects (Commentary on Findlay & Walker). Behav Brain Sci 22:694–695

    Article  Google Scholar 

  • Pisella L, Mattingley JB (2004) The contribution of spatial remapping impairments to unilateral visual neglect. Neurosci Biobehav Rev 28:181–200

    Article  PubMed  Google Scholar 

  • Poletti M, Burr DC, Rucci M (2013) Optimal multimodal integration in spatial localization. J Neurosci 33:14259–14268

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Proske U, Gandevia SC (2012) The proprioceptive senses: their roles in signalling body shape, body position and movement, and muscle force. Physiol Rev 92:1651–1697

    Article  CAS  PubMed  Google Scholar 

  • Reingold EM, Stampe DM (2002) Saccadic inhibition in voluntary and reflexive saccades. J Cogn Neurosci 14:371–388

    Article  PubMed  Google Scholar 

  • Rizzolatti G, Buchtel HA, Camarda R, Scandolara C (1980) Neurons with complex visual properties in the superior colliculus of the macaque monkey. Exp Brain Res 38(1):37–42

    Article  CAS  PubMed  Google Scholar 

  • Sommer MA, Wurtz RH (1998) Frontal eye field neurons orthodromically activated from the superior colliculus. J Neurophysiol 80:3331–3335

    CAS  PubMed  Google Scholar 

  • Sommer MA, Wurtz RH (2002) A pathway in primate brain for internal monitoring of movements. Science 296:1480–1482

    Article  CAS  PubMed  Google Scholar 

  • Sommer MA, Wurtz RH (2004) What the brainstem tells the frontal cortex. II. Role of the SC-MD-FEF pathway in corollary discharge. J Neurophysiol 91:1403–1423

    Article  PubMed  Google Scholar 

  • Sparks DL, Hartwich-Young R (1989) The deeper layers of the superior colliculus. In: Wurtz RH, Goldberg ME (eds) Rev Oculomotor Res. The neurobiology of saccadic eye movements. Elsevier Science Publishers, Amsterdam, pp 213–255

    Google Scholar 

  • Sperry RW (1950) Neural basis of the spontaneous optokinetic response produced by visual inversion. J Comp Physiol Psychol 43:482–489

    Article  CAS  PubMed  Google Scholar 

  • Walker R, McSorley E (2006) The parallel programming of voluntary and reflexive saccades. Vis Res 46(13):2082–2093

    Article  PubMed  Google Scholar 

  • Wurtz RH (2008) Neuronal mechanisms of visual stability. Vis Res 48:2070–2089

    Article  PubMed Central  PubMed  Google Scholar 

  • Wurtz RH, Joiner WM, Berman RA (2011) Neuronal mechanisms for visual stability: progress and problems. Philos Trans R Soc Lond B Biol Sci 366:492–503

    Article  PubMed Central  PubMed  Google Scholar 

  • Zimmermann E, Fink G, Cavanagh P (2013a) Perifoveal spatial compression. J Vis 13(21):1–9

    Google Scholar 

  • Zimmermann E, Morrone MC, Fink GR, Burr D (2013b) Spatiotopic neural representations develop slowly across saccades. Curr Biol 5:R193–R194

    Article  Google Scholar 

  • Zimmerman E, Born S, Fink GR, Cavanagh P (2014) Masking produces compression of space and time in the absence of eye movements. J Neurophysiol. doi:10.1152/jn.00156.2014

    Google Scholar 

Download references

Acknowledgments

This research was funded by a European Research Council Starting Grant award (Grant Agreement No. 313658) to D.M. and a research fellowship awarded to A.B. by the Comune di Rovereto.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

All procedures performed in studies involving human participants were in accordance with the ethical standards and the guidelines of the University of Trento Ethics Committee and with the 1964 Helsinki declaration and its later amendments. Informed consent was obtained from all individual participants included in the study.

Author information

Authors and Affiliations

  1. Department of Psychology and Cognitive Sciences, Center for Mind/Brain Sciences, University of Trento, 38068, Rovereto, Italy

    Antimo Buonocore & David Melcher

Authors
  1. Antimo Buonocore
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David Melcher
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Antimo Buonocore.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Buonocore, A., Melcher, D. Disrupting saccadic updating: visual interference prior to the first saccade elicits spatial errors in the secondary saccade in a double-step task. Exp Brain Res 233, 1893–1905 (2015). https://doi.org/10.1007/s00221-015-4261-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-015-4261-5

Keywords

  • Corollary discharge
  • Saccadic inhibition
  • Eye movements
  • Double-step saccade