Skip to main content
SpringerLink
Log in

Evidence for spatial tuning of movement inhibition

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

Abstract

The time to initiate a movement can, even implicitly, be influenced by the environment. All primates, including humans, respond faster and with greater accuracy to stimuli that are brighter, louder or associated with larger reward, than to neutral stimuli. Whether this environment also modulates the executive functions which allow ongoing actions to be suppressed remains an issue of debate. In this study, we investigated the implicit learning of spatial selectivity of movement inhibition in humans and macaque monkeys performing a saccade-countermanding task. The occurrence of stop trials, in which subjects were visually instructed to cancel a prepared movement, was manipulated according to the target location. One visual target was associated with higher probability of stop signal appearance (e.g., 80 %), while the second target was associated with low fraction of stop (e.g., 20 %). The absolute occurrence of stop trials across the two targets (50 %) remains constant. The results show that human and macaque monkeys can selectively adapt their behaviors according to the implicit probability of stopping. Behavioral adjustments were larger when targets were in different hemifields and for larger distances between targets. Reduced selective inhibitory behaviors were observed when 15° of visual angle separated the targets, and this effect vanished when targets were separated by only 2°. Overall, our study shows that both response and inhibition times can be modulated by the relative spatial occurrence of stop signals. We speculate that beyond the particular effect we observed in the context of the saccade paradigm, selective motor execution may imply a disinhibitory mechanism that modulates the motor pathways associated with the fronto-median cortex and basal ganglia circuits.

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

Similar content being viewed by others

References

  • Aron AR, Behrens TE, Smith S, Frank MJ, Poldrack RA (2007) Triangulating a cognitive control network using diffusion-weighted magnetic resonance imaging (MRI) and functional MRI. J Neurosci 27(14):3743–3752

    Article  CAS  PubMed  Google Scholar 

  • Awh E, Vogel EK, Oh SH (2006) Interactions between attention and working memory. Neuroscience 139(1):201–208

    Article  CAS  PubMed  Google Scholar 

  • Boucher L, Palmeri TJ, Logan GD, Schall JD (2007) Inhibitory control in mind and brain: an interactive race model of countermanding saccades. Psychol Rev 114(2):376–397

    Article  PubMed  Google Scholar 

  • Corneil BD, Cheng JC, Goonetilleke SC (2013) Dynamic and opposing adjustment of movement cancellation and generation in an oculomotor countermanding task. J Neurosci 12(33):9975–9984

    Article  Google Scholar 

  • Curtis CE (2006) Prefrontal and parietal contributions to spatial working memory. Neuroscience 139(1):173–180

    Article  CAS  PubMed  Google Scholar 

  • Curtis CE, Rao VY, D’Esposito M (2004) Maintenance of spatial and motor codes during oculomotor delayed response tasks. J Neurosci 24(16):3944–3952

    Article  CAS  PubMed  Google Scholar 

  • Curtis CE, Cole MW, Rao VY, D’Esposito M (2005) Canceling planned action: an FMRI study of countermanding saccades. Cereb Cortex 15(9):1281–1289

    Article  PubMed  Google Scholar 

  • Defelipe J, González-Albo MC, Del Río MR, Elston GN (1999) Distribution and patterns of connectivity of interneurons containing calbindin, calretinin, and parvalbumin in visual areas of the occipital and temporal lobes of the macaque monkey. J Comp Neurol 412(3):515–526

    Article  CAS  PubMed  Google Scholar 

  • Dhawan S, Deubel H, Jonikaitis D (2013) Inhibition of saccades elicits attentional suppression. J Vis 13(6):9. doi:10.1167/13.6.9

    Article  PubMed  Google Scholar 

  • Dimoska A, Johnstone SJ (2008) Effects of varying stop-signal probability on ERPs in the stop-signal task: do they reflect variations in inhibitory processing or simply novelty effects? Biol Psychol 77(3):324–336

    Article  PubMed  Google Scholar 

  • Dorris MC, Munoz DP (1998) Saccadic probability influences motor preparation signals and time to saccadic initiation. J Neurosci 18:7015–7026

    CAS  PubMed  Google Scholar 

  • Dorris MC, Paré M, Munoz DP (1997) Neuronal activity in monkey superior colliculus related to the initiation of saccadic eye movements. J Neurosci 17:8566–8579

    CAS  PubMed  Google Scholar 

  • Dorris MC, Paré M, Munoz DP (2000) Immediate neural plasticity shapes motor performance. J Neurosci 20:RC52

    CAS  PubMed  Google Scholar 

  • Emeric EE, Brown JW, Boucher L, Carpenter RH, Hanes DP, Harris R, Logan GD, Mashru RN, Paré M, Pouget P, Stuphorn V, Taylor TL, Schall JD (2007) Influence of history on saccade countermanding performance in humans and macaque monkeys. Vision Res 47(1):35–49

    Article  PubMed  PubMed Central  Google Scholar 

  • Everling S, Munoz DP (2000) Neuronal correlates for preparatory set associated with pro-saccades and anti-saccades in the primate frontal eye field. J Neurosci 20:387–400

    CAS  PubMed  Google Scholar 

  • Everling S, Dorris MC, Klein RM, Munoz DP (1999) Role of primate superior colliculus in preparation and execution of anti-saccades and pro-saccades. J Neurosci 19:2740–2754

    CAS  PubMed  Google Scholar 

  • Falkner AL, Krishna BS, Goldberg ME (2010) Surround suppression sharpens the priority map in the lateral intraparietal area. J Neurosci 30(38):12787–12797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hanes DP, Schall JD (1995) Countermanding saccades in macaque. Vis Neurosci 12:929–937

    Article  CAS  PubMed  Google Scholar 

  • Hanes DP, Schall JD (1996) Neural control of voluntary movement initiation. Science 274(5286):427–430

    Article  CAS  PubMed  Google Scholar 

  • Hanes DP, Patterson WF 2nd, Schall JD (1998) Role of frontal eye fields in countermanding saccades: visual, movement, and fixation activity. J Neurophysiol 79(2):817–834

    CAS  PubMed  Google Scholar 

  • Hasegawa RP, Peterson BW, Goldberg ME (2004) Prefrontal neurons coding suppression of specific saccades. Neuron 43(3):415–425

    Article  CAS  PubMed  Google Scholar 

  • Heitz RP, Schall JD (2013) Neural chronometry and coherency across speed–accuracy demands reveal lack of homomorphism between computational and neural mechanisms of evidence accumulation. Philos Trans R Soc Lond B Biol Sci 368(1628):20130071

    Article  PubMed  PubMed Central  Google Scholar 

  • Lansbergen MM, Schutter DJ, Kenemans JL (2007) Subjective impulsivity and baseline EEG in relation to stopping performance. Brain Res 1148:161–169

    Article  CAS  PubMed  Google Scholar 

  • Lappin JS, Eriksen CW (1966) Use of a delayed signal to stop a visual reaction-time response. J Exp Psychol 72:805–811

    Article  Google Scholar 

  • Lo CC, Boucher L, Paré M, Schall JD, Wang XJ (2009) Proactive inhibitory control and attractor dynamics in countermanding action: a spiking neural circuit model. J Neurosci 29(28):9059–9071

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Logan GD (1981) Attention, automaticity, and the ability to stop a speeded choice response. In: Long J, Baddeley AD (eds) Attention and performance IX. Erlbaum, Hillsdale

    Google Scholar 

  • Logan GD, Burkell J (1986) Dependence and independence in responding to double stimulation: a comparison of stop, change, and dual-task paradigms. J Exp Psychol Hum Percept Perform 12:549–563

    Article  Google Scholar 

  • Logan GD, Cowan WB (1984) On the ability to inhibit thought and action: a theory of an act of control. Psychol Rev 91:295–327

    Article  Google Scholar 

  • Munoz DP, Everling S (2004) Look away: the anti-saccade task and the voluntary control of eye movement. Nat Rev Neurosci 5(3):218–228

    Article  CAS  PubMed  Google Scholar 

  • Munoz DP, Dorris MC, Paré M, Everling S (2000) On your mark, get set: brainstem circuitry underlying saccadic initiation. Can J Physiol Pharmacol 78:934–944

    Article  CAS  PubMed  Google Scholar 

  • Ollman RT (1973) Simple reactions with random countermanding of the “go”-signal. In: Kornblum S (ed) Attention and performance IV. Academic Press, New York, pp 571–581

    Google Scholar 

  • Paré M, Hanes DP (2003) Controlled movement processing: superior colliculus activity associated with countermanded saccades. J Neurosci 23(16):6480–6489

    PubMed  Google Scholar 

  • Poitou T, Pouget P (2012) Saccadometry and movement inhibition. Biocybern Biomed Eng 32(2):33–47

    Article  Google Scholar 

  • Pouget P, Wattiez N, Rivaud-Péchoux S, Gaymard B (2010) Rapid development of tolerance to sub-anaesthetic dose of ketamine: an oculomotor study in macaque monkeys. Psychopharmacology 209(4):313–318

    Article  CAS  PubMed  Google Scholar 

  • Pouget P, Logan GD, Palmeri TJ, Boucher L, Paré M, Schall JD (2011) Neural basis of adaptive response time adjustment during saccade countermanding. J Neurosci 31(35):12604–12612

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramautar JR, Kok A, Ridderinkhof KR (2004) Effects of stop-signal probability in the stop-signal paradigm: the N2/P3 complex further validated. Brain Cogn 56(2):234–252

    Article  CAS  PubMed  Google Scholar 

  • Rao SG, Williams GV, Goldman-Rakic PS (1999) Isodirectional tuning of adjacent interneurons and pyramidal cells during working memory: evidence for microcolumnar organization in PFC. J Neurophysiol 81(4):1903-1916

    CAS  PubMed  Google Scholar 

  • Schlag J, Dassonville P, Schlag-Rey M (1998) Interaction of the two frontal eye fields before saccade onset. J Neurophysiol 79(1):64-72

    CAS  PubMed  Google Scholar 

  • Schall JD (2004) On the role of frontal eye field in guiding attention and saccades. Vision Res Jun 44(12):1453-1467

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Schall JD, Hanes DP, Thompson KG, King DJ (1995) Saccade target selection in frontal eye field of macaque. I. Visual and premovement activation. J Neurosci 15:6905–6918

    CAS  PubMed  Google Scholar 

  • Sparks DL (1976) Functional properties of neurons in the monkey superior colliculus: coupling of neuronal activity and saccade onset. Brain Res 156:1–16

    Article  Google Scholar 

  • Smyth MM, Scholey KA (1994) Characteristics of spatial memory span: is there an analogy to the word length effect, based on movement time? Q J Exp Psychol A 47(1):91–117

    Article  CAS  PubMed  Google Scholar 

  • Stuphorn V, Schall JD (2002) Neuronal control and monitoring of initiation of movements. Muscle Nerve 26:326–339

    Article  PubMed  Google Scholar 

  • Sundberg KA, Mitchell JF, Reynolds JH (2009) Spatial attention modulates center-surround interactions in macaque visual area V4. Neuron 61:1–12

    Article  Google Scholar 

  • Verbruggen F, Logan GD (2008) Response inhibition in the stop-signal paradigm. Trends Cogn Sci 12(11):418–424

    Article  PubMed  PubMed Central  Google Scholar 

  • Verbruggen F, Logan GD (2009) Proactive adjustments of response strategies in the stop-signal paradigm. J Exp Psychol Hum Percept Perform 35(3):835–854

    Article  PubMed  PubMed Central  Google Scholar 

  • Verbruggen F, Chambers CD, Logan GD (2013) Fictitious inhibitory differences: how skewness and slowing distort the estimation of stopping latencies. Psychol Sci 24(3):352–362

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We wish to thank Matt Nelson for discussing the original design of the task.

Author information

Authors and Affiliations

  1. CNRS UMR 7225, INSERM UMRS 975, Institut du Cerveau et la Möelle (ICM), Hôpital de la Salpêtrière, Université Pierre et Marie Curie, 47 boulevard de l’Hôpital, 75651, Paris Cedex 13, France

    Nicolas Wattiez, Tymothée Poitou, Sophie Rivaud-Péchoux & Pierre Pouget

Authors
  1. Nicolas Wattiez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tymothée Poitou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sophie Rivaud-Péchoux
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pierre Pouget
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pierre Pouget.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wattiez, N., Poitou, T., Rivaud-Péchoux, S. et al. Evidence for spatial tuning of movement inhibition. Exp Brain Res 234, 1957–1966 (2016). https://doi.org/10.1007/s00221-016-4594-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-016-4594-8

Keywords

Search

Navigation