Skip to main content
Log in

Involuntary inhibition of movement initiation alters oculomotor competition resolution

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Identifying a stimulus as the target for a goal-directed movement involves inhibiting competing responses. Separable inhibitory interconnections bias local competition to ensure only one stimulus is selected and to alter movement initiation. Behavioural evidence of these inhibitory processes comes from the effects of distracters on oculomotor landing positions and saccade latencies. Here, we investigate the relationship between these two sources of inhibition. Targets were presented with or without close and remote distracters. In separate experiments the possible position and identity of the target and distracters were manipulated. In all cases saccade landing position was found to be less affected by the presence of the close distracter when remote distracters were also present. The involuntary increase in the latency of saccade initiation caused by the presence of the remote distracters alters the state of competitive processes involved in selecting the saccade target thus changing its landing position.

This is a preview of subscription content, log in via an institution to check access.

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Notes

  1. Main effect of target distance (F 1,12 = 7.1, p < 0.05); interaction between target distance and experiment (F 1,12 = 9.2, p < 0.05) and an interaction between global distracter and target distance (F 1,12 = 8.32, p < 0.05). These stem from latencies elicited to near targets. Latencies are longer for near targets in experiment 2b and over both experiments the presence of the ipsilateral distractor reduced saccade latency to the near target but not those to the far target. It is unclear what could be underlying this effect, but it has no bearing on the current investigation.

References

  • Allport A (1993) Attention and Control: have we been asking the wrong questions—a critical review of the last twenty-five years. In: Meyer DE, Kornblum S (eds) Attention and performance XIV: a silver jubilee. MIT, Cambridge, pp 183–218

    Google Scholar 

  • Bruce CJ, Goldberg ME (1985) Primate frontal eye fields. I. Single neurons discharging before saccades. J Neurophysiol 53(3):603–635

    Google Scholar 

  • Chou IH, Sommer MA, Schiller PH (1999) Express averaging saccades in monkeys. Vision Res 39:4200–4216

    Article  PubMed  CAS  Google Scholar 

  • Coëffé C, O’Regan JK (1987) Reducing the influence of non-target stimuli on saccade accuracy: predictability and latency effects. Vision Res 27:227–240

    Article  PubMed  Google Scholar 

  • Desimone R, Duncan J (1995) Neural mechanisms of selective visual attention. Ann Rev Neurosci 18:193–222

    Article  PubMed  CAS  Google Scholar 

  • Deubel H, Wolf W, Hauske M (1984) The evaluation of the oculomotor error signal. In: Gale AG, Johnson FW (eds) Theoretical and applied aspects of oculomotor research. Elsevier, Amsterdam, pp 55–62

    Google Scholar 

  • Findlay JM (1981) Local and global influences on saccadic eye movements. In: Fisher DF, Monty RA, Senders JW (eds) Eye movements, cognition and visual perception. Lawrence Erlbaum, Hillsdale, pp 171–179

    Google Scholar 

  • Findlay JM (1982) Global processing for saccadic eye movements. Vision Res 22:1033–1045

    Article  PubMed  CAS  Google Scholar 

  • Findlay JM, Brown V (2006) Eye scanning of multi-element displays: Ii. Saccade planning. Vision Res 46:216–227

    Article  PubMed  Google Scholar 

  • Findlay JM, Walker R (1999) A model of saccadic eye movement generation based on parallel processing and competitive inhibition. Behav Brain Sci 22:661–721

    PubMed  CAS  Google Scholar 

  • Gandhi NJ, Keller EL (1995) Interrupting saccades by electrical stimulation of the superior colliculus determines an extended fixation zone. Soc Neurosci Abstr 21:1193

    Google Scholar 

  • Glimcher PW, Sparks DL (1993) Representation of averaging saccades in the superior colliculus of the monkey. Exp Brain Res 95:429–435

    Article  PubMed  CAS  Google Scholar 

  • Godijn R, Theeuwes J (2002) Parallel programming of saccades: evidence for a competitive inhibition model. J Exp Psychol Hum Percept Perform 28:1039–1054

    Article  PubMed  Google Scholar 

  • Goldberg ME, Bisley JW, Powell KD, Gottlieb J (2006) Saccades, salience and attention: the role of the lateral intraparietal area in visual behavior. ProgBrain Res 155:157–175

    Google Scholar 

  • Hanes DP, Schall JD (1996) Neural control of voluntary movement initiation. Science 274:427–430

    Article  PubMed  CAS  Google Scholar 

  • Hikosaka O (1989) Role of basal ganglia in initiation of voluntary movements. In: Arbib MA, Amari S (eds) Dynamic interactions in neural networks: models and data. Springer-Verlag, New York, pp 153–167

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Honda H (2005) The remote distracter effect of saccade latencies in fixation-offset and overlap conditions. Vision Research 45:2773–2779

    Article  PubMed  Google Scholar 

  • Kopecz K (1995) Saccadic reaction time in gap/overlap paradigm: a model based on integration of intentional and visual information on neural, dynamic fields. Vision Res 35:2911–2925

    Article  PubMed  CAS  Google Scholar 

  • Lee P, Hall WC (2006) An in vitro study of horizontal connections in the intermediate layer of the superior colliculus. J Neurosci 26:4763–4768

    Article  PubMed  CAS  Google Scholar 

  • Lee C, Rohrer WH, Sparks DL (1988) Population coding of saccadic eye movements by neurons in the superior colliculus. Nature 332:357–360

    Article  PubMed  CAS  Google Scholar 

  • Ludwig CJH, Gilchrist ID (2003) Target similarity affects saccade curvature away from irrelevant onsets. Exp Brain Res 152:60–69

    Article  PubMed  Google Scholar 

  • Ludwig CJ, Mildinhall JW, Gilchrist ID (2007) A population coding account for systematic variation in saccadic dead time. J Neurophysiol 97:795–805

    Article  PubMed  Google Scholar 

  • McIlwain JT (1986) Point images in the visual system: New interest in an old idea. Trends Neurosci 9:354–358

    Article  Google Scholar 

  • McIlwain JT (1991) Distributed spatial coding in the superior colliculus: a review. Vis Neurosci 6:3–13

    Article  PubMed  CAS  Google Scholar 

  • McPeek RM (2006) Incomplete suppression of distracter-related activity in the frontal eye field results in curved saccades. J Neurophysiol 96:2699–2711

    Article  PubMed  Google Scholar 

  • McPeek RM, Han JH, Keller EL (2003) Competition between saccade goals in the superior colliculus produces saccade curvature. J Neurophysiol 89:2577–2590

    Article  PubMed  Google Scholar 

  • McSorley E, Findlay JM (2003) Saccade target selection in visual search: accuracy improves when more distracters are present. J Vis 3:877–892

    PubMed  Google Scholar 

  • McSorley E, Haggard P, Walker R (2006) Time-course of oculomotor inhibition revealed by saccade trajectory modulation. J Neurophysiol 96:1420–1424

    Article  PubMed  Google Scholar 

  • Munoz DP, Istvan PJ (1998) Lateral inhibitory interactions in the intermediate layers of the monkey superior colliculus. J Neurophysiol 79:1193–1209

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Munoz DP, Wurtz RH (1995a) Saccade-related activity in monkey superior colliculus 1: characteristics of burst and buildup cells. J Neurophysiol 73:2313–2333

    PubMed  CAS  Google Scholar 

  • Munoz DP, Wurtz RH (1995b) Saccade-related activity in monkey superior colliculus 2. Spread of activity during saccades. J Neurophysiol 73:2334–2348

    PubMed  CAS  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 distracter effect. Behav Brain Sci 22:694–695

    Article  Google Scholar 

  • Ottes FP, Van Gisbergen JAM, Eggermont JJ (1984) Metrics of saccade responses to visual double stimuli: two different modes. Vision Res 24(10):1169–1179

    Google Scholar 

  • Ottes FP, Van Gisbergen JAM, Eggermont JJ (1985) Latency dependence of colour-based target vs nontarget discrimination by the saccadic system. Vision Res 25:849–862

    Article  PubMed  CAS  Google Scholar 

  • Port NL, Wurtz RH (2003) Sequential activity of simultaneously recorded neurons in the superior colliculus during curved saccades. J Neurophysiol 90:1887–1903

    Article  PubMed  Google Scholar 

  • Ratcliff R, Hasegawa YT, Hasegawa YP, Smith PL, Segraves MA (2007) Dual diffusion model for single-cell recording data from the superior colliculus in a brightness-discrimination task. J Neurophysiol 97:1756–1774

    Article  PubMed  Google Scholar 

  • Schall JD, Thompson KG (1999) Neural selection and control of visually guided eye movements. Ann Rev Neurosci 22:241–259

    Article  PubMed  CAS  Google Scholar 

  • Sommer MA, Wurtz RH (2004a) What the brain stem tells the frontal cortex. I. Oculomotor signals sent from superior colliculus to frontal eye field via mediodorsal thalamus. J Neurophysiol 91:1381–1402

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Trappenberg TP, Dorris MC, Munoz DP, Klein RM (2001) A model of saccade initiation based on the competitive integration of exogenous and endogenous signals in the superior colliculus. J Cognitive Neurosci 13:256–271

    Article  CAS  Google Scholar 

  • van Opstal AJ, van Gisbergen JAM (1989) A nonlinear model for collicular spatial interactions underlying the metrical properties of electrically elicited saccades. Bio Cybern 60:171–183

    Article  Google Scholar 

  • Walker R, Kentridge RW, Findlay JM (1995) Independent contributions of the orienting of attention, fixation offset and bilateral stimulation on human saccadic latencies. Exp Brain Res 103:294–310

    Article  PubMed  CAS  Google Scholar 

  • Walker R, Deubel H, Schneider WX, Findlay JM (1997) Effect of remote distracters on saccade programming: Evidence for an extended fixation zone. J Neurophysiol 78:1108–1119

    PubMed  CAS  Google Scholar 

  • Wurtz RH, Sommer MA (2004) Identifying corollary discharges for movement in the primate brain. Prog Brain Res 144:47–60

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The work was funded by a grant from the Engineering and Physical Sciences Research Council (awarded to E.M.). Thanks to Casimir Ludwig and an anonymous reviewer for helpful comments.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alice G. Cruickshank.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cruickshank, A.G., McSorley, E. Involuntary inhibition of movement initiation alters oculomotor competition resolution. Exp Brain Res 193, 467–476 (2009). https://doi.org/10.1007/s00221-008-1645-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-008-1645-9

Keywords

Navigation