Skip to main content
SpringerLink
Log in

Sensory and motor mechanisms of oculomotor inhibition of return

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

Abstract

We propose two explicit mechanisms contributing to oculomotor inhibition of return (IOR): sensory and motor. Sensory mechanism: repeated visual stimulation results in a reduction in visual input to the superior colliculus (SC); consequently, saccades to targets that appear at previously stimulated retinotopic locations will have longer latencies than those that appear at unstimulated locations. Motor mechanism: the execution of a saccade results in asymmetric activation in the SC; as a result, saccades that reverse vectors will have longer latencies than those that repeat vectors. In the IOR literature, these two mechanisms correspond to IOR effects observed following covert exogenous orienting and overt endogenous orienting, respectively. We predict that these two independent mechanisms will have additive effects, a prediction that is confirmed in a behavioral experiment. We then discuss how our theory and findings relate to the oculomotor IOR literature.

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

Access this article

Log in via an institution

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
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Notes

  1. Human electrophysiological (EEG) studies also showed that target-elicited early visual ERP components (P1 and N1) are reduced for cued targets (see Prime and Ward 2006, for a review). Reduced BOLD signal to cued targets has also been observed in human visual cortex (e.g., Anderson and Rees 2011).

  2. One could always use two differential equations to approximate this input reduction, but we chose to use the alpha function for simplicity.

  3. One might suggest that this mechanism should not be regarded as a contributor to IOR because the forward facilitation it generates (saccade momentum) causes a disadvantage for return saccades. Although such a suggestion has merit, so too does our maintenance of the IOR terminology. Our previous modeling papers (Satel et al. 2011; Wang et al. 2011) have addressed two extreme situations where the behavioral effects had been, by convention in the field, labeled as IOR: (1) covert orienting where IOR is elicited by uninformative peripheral cues while the participant maintains fixation until target presentation; (2) overt orienting where IOR is used to label longer latencies for saccades returning to previously fixated locations (e.g., Klein and MacInnes 1999). We prefer to continue to use “IOR” to label both cases because we are following the “convention” in the field where IOR is used to loosely refer to a set of processes that facilitate orienting to novelty. The importance of our contribution rests not on terminology but on the computationally explicit nature of the sensory and motor mechanisms we have proposed to implement these processes.

  4. Readers may be surprised that the saccade back to the central fixation was no slower than the one to the peripheral box (in response to the cue) in the M task. It should be noted that unlike saccades to the targets of which the direction was unpredictable, saccades made in response to the cue-back signal were always directed to the central box.

  5. Although the conceptual underpinning seems quite different (rooted as it is in the notion of cue-target integration) Lupianez’s proposal of a cue-induced “onset detection cost” (Lupiáñez 2010; see also Hu et al. 2011) shares quite a few properties with this suppression effect that is fundamental to our sensory mechanism.

References

  • Abrams RA, Dobkin RS (1994) Inhibition of return: effects of attentional cueing on eye movement latencies. J Exp Psychol Hum Percept Perform 20:467–477

    Article  PubMed  CAS  Google Scholar 

  • Amari S (1977) Dynamics of pattern formation in lateral-inhibition type neural fields. Biol Cybern 27:77–87

    Article  PubMed  CAS  Google Scholar 

  • Anderson EJ, Rees G (2011) Neural correlates of spatial orienting in the human superior colliculus. J Neurophysiol 106:2273–2284

    Article  PubMed  Google Scholar 

  • Bell AH, Munoz DP (2008) Activity in the superior colliculus reflects dynamic interactions between voluntary and involuntary influences on orienting behaviour. Eur J Neurosci 28:1654–1660

    Article  PubMed  Google Scholar 

  • Bell AH, Fecteau JH, Munoz DP (2004) Using auditory and visual stimuli to investigate the behavioral and neuronal consequences of reflexive covert orienting. J Neurophysiol 91:2172–2184

    Article  PubMed  Google Scholar 

  • Berlucchi G (2006) Inhibition of return: a phenomenon in search of a mechanism and a better name. Cogn Neuropsychol 23:1065–1074

    Article  PubMed  Google Scholar 

  • Dodd MD, Van der Stigchel S, Hollingworth A (2009) Novelty is not always the best policy: inhibition of return and facilitation of return as a function of visual task. Psychol Sci 20:333–339

    Article  PubMed  Google Scholar 

  • Dorris MC, Taylor TL, Klein RM, Munoz DP (1999) Influence of previous visual stimulus or saccade on saccadic reaction times in monkey. J Neurophysiol 81:2429–2436

    PubMed  CAS  Google Scholar 

  • Dorris MC, Klein RM, Everling S, Munoz DP (2002) Contribution of the primate superior colliculus to inhibition of return. J Cogn Neurosci 14:1256–1263

    Article  PubMed  Google Scholar 

  • Dorris MC, Olivier E, Munoz DP (2007) Competitive integration of visual and preparatory signals in the superior colliculus during saccadic programming. Journal Neurosci 27:5053–5062

    Article  CAS  Google Scholar 

  • Dukewich KR (2009) Reconceptualizing inhibition of return as habituation of the orienting response. Psychon Bull Rev 16:238–251

    Article  PubMed  Google Scholar 

  • Fecteau JH, Munoz DP (2005) Correlates of capture of attention and inhibition of return across stages of visual processing. J Cogn Neurosci 17:1714–1727

    Article  PubMed  Google Scholar 

  • Fecteau JH, Munoz DP (2006) Salience, relevance, and firing: a priority map for target selection. Trends Cogn Sci 10:382–390

    Article  PubMed  Google Scholar 

  • Fecteau JH, Bell AH, Munoz DP (2004) Neural correlates of the automatic and goal-driven biases in orienting spatial attention. J Neurophysiol 92:1728–1737

    Article  PubMed  Google Scholar 

  • Gore JL, Dorris MC, Munoz DP (2002) Time course of a repetition effect on saccadic reaction time in non-human primates. Arch Ital Biol 140:203–210

    PubMed  CAS  Google Scholar 

  • Hilchey M, Klein RM, Ivanoff J (2011) In: Annual meeting of vision sciences society. Perceptual and motor IOR: components or flavours? Naples, Florida

  • Hooge ITC, Frens MA (2000) Inhibition of saccade return (ISR): spatio-temporal properties of saccade programming. Vis Res 40:3415–3426

    Article  PubMed  CAS  Google Scholar 

  • Hooge ITC, Over EAB, van Wezel RJA, Frens MA (2005) Inhibition of return is not a foraging facilitator in saccadic search and free viewing. Vis Res 45:1901–1908

    Article  PubMed  Google Scholar 

  • Hu FK, Samuel AG, Chan AS (2011) Eliminating inhibition of return by changing salient nonspatial attributes in a complex environment. J Exp Psychol Gen 140:35–50

    Article  PubMed  Google Scholar 

  • Huber DE (2008) Immediate priming and cognitive aftereffects. J Exp Psychol Gen 137:324–347

    Article  PubMed  Google Scholar 

  • Klein R (1988) Inhibitory tagging system facilitates visual search. Nature 334:430–431

    Article  PubMed  CAS  Google Scholar 

  • Klein RM, Hilchey M (2011) Oculomotor inhibition of return. In: Liversedge S, Gilchrist I, Everling S (eds) The Oxford handbook of eye movements. Oxford University Press, London, pp 471–492

    Google Scholar 

  • Klein RM, Macinnes JW (1999) Inhibition of return is a foraging facilitator in visual search. Psychol Sci 10:346–352

    Article  Google Scholar 

  • Klein RM, Taylor T (1994) Categories of cognitive inhibition with reference to attention. In: Dagenbach D, Carr TH (eds) Inhibitory processes in attention, memory and language. Academic Press, New York, pp 113–150

    Google Scholar 

  • Klein RM, Munoz DP, Dorris MC, Taylor TL (1998) Inhibition of return in monkey and man. Unpublished manuscript

  • Lupiáñez J (2010) Inhibition of return. In: Nobre K, Coull JT (eds) Attention and time. Oxford University Press, Cambridge, pp 17–34

    Chapter  Google Scholar 

  • Macinnes JW, Klein RM (2003) Inhibition of return biases orienting during the search of complex scenes. Sci World J 3:75–86

    Article  Google Scholar 

  • Masson MEJ, Loftus GR (2003) Using confidence intervals for graphically based data interpretation. Can J Exp Psychol 57:203–220

    Article  PubMed  Google Scholar 

  • Mathôt S, Theeuwes J (2011) Gradual remapping results in early retinotopic and late spatiotopic inhibition of return. Psychol Sci 21:1793–1798

    Article  Google Scholar 

  • Maylor EA, Hockey R (1985) Inhibitory component of externally controlled covert orienting in visual space. J Exp Psychol Hum Percept Perform 11:777–787

    Article  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. I. 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. II. Spread of activity during saccades. J Neurophysiol 73:2334–2348

    PubMed  CAS  Google Scholar 

  • Munoz DP, Fecteau JH, J. Hyona DPM (2002) In: The Brain’s eye: Neurobiological and clinical aspects of oculomotor research. Vying for dominance: dynamic interactions control visual fixation and saccadic initiation in the superior colliculus. Elsevier, pp 3–19

  • Patel SS, Peng X, Sereno AB (2010) Shape effects on reflexive spatial selective attention and a plausible neurophysiological model. Vis Res 50:1235–1248

    Article  PubMed  Google Scholar 

  • Pertzov Y, Zohary E, Avidan G (2011) Rapid formation of spatiotopic representations as revealed by inhibition of return. J Neurosci 30:8882–8887

    Article  Google Scholar 

  • Posner MI, Cohen Y (1984) Components of visual orienting. In: Bouma H, Bouwhuis DG (eds) Attention and performance. Erlbaum, Hillsdale, pp 531–556

    Google Scholar 

  • Posner MI, Rafal RD, Choate LS, Vaughan J (1985) Inhibition of return: neural basis and function. Cogn Neuropsychol 2:211–228

    Google Scholar 

  • Prime DJ, Ward LM (2006) Cortical expressions of inhibition of return. Brain Res 1072:161–174

    Article  PubMed  CAS  Google Scholar 

  • Rafal R, Egly R, Rhodes D (1994) Effects of inhibition of return on voluntary and visually guided saccades. Can J Exp Psychol 48:284–300

    Article  PubMed  CAS  Google Scholar 

  • Samuel AG, Kat D (2003) Inhibition of return: a graphical meta-analysis of its time course and an empirical test of its temporal and spatial properties. Psychon Bull Rev 10:897–906

    Article  PubMed  Google Scholar 

  • Satel J, Wang Z, Trappenberg TP, Klein RM (2011) Modeling inhibition of return as short-term depression of early sensory input to the superior colliculus. Vis Res 51:987–996

    Article  PubMed  CAS  Google Scholar 

  • Smith TJ, Henderson JM (2009) Facilitation of return during scene viewing. Vis Cogn 17:1083–1108

    Article  Google Scholar 

  • Smith TJ, Henderson JM (2011a) Does oculomotor inhibition of return influence fixation probability during scene search? Atten Percept Psychophys 73:2384–2398

    Article  PubMed  Google Scholar 

  • Smith TJ, Henderson JM (2011b) Looking back at Waldo: oculomotor inhibition of return does not prevent return fixations. J Vis 11(1):1–11, art no 3

    Google Scholar 

  • Snyder JJ, Kingstone A (2000) Inhibition of return and visual search: how many separate loci are inhibited? Percept Psychophys 62:452–458

    Article  PubMed  CAS  Google Scholar 

  • Sternberg S (1967) Two operations in character recognition: some evidence from reaction-time measurements. Percept Psychophys 2:45–53

    Article  Google Scholar 

  • Taylor TL, Klein RM (1998) On the causes and effects of inhibition of return. Psychon Bull Rev 5:625–643

    Article  Google Scholar 

  • Taylor TL, Klein RM (2000) Visual and motor effects in inhibition of return. J Exp Psychol Hum Percept Perform 26:1639–1656

    Article  PubMed  CAS  Google Scholar 

  • Tipper SP, Weaver B, Jerreat LM, Burak AL (1994) Object-based and environment-based inhibition of return of visual attention. J Exp Psychol Hum Percept Perform 20:478–499

    Article  PubMed  CAS  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 Cogn Neurosci 13:256–271

    Article  PubMed  CAS  Google Scholar 

  • Wang Z, Klein RM (2010) Searching for inhibition of return in visual search: a review. Vis Res 50:220–228

    Article  PubMed  Google Scholar 

  • Wang Z, Satel J, Trappenberg TP, Klein RM (2011) Aftereffects of saccades explored in a dynamic neural field model of the superior colliculus. J Eye Mov Res 4:1–16

    Google Scholar 

  • Watanabe K (2001) Inhibition of return in averaging saccades. Exp Brain Res 138:330–342

    Article  PubMed  CAS  Google Scholar 

  • Wilson HR, Cowan JD (1973) A mathematical theory of the functional dynamics of cortical and thalamic nervous tissue. Biol Cybern 13:55–80

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Juan Lupiáñez, Matthew Hilchey and two anonymous reviewers for their constructive comments and suggestions on an earlier version of this paper. Z. Wang was supported by China Scholarship Council (CSC); R. M. Klein was supported by Natural Sciences and Engineering Research Council of Canada (NSERC).

Author information

Authors and Affiliations

  1. Department of Psychology, Dalhousie University, Halifax, NS, B3H 4R2, Canada

    Zhiguo Wang & Raymond M. Klein

  2. Institute of Psychology, Chinese Academy of Sciences, Beijing, China

    Zhiguo Wang

  3. Faculty of Computer Science, Dalhousie University, Halifax, NS, B3H 4R2, Canada

    Jason Satel

Authors
  1. Zhiguo Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jason Satel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Raymond M. Klein
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Raymond M. Klein.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, Z., Satel, J. & Klein, R.M. Sensory and motor mechanisms of oculomotor inhibition of return. Exp Brain Res 218, 441–453 (2012). https://doi.org/10.1007/s00221-012-3033-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-012-3033-8

Keywords

Search

Navigation