Skip to main content
SpringerLink
Log in

Neural processes mediating the preparation and release of focal motor output are suppressed or absent during imagined movement

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

Abstract

Movements that are executed or imagined activate a similar subset of cortical regions, but the extent to which this activity represents functionally equivalent neural processes is unclear. During preparation for an executed movement, presentation of a startling acoustic stimulus (SAS) evokes a premature release of the planned movement with the spatial and temporal features of the tasks essentially intact. If imagined movement incorporates the same preparatory processes as executed movement, then a SAS should release the planned movement during preparation. This hypothesis was tested using an instructed-delay cueing paradigm during which subjects were required to rapidly release a handheld weight while maintaining the posture of the arm or to perform first-person imagery of the same task while holding the weight. In a subset of trials, a SAS was presented at 1500, 500, or 200 ms prior to the release cue. Task-appropriate preparation during executed and imagined movements was confirmed by electroencephalographic recording of a contingent negative variation waveform. During preparation for executed movement, a SAS often resulted in premature release of the weight with the probability of release progressively increasing from 24 % at −1500 ms to 80 % at −200 ms. In contrast, the SAS rarely (<2 % of trials) triggered a release of the weight during imagined movement. However, the SAS frequently evoked the planned postural response (suppression of bicep brachii muscle activity) irrespective of the task or timing of stimulation (even during periods of postural hold without preparation). These findings provide evidence that neural processes mediating the preparation and release of the focal motor task (release of the weight) are markedly attenuated or absent during imagined movement and that postural and focal components of the task are prepared independently.

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

Similar content being viewed by others

References

  • Alibiglou L, MacKinnon CD (2012) The early release of planned movement by acoustic startle can be delayed by transcranial magnetic stimulation over the motor cortex. J Physiol 590:919–936

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Aruin AS, Shiratori T, Latash ML (2001) The role of action in postural preparation for loading and unloading in standing subjects. Exp Brain Res 138:458–466

    Article  CAS  PubMed  Google Scholar 

  • Bakker M, de Lange FP, Stevens JA, Toni I, Bloem BR (2007) Motor imagery of gait: a quantitative approach. Exp Brain Res 179:497–504

    Article  CAS  PubMed  Google Scholar 

  • Bakker M, De Lange FP, Helmich RC, Scheeringa R, Bloem BR, Toni I (2008) Cerebral correlates of motor imagery of normal and precision gait. Neuroimage 41:998–1010

    Article  CAS  PubMed  Google Scholar 

  • Barclay-Goddard RE, Stevenson TJ, Poluha W, Thalman L (2011) Mental practice for treating upper extremity deficits in individuals with hemiparesis after stroke. Cochrane Database Syst Rev 5:1–47

    Google Scholar 

  • Bateni H, Zecevic A, McIlroy WE, Maki BE (2004) Resolving conflicts in task demands during balance recovery: does holding an object inhibit compensatory grasping? Exp Brain Res 157:49–58

    Article  PubMed  Google Scholar 

  • Braun S, Kleynen M, Schols J, Schack T, Beurskens A, Wade D (2008) Using mental practice in stroke rehabilitation: a framework. Clin Rehabil 22:579–591

    Article  PubMed  Google Scholar 

  • Braun S, Kleynen M, van Heel T, Kruithof N, Wade D, Beurskens A (2013) The effects of mental practice in neurological rehabilitation; a systematic review and meta-analysis. Front Hum Neurosci 7:390

    Article  PubMed Central  PubMed  Google Scholar 

  • Brown P, Rothwell JC, Thompson PD, Britton TC, Day BL, Marsden CD (1991) New observations on the normal auditory startle reflex in man. Brain 114(Pt 4):1891–1902

    Article  PubMed  Google Scholar 

  • Butler AJ, Page SJ (2006) Mental practice with motor imagery: evidence for motor recovery and cortical reorganization after stroke. Arch Phys Med Rehabil 87:S2–S11

    Article  PubMed Central  PubMed  Google Scholar 

  • Caldara R, Deiber MP, Andrey C, Michel CM, Thut G, Hauert CA (2004) Actual and mental motor preparation and execution: a spatiotemporal ERP study. Exp Brain Res 159:389–399

    Article  PubMed  Google Scholar 

  • Carlsen AN, MacKinnon CD (2010) Motor preparation is modulated by the resolution of the response timing information. Brain Res 1322:38–49

    Article  CAS  PubMed  Google Scholar 

  • Carlsen AN, Chua R, Inglis JT, Sanderson DJ, Franks IM (2004a) Can prepared responses be stored subcortically? Exp Brain Res 159:301–309

    Article  PubMed  Google Scholar 

  • Carlsen AN, Chua R, Inglis JT, Sanderson DJ, Franks IM (2004b) Prepared movements are elicited early by startle. J Mot Behav 36:253–264

    Article  PubMed  Google Scholar 

  • Carlsen AN, Dakin CJ, Chua R, Franks IM (2007) Startle produces early response latencies that are distinct from stimulus intensity effects. Exp Brain Res 176:199–205

    Article  PubMed  Google Scholar 

  • Carlsen AN, Almeida QJ, Franks IM (2012a) Startle decreases reaction time to active inhibition. Exp Brain Res 217:7–14

    Article  PubMed  Google Scholar 

  • Carlsen AN, Maslovat D, Franks IM (2012b) Preparation for voluntary movement in healthy and clinical populations: evidence from startle. Clin Neurophysiol 123:21–33

    Article  PubMed  Google Scholar 

  • Carrillo-de-la-Pena MT, Galdo-Alvarez S, Lastra-Barreira C (2008) Equivalent is not equal: primary motor cortex (MI) activation during motor imagery and execution of sequential movements. Brain Res 1226:134–143

    Article  CAS  PubMed  Google Scholar 

  • Cisek P, Kalaska JF (2004) Neural correlates of mental rehearsal in dorsal premotor cortex. Nature 431:993–996

    Article  CAS  PubMed  Google Scholar 

  • Confais J, Kilavik BE, Ponce-Alvarez A, Riehle A (2012) On the anticipatory precue activity in motor cortex. J Neurosci 32:15359–15368

    Article  CAS  PubMed  Google Scholar 

  • Cordo PJ, Nashner LM (1982) Properties of postural adjustments associated with rapid arm movements. J Neurophysiol 47:287–302

    CAS  PubMed  Google Scholar 

  • Cressman EK, Carlsen AN, Chua R, Franks IM (2006) Temporal uncertainty does not affect response latencies of movements produced during startle reactions. Exp Brain Res 171:278–282

    Article  PubMed  Google Scholar 

  • Cunnington R, Iansek R, Bradshaw JL, Phillips JG (1996) Movement-related potentials associated with movement preparation and motor imagery. Exp Brain Res 111:429–436

    Article  CAS  PubMed  Google Scholar 

  • Decety J (1993) Analysis of actual and mental movement times in graphic tasks. Acta Psychol (Amst) 82:367–372

    Article  CAS  Google Scholar 

  • Decety J, Jeannerod M (1995) Mentally simulated movements in virtual reality: does Fitts’s law hold in motor imagery? Behav Brain Res 72:127–134

    Article  CAS  PubMed  Google Scholar 

  • Decety J, Jeannerod M, Prablanc C (1989) The timing of mentally represented actions. Behav Brain Res 34:35–42

    Article  CAS  PubMed  Google Scholar 

  • Dickstein R, Dunsky A, Marcovitz E (2004) Motor imagery for gait rehabilitation in post-stroke hemiparesis. Phys Ther 84:1167–1177

    PubMed  Google Scholar 

  • Dunsky A, Dickstein R, Ariav C, Deutsch J, Marcovitz E (2006) Motor imagery practice in gait rehabilitation of chronic post-stroke hemiparesis: four case studies. Int J Rehabil Res 29:351–356

    Article  PubMed  Google Scholar 

  • Duque J, Ivry RB (2009) Role of corticospinal suppression during motor preparation. Cereb Cortex 19:2013–2024

    Article  PubMed Central  PubMed  Google Scholar 

  • Duque J, Lew D, Mazzocchio R, Olivier E, Ivry RB (2010) Evidence for two concurrent inhibitory mechanisms during response preparation. J Neurosci 30:3793–3802

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fontani G, Migliorini S, Benocci R, Facchini A, Casini M, Corradeschi F (2007) Effect of mental imagery on the development of skilled motor actions. Percept Mot Skills 105:803–826

    PubMed  Google Scholar 

  • Frank C, Land WM, Popp C, Schack T (2014) Mental representation and mental practice: experimental investigation on the functional links between motor memory and motor imagery. PLoS ONE 9:e95175

    Article  PubMed Central  PubMed  Google Scholar 

  • Gahery Y, Ioffe ME, Massion J, Polit A (1981) Postural support for local movements in cats and dogs. Zh Vyssh Nerv Deiat Im I P Pavlova 31:232–241

    CAS  PubMed  Google Scholar 

  • Gentili R, Papaxanthis C, Pozzo T (2006) Improvement and generalization of arm motor performance through motor imagery practice. Neuroscience 137:761–772

    Article  CAS  PubMed  Google Scholar 

  • Gerardin E, Sirigu A, Lehericy S et al (2000) Partially overlapping neural networks for real and imagined hand movements. Cereb Cortex 10:1093–1104

    Article  CAS  PubMed  Google Scholar 

  • Green JB, Bialy Y, Sora E, Thatcher RW (1997) An electroencephalographic study of imagined movement. Arch Phys Med Rehabil 78:578–581

    Article  CAS  PubMed  Google Scholar 

  • Hanakawa T, Dimyan MA, Hallett M (2008) Motor planning, imagery, and execution in the distributed motor network: a time-course study with functional MRI. Cereb Cortex 18:2775–2788

    Article  PubMed Central  PubMed  Google Scholar 

  • Hodges PW, Bui BH (1996) A comparison of computer-based methods for the determination of onset of muscle contraction using electromyography. Electroencephalogr Clin Neurophysiol 101:511–519

    CAS  PubMed  Google Scholar 

  • Holmes P, Calmels C (2008) A neuroscientific review of imagery and observation use in sport. J Mot Behav 40:433–445

    Article  PubMed  Google Scholar 

  • Hugon M, Massion J, Wiesendanger M (1982) Anticipatory postural changes induced by active unloading and comparison with passive unloading in man. Pflugers Arch 393:292–296

    Article  CAS  PubMed  Google Scholar 

  • Ietswaart M, Johnston M, Dijkerman HC, Joice S, Scott CL, MacWalter RS, Hamilton SJ (2011) Mental practice with motor imagery in stroke recovery: randomized controlled trial of efficacy. Brain 134:1373–1386

    Article  PubMed Central  PubMed  Google Scholar 

  • Jackson PL, Doyon J, Richards CL, Malouin F (2004) The efficacy of combined physical and mental practice in the learning of a foot-sequence task after stroke: a case report. Neurorehabil Neural Repair 18:106–111

    Article  PubMed  Google Scholar 

  • Jankelowitz SK, Colebatch JG (2002) Movement-related potentials associated with self-paced, cued and imagined arm movements. Exp Brain Res 147:98–107

    Article  CAS  PubMed  Google Scholar 

  • Jeannerod M (2001) Neural simulation of action: a unifying mechanism for motor cognition. Neuroimage 14:S103–S109

    Article  CAS  PubMed  Google Scholar 

  • Kearns DW, Crossman J (1992) Effects of a cognitive intervention package on the free-throw performance of varsity basketball players during practice and competition. Percept Mot Skills 75:1243–1253

    Article  CAS  PubMed  Google Scholar 

  • Kho AY, Liu KP, Chung RC (2014) Meta-analysis on the effect of mental imagery on motor recovery of the hemiplegic upper extremity function. Aust Occup Ther J 61:38–48

    Article  PubMed  Google Scholar 

  • Kranczioch C, Mathews S, Dean PJ, Sterr A (2009) On the equivalence of executed and imagined movements: evidence from lateralized motor and nonmotor potentials. Hum Brain Mapp 30:3275–3286

    Article  PubMed  Google Scholar 

  • Kranczioch C, Mathews S, Dean P, Sterr A (2010) Task complexity differentially affects executed and imagined movement preparation: evidence from movement-related potentials. PLoS ONE 5:e9284

    Article  PubMed Central  PubMed  Google Scholar 

  • Kumru H, Valls-Solé J (2006) Excitability of the pathways mediating the startle reaction before execution of a voluntary movement. Exp Brain Res 169:427–432

    Article  PubMed  Google Scholar 

  • la Fougere C, Zwergal A, Rominger A et al (2010) Real versus imagined locomotion: a [18F]-FDG PET-fMRI comparison. Neuroimage 50:1589–1598

    Article  PubMed  Google Scholar 

  • Lotze M, Cohen LG (2006) Volition and imagery in neurorehabilitation. Cogn Behav Neurol 19:135–140

    Article  PubMed  Google Scholar 

  • Lotze M, Montoya P, Erb M et al (1999) Activation of cortical and cerebellar motor areas during executed and imagined hand movements: an fMRI study. J Cogn Neurosci 11:491–501

    Article  CAS  PubMed  Google Scholar 

  • MacKinnon CD, Bissig D, Chiusano J et al (2007) Preparation of anticipatory postural adjustments prior to stepping. J Neurophysiol 97:4368–4379

    Article  PubMed  Google Scholar 

  • MacKinnon CD, Allen DP, Shiratori T, Rogers MW (2013) Early and unintentional release of planned motor actions during motor cortical preparation. PLoS ONE 8:e63417

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Malouin F, Richards CL, Jackson PL, Dumas F, Doyon J (2003) Brain activations during motor imagery of locomotor-related tasks: a PET study. Hum Brain Mapp 19:47–62

    Article  PubMed  Google Scholar 

  • Maslovat D, Chua R, Hodges NJ (2013) When unintended movements “leak” out: a startling acoustic stimulus can elicit a prepared response during motor imagery and action observation. Neuropsychologia 51:838–844

    Article  PubMed  Google Scholar 

  • Mason SG, Bashashati A, Fatourechi M, Navarro KF, Birch GE (2007) A comprehensive survey of brain interface technology designs. Ann Biomed Eng 35:137–169

    Article  CAS  PubMed  Google Scholar 

  • Olsson CJ, Jonsson B, Nyberg L (2008) Internal imagery training in active high jumpers. Scand J Psychol 49:133–140

    Article  PubMed  Google Scholar 

  • Rogers MW, Kennedy R, Palmer S et al (2011) Postural preparation prior to stepping in patients with Parkinson’s disease. J Neurophysiol 106:915–924

    Article  PubMed  Google Scholar 

  • Roland PE, Larsen B, Lassen NA, Skinhoj E (1980) Supplementary motor area and other cortical areas in organization of voluntary movements in man. J Neurophysiol 43:118–136

    CAS  PubMed  Google Scholar 

  • Schack T, Essig K, Frank C, Koester D (2014) Mental representation and motor imagery training. Front Hum Neurosci 8:328

    Article  PubMed Central  PubMed  Google Scholar 

  • Sharma N, Pomeroy VM, Baron JC (2006) Motor imagery: a backdoor to the motor system after stroke? Stroke 37:1941–1952

    Article  PubMed  Google Scholar 

  • Sirigu A, Duhamel JR (2001) Motor and visual imagery as two complementary but neurally dissociable mental processes. J Cogn Neurosci 13:910–919

    Article  CAS  PubMed  Google Scholar 

  • Smith JL, Jamadar S, Provost AL, Michie PT (2013) Motor and non-motor inhibition in the Go/NoGo task: an ERP and fMRI study. Int J Psychophysiol 87:244–253

    Article  PubMed  Google Scholar 

  • Snijders AH, Leunissen I, Bakker M, Overeem S, Helmich RC, Bloem BR, Toni I (2011) Gait-related cerebral alterations in patients with Parkinson’s disease with freezing of gait. Brain 134:59–72

    Article  PubMed  Google Scholar 

  • Stephan KM, Fink GR, Passingham RE, Silbersweig D, Ceballos-Baumann AO, Frith CD, Frackowiak RS (1995) Functional anatomy of the mental representation of upper extremity movements in healthy subjects. J Neurophysiol 73:373–386

    CAS  PubMed  Google Scholar 

  • Valls-Solé J, Rothwell JC, Goulart F, Cossu G, Munoz E (1999) Patterned ballistic movements triggered by a startle in healthy humans. J Physiol 516(Pt 3):931–938

    Article  PubMed Central  PubMed  Google Scholar 

  • Valls-Solé J, Kumru H, Kofler M (2008) Interaction between startle and voluntary reactions in humans. Exp Brain Res 187:497–507

    Article  PubMed  Google Scholar 

  • Walter WG, Cooper R, Aldridge VJ, McCallum WC, Winter AL (1964) Contingent negative variation: an electric sign of sensorimotor association and expectancy in the human brain. Nature 203:380–384

    Article  CAS  PubMed  Google Scholar 

  • Wriessnegger SC, Steyrl D, Koschutnig K, Muller-Putz GR (2014) Short time sports exercise boosts motor imagery patterns: implications of mental practice in rehabilitation programs. Front Hum Neurosci 8:469

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We thank the volunteers for these experiments, and the technical assistance from Mr. Di Zhang. J.E. was supported by a Grant from NIH T32 HD057845 and ANC by a Grant from the Natural Sciences and Engineering Research Council of Canada (PDF-357177).

Author information

Authors and Affiliations

  1. Department of Physical Therapy and Human Movement Sciences, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA

    Jeremy S. Eagles, Anthony N. Carlsen & Colum D. MacKinnon

  2. School of Human Kinetics, Faculty of Health Sciences, University of Ottawa, Ottawa, Canada

    Anthony N. Carlsen

  3. Department of Neurology, University of Minnesota, 717 Delaware St., S.E., Minneapolis, MN, 55455, USA

    Colum D. MacKinnon

Authors
  1. Jeremy S. Eagles
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anthony N. Carlsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Colum D. MacKinnon
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Colum D. MacKinnon.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Eagles, J.S., Carlsen, A.N. & MacKinnon, C.D. Neural processes mediating the preparation and release of focal motor output are suppressed or absent during imagined movement. Exp Brain Res 233, 1625–1637 (2015). https://doi.org/10.1007/s00221-015-4237-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-015-4237-5

Keywords

Search

Navigation