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Inhibitory control of reaching movements in humans

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An Erratum to this article was published on 14 February 2009

Abstract

Behavioral flexibility provides a very large repertoire of actions and strategies, however, it carries a cost: a potential interference between different options. The voluntary control of behavior starts exactly with the ability of deciding between alternatives. Certainly inhibition plays a key role in this process. Here we examined the inhibitory control of reaching arm movements with the countermanding paradigm. Right-handed human subjects were asked to perform speeded reaching movements toward a visual target appearing either on the same or opposite side of the reaching arm (no-stop trials), but to withhold the commanded movement whenever an infrequent stop signal was presented (stop trials). As the delay between go and stop signals increased, subjects increasingly failed to inhibit the movement. From this inhibitory function and the reaction times of movements in no-stop trials, we estimated the otherwise unobservable duration of the stopping process, the stop signal reaction time (SSRT). We found that the SSRT for reaching movements was, on average, 206 ms and that it varied with the reaching arm and the target position even though the stop signal was a central stimulus. In fact, subjects were always faster to withhold reaching movements toward visual targets appearing on the same side of the reaching arm. This behavior strictly parallels the course of the reaction times of no-stop trials. These data show that the stop and go processes interacting in this countermanding task are independent, but most likely influenced by a common factor when under the control of the same hemisphere. In addition, we show that the point beyond which the response cannot be inhibited, the so-called point-of-no-return that divides controlled and ballistic phases of movement processing, lies after the inter-hemispheric transfer.

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References

  • Aron AR, Fletcher PC, Bullmore ET, Sahakian BJ, Robbins TW (2003) Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans. Nat Neurosci 6:115–116

    Article  PubMed  CAS  Google Scholar 

  • Asrress KN, Carpenter RH (2001) Saccadic countermanding: a comparison of central and peripheral stop signals. Vision Res 41:2645–2651

    Article  PubMed  CAS  Google Scholar 

  • Band GPH (1997) Preparation, adjustment, and inhibition of responses. PhD Thesis, Faculteit Psychologie, Universiteit van Amsterdam

  • Barthelemy S, Boulinguez P (2002a) Manual asymmetries in the directional coding of reaching: further evidence for hemispatial effects and right hemisphere dominance for movement planning. Exp Brain Res 147:305–312

    Article  Google Scholar 

  • Barthelemy S, Boulinguez P (2002b) Orienting visuospatial attention generates manual reaction time asymmetries in target detection and pointing. Behav Brain Res 133:109–116

    Article  Google Scholar 

  • Bashore TR (1981) Vocal and manual reaction time estimates of interhemispheric transmission time. Psychol Bull 89:352–368

    Article  PubMed  CAS  Google Scholar 

  • Botvinick MM, Braver TS, Barch DM, Carter CS, Cohen JD (2001) Conflict monitoring and cognitive control. Psychol Rev 108:624–652

    Article  PubMed  CAS  Google Scholar 

  • Boulinguez P, Nougier V, Velay JL (2001) Manual asymmetries in reaching movement control. I: Study of right-handers. Cortex 37:101–122

    Article  PubMed  CAS  Google Scholar 

  • Brown JW, Braver TS (2005) Learned predictions of error likelihood in the anterior cingulate cortex. Science 307:1118–1121

    Article  PubMed  CAS  Google Scholar 

  • Bryden MP (1977) Measuring handedness with questionnaires. Neuropsychologia 15:617–624

    Article  PubMed  CAS  Google Scholar 

  • Cabel DW, Armstrong IT, Reingold E, Munoz DP (2000) Control of saccade initiation in a countermanding task using visual and auditory stop signals. Exp Brain Res 133:431–441

    Article  PubMed  CAS  Google Scholar 

  • Caminiti R, Ferraina S, Battaglia-Mayer A (1998) Visuomotor transformations: early cortical mechanisms of reaching. Curr Opin Neurobiol 8:753–761

    Article  PubMed  CAS  Google Scholar 

  • Cavina-Pratesi C, Bricolo E, Pellegrini B, Marzi CA (2004) At what stage of manual visual reaction time does interhemispheric transmission occur: controlled or ballistic? Exp Brain Res 155:220–230

    Article  PubMed  CAS  Google Scholar 

  • Colonius H, Ozyurt J, Arndt PA (2001) Countermanding saccades with auditory stop signals: testing the race model. Vision Res 41:1951–1968

    Article  PubMed  CAS  Google Scholar 

  • Corneil BD, Elsley JK (2005) Countermanding eye-head gaze shifts in humans: marching orders are delivered to the head first. J Neurophysiol 94:883–895

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • De Jong R, Coles MG, Logan GD, Gratton G (1990) In search of the point of no return: the control of response processes. J Exp Psychol Hum Percept Perform 16:164–182

    Article  PubMed  Google Scholar 

  • Desmurget M, Grafton S (2000) Forward modeling allows feedback control for fast reaching movements. Trends Cogn Sci 4:423–431

    Article  PubMed  Google Scholar 

  • Douglas VI (1999) Cognitive control processes in attention-deficit hyperactivity disorder. In: Quay HC, Hogan AE (eds) Handbook of disruptive behavior disorders. Kluwer Academic/Plenum Publishers, NewYork

  • Dum RP, Strick PL (1996) Spinal cord terminations of the medial wall motor areas in macaque monkeys. J Neurosci 16:6513–6525

    PubMed  CAS  Google Scholar 

  • Fisk JD, Goodale MA (1988) The effects of unilateral brain damage on visually guided reaching: hemispheric differences in the nature of the deficit. Exp Brain Res 72:425–435

    Article  PubMed  CAS  Google Scholar 

  • Georgopoulos AP (1986) On reaching. Annu Rev Neurosci 9:147–170

    Article  PubMed  CAS  Google Scholar 

  • Georgopoulos AP (1996) Arm movements in monkeys: behavior and neurophysiology. J Comp Physiol [A] 179:603–612

    Article  CAS  Google Scholar 

  • Graziano MS, Taylor CS, Moore T, Cooke DF (2002) The cortical control of movement revisited. Neuron 36:349–362

    Article  PubMed  CAS  Google Scholar 

  • Hanes DP, Carpenter RH (1999) Countermanding saccades in humans. Vision Res 39:2777–2791

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ito S, Stuphorn V, Brown JW, Schall JD (2003) Performance monitoring by the anterior cingulate cortex during saccade countermanding. Science 302:120–122

    Article  PubMed  CAS  Google Scholar 

  • Johnson PB, Ferraina S, Bianchi L, Caminiti R (1996) Cortical networks for visual reaching. Physiological and anatomical organization of frontal and parietal lobe arm regions. Cereb Cortex 6:102–119

    CAS  Google Scholar 

  • Jones AD, Cho RY, Nystrom LE, Cohen JD, Braver TS (2002) A computational model of anterior cingulate function in speeded response tasks: effects of frequency, sequence, and conflict. Cogn Affect Behav Neurosci 2:300–317

    Article  PubMed  Google Scholar 

  • Kalaska JF, Crammond DJ (1995) Deciding not to GO: neuronal correlates of response selection in a GO/NOGO task in primate premotor and parietal cortex. Cereb Cortex 5:410–428

    Article  PubMed  CAS  Google Scholar 

  • Kalaska JF, Scott SH, Cisek P, Sergio LE (1997) Cortical control of reaching movements. Curr Opin Neurobiol 7:849–859

    Article  PubMed  CAS  Google Scholar 

  • Kornylo K, Dill N, Saenz M, Krauzlis RJ (2003) Cancelling of pursuit and saccadic eye movements in humans and monkeys. J Neurophysiol 89:2984–2999

    Article  PubMed  Google Scholar 

  • Kramer AF, Humphrey DG, Larish JF, Logan GD, Strayer DL (1994) Aging and inhibition: beyond a unitary view of inhibitory processing in attention. Psychol Aging 9:491–512

    Article  PubMed  CAS  Google Scholar 

  • Kudo K, Ohtsuki T (1998) Functional modification of agonist-antagonist electromyographic activity for rapid movement inhibition. Exp Brain Res 122:23–30

    Article  PubMed  CAS  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 

  • Liddle PF, Kiehl KA, Smith AM (2001) Event-related fMRI study of response inhibition. Hum Brain Mapp 12:100–109

    Article  PubMed  CAS  Google Scholar 

  • Logan GD (1981) Attention, automaticity and the ability to stop a speeded choice response. In: Long J, Baddley AD (eds) Attention and performance IX. Hillsdale, Erlbaum, NJ, pp 205–222

    Google Scholar 

  • Logan GD (1994) On the ability to inhibit thought and action: a users’ guide to the stop signal paradigm. In: Dagenbach D, Carr TH (eds) Inhibitory processes in attention, memory and language. Academic Press, San Diego, pp 189–239

    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 

  • Logan GD, Irwin DE (2000) Don’t look! Don’t touch! Inhibitory control of eye and hand movements. Psychon Bull Rev 7:107–112

    PubMed  CAS  Google Scholar 

  • Marzi CA (1999) The Poffenberger paradigm: a first, simple, behavioural tool to study interhemispheric transmission in humans. Brain Res Bull 50:421–422

    Article  PubMed  CAS  Google Scholar 

  • Marzi CA, Bisiacchi P, Nicoletti R (1991) Is interhemispheric transfer of visuomotor information asymmetric? Evidence from a meta-analysis. Neuropsychologia 29:1163–1177

    Article  PubMed  CAS  Google Scholar 

  • McGarry T, Franks IM (1997) A horse race between independent processes: evidence for a phantom point of no return in preparation of a speeded motor response. J Exp Psychol Hum Percept Perform 23:1533–1542

    Article  PubMed  CAS  Google Scholar 

  • Mesulam MM (1981) A cortical network for directed attention and unilateral neglect. Ann Neurol 10:309–325

    Article  PubMed  CAS  Google Scholar 

  • Mieschke PE, Elliott D, Helsen WF, Carson RG, Coull JA (2001) Manual asymmetries in the preparation and control of goal-directed movements. Brain Cogn 45:129–140

    Article  PubMed  CAS  Google Scholar 

  • Miller J, Riehle A, Requin J (1992) Effects of preliminary perceptual output on neuronal activity of the primary motor cortex. J Exp Psychol Hum Percept Perform 18:1121–1138

    Article  PubMed  CAS  Google Scholar 

  • Mirabella G, Pani P, Ferraina S (2004) Countermanding reaching in monkeys (Macaca mulatta) and humans. Soc Neurosci Abstr 30:211.4

    Google Scholar 

  • Moll L, Kuypers HG (1977) Premotor cortical ablations in monkeys: contralateral changes in visually guided reaching behavior. Science 198:317–319

    Article  PubMed  CAS  Google Scholar 

  • Neely K, Binsted G, Heath M (2005) Manual asymmetries in bimanual reaching: the influence of spatial compatibility and visuospatial attention. Brain Cogn 57:102–105

    Article  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, pp571–581

    Google Scholar 

  • Osman A, Kornblum S, Meyer DE (1990) Does motor programming necessitate response execution? J Exp Psychol Hum Percept Perform 16:183–198

    Article  PubMed  CAS  Google Scholar 

  • Ozyurt J, Colonius H, Arndt PA (2003) Countermanding saccades: evidence against independent processing of go and stop signals. Percept Psychophys 65:420–428

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Poffenberger AT (1912) Reaction time to retinal stimulation with special reference to the time lost in conduction through nervous centres. Arch Psychol 23:1–73

    Google Scholar 

  • Port NL, Kruse W, Lee D, Georgopoulos AP (2001) Motor cortical activity during interception of moving targets. J Cogn Neurosci 13:306–318

    Article  PubMed  CAS  Google Scholar 

  • Rieger M, Gauggel S (1999) Inhibitory after-effects in the stop signal paradigm. Br J Psychol 90:509–518

    Article  Google Scholar 

  • Rubia K, Russell T, Bullmore ET, Soni W, Brammer MJ, Simmons A, Taylor E, Andrew C, Giampietro V, Sharma T (2001) An fMRI study of reduced left prefrontal activation in schizophrenia during normal inhibitory function. Schizophr Res 52:47–55

    Article  PubMed  CAS  Google Scholar 

  • Stuphorn V, Taylor TL, Schall JD (2000) Performance monitoring by the supplementary eye field. Nature 408:857–860

    Article  PubMed  CAS  Google Scholar 

  • Van den Wildenberg WP, Van der Molen MW, Logan GD (2002) Reduced response readiness delays stop signal inhibition. Acta Psychol (Amst) 111:155–169

    Article  Google Scholar 

  • Van der Schoot M, Licht R, Horsley TM, Sergeant JA (2003) Hemispheric differences in stop task performance. Acta Psychol (Amst) 112:279–295

    Article  Google Scholar 

  • Velay JL, Benoit-Dubrocard S (1999) Hemispheric asymmetry and interhemispheric transfer in reaching programming. Neuropsychologia 37:895–903

    Article  PubMed  CAS  Google Scholar 

  • Velay JL, Daffaure V, Giraud K, Habib M (2002) Interhemispheric sensorimotor integration in pointing movements: a study on dyslexic adults. Neuropsychologia 40:827–834

    Article  PubMed  Google Scholar 

  • Velay JL, Daffaure V, Raphael N, Benoit-Dubrocard S (2001) Hemispheric asymmetry and interhemispheric transfer in pointing depend on the spatial components of the movement. Cortex 37:75–90

    Article  PubMed  CAS  Google Scholar 

  • Watanabe J, Sugiura M, Sato K, Sato Y, Maeda Y, Matsue Y, Fukuda H, Kawashima R (2002) The human prefrontal and parietal association cortices are involved in NO-GO performances: an event-related fMRI study. Neuroimage 17:1207–1216

    Article  PubMed  Google Scholar 

  • Wise SP (1985) The primate premotor cortex: past, present, and preparatory. Annu Rev Neurosci 8:1–19

    Article  PubMed  CAS  Google Scholar 

  • Wise SP, Boussaoud D, Johnson PB, Caminiti R (1997) Premotor and parietal cortex: corticocortical connectivity and combinatorial computations. Annu Rev Neurosci 20:25–42

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the grant C26G031031 from the University of Rome ‘La Sapienza’ and partially by the grant 530/F4/1 from the Italian National Institute of Health and by the grant 2005051741 from the MIUR. M. Paré is a EBJL Foundation Research Scholar and he holds a New Investigator Award from the Canadian Institutes of Health Research. He was a Visiting Professor (fall 2004) at the University of Rome ‘La Sapienza’. We would like to acknowledge the contribution of Trina Norden-Krichmar for invaluable advice concerning the Cortex set-up.

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Authors and Affiliations

  1. Department of Human Physiology and Pharmacology, University ‘La Sapienza’, Piazzale Aldo Moro 5, 00185, Rome, Italy

    Giovanni Mirabella, Pierpaolo Pani, Martin Paré & Stefano Ferraina

  2. Dottorato di Ricerca in Neurofisiologia, University ‘La Sapienza’, Piazzale Aldo Moro 5, 00185, Rome, Italy

    Pierpaolo Pani

  3. Department of Physiology, Queen’s University, Kingston, ON, Canada, K7L 3N6

    Martin Paré

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  1. Giovanni Mirabella
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  4. Stefano Ferraina
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Correspondence to Stefano Ferraina.

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An erratum to this article can be found at http://dx.doi.org/10.1007/s00221-009-1727-3.

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Mirabella, G., Pani, P., Paré, M. et al. Inhibitory control of reaching movements in humans. Exp Brain Res 174, 240–255 (2006). https://doi.org/10.1007/s00221-006-0456-0

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