Abstract
Arm motor recovery after stroke is mainly attributed to reorganization of the primary motor cortex (M1). While M1 contralateral to the paretic arm (cM1) is critical for recovery, the role of ipsilateral M1 (iM1) is still inconclusive. Whether iM1 activity is related to recovery, behavioral compensation, or both is still far from settled. We hypothesized that the magnitude of iM1 activity in chronic stroke survivors will increase or decrease in direct proportion to the degree that movements of the paretic arm are compensated. Movement kinematics (VICON, Oxford Metrics) and functional MRI data (3T MR system) were collected in 11 patients before and after a 4-week training designed to improve motor control of the paretic arm and decrease compensatory trunk recruitment. Twelve matched controls underwent similar evaluations and training. Relationships between iM1 activity and trunk motion were analyzed. At baseline, patients exhibited increased iM1 activity (p = 0.001) and relied more on trunk movement (p = 0.02) than controls. These two variables were directly and significantly related in patients (r = 0.74, p = 0.01) but not in controls (r = 0.28, p = 0.4). After training, patients displayed a significant reduction in iM1 activity (p = 0.008) and a trend toward decreased trunk use (p = 0.1). The relationship between these two variables remained significant (r = 0.66, p = 0.03) and different from controls (r = 0.26, p = 0.4). Our preliminary results suggest that iM1 may play a role in compensating for brain damage rather than directly gaining control of the paretic arm. However, we recommend caution in interpreting these results until more work is completed.
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References
Ada L, Canning C, Dwyer T (2000) Effect of muscle length on strength and dexterity after stroke. Clin Rehabil 14:55–61
Allred RP, Maldonado MA, Hsu Je, Jones TA (2005) Training the “less-affected” forelimb after unilateral cortical infarcts interferes with functional recovery of the impaired forelimb in rats. Restor Neurol Neurosci 23:297–302
Bastlová P, Frgalová I, Kolářová B, Elfmark M, Krobot A (2014) The upper extremity function of stroke patients in the view of surface electromyography. Perofese Online 7:1–6
Bawa P, Hamm JD, Dhillon P, Gross PA (2004) Bilateral responses of upper limb muscles to transcranial magnetic stimulation in human subjects. Exp Brain Res 158:385–390
Blicher JU, Near J, Naess-Schmidt E, Stagg CJ, Johansen-Berg H, Nielsen JF, Ostergaard L, Ho YC (2015) GABA levels are decreased after stroke and GABA changes during rehabilitation correlate with motor improvement. Neurorehabil Neural Repair 29:278–286
Boyd LA, Vidoni ED, Wessel BD (2010) Motor learning after stroke: is skill acquisition a prerequisite for contralesional neuroplastic change? Neurosci Lett 482:21–25
Bradnam LV, Stinear CM, Barber PA, Byblow WD (2012) Contralesional hemisphere control of the proximal paretic upper limb following stroke. Cereb Cortex 22:2662–2671
Bressel E, Bressel M, Marquez M, Heise GD (2001) The effect of handgrip position on upper extremity neuromuscular responses to arm cranking exercise. J Electromyogr Kinesiol 11(4):291–298
Buetefisch CM, Revill KP, Shuster L, Hines B, Parsons M (2014) Motor demand-dependent activation of ipsilateral motor cortex. J Neurophysiol 112:999–1009
Buonomano DV, Merzenich MM (1998) Cortical plasticity: from synapses to maps. Annu Rev Neurosci 21:149–186
Butefisch CM, Netz J, Wessling M, Seitz RJ, Homberg V (2003) Remote changes in cortical excitability after stroke. Brain 126:470–481
Butefisch CM, Wessling M, Netz J, Seitz RJ, Homberg V (2008) Relationship between interhemispheric inhibition and motor cortex excitability in subacute stroke patients. Neurorehabil Neural Repair 22:4–21
Byrnes ML, Thickbroom GW, Phillips BA, Mastaglia FL (2001) Long-term changes in motor cortical organisation after recovery from subcortical stroke. Brain Res 889:278–287
Chollet F, DiPiero V, Wise RJ, Brooks DJ, Dolan RJ, Frackowiak RS (1991) The functional anatomy of motor recovery after stroke in humans: a study with positron emission tomography. Ann Neurol 29:63–71
Cirstea MC, Levin MF (2000) Compensatory strategies for reaching in stroke. Brain 123(Pt 5):940–953
Cirstea MC, Levin MF (2007) Improvement of arm movement patterns and endpoint control depends on type of feedback during practice in stroke survivors. Neurorehab Neural Repair 21:398–411
Cirstea CM, Ptito A, Levin MF (2006) Feedback and cognition in arm motor skill reacquisition after stroke. Stroke 37:1237–1242
Cirstea CM, Brooks WM, Craciunas SC, Popescu EA, Choi IY, Lee P, Bani-Ahmed A, Yeh HW, Savage CR, Cohen LG et al (2011) Primary motor cortex in stroke: a functional MRI-guided proton MR spectroscopic study. Stroke 42:1004–1009
Cirstea CM, Lee P, Craciunas SC, Choi IY, Burris JE, Nudo RJ (2018) Pre-therapy neural state of bilateral motor and premotor cortices predicts therapy gain after subcortical stroke: a pilot study. Am J Phys Med Rehabil 97:23–33
Colebatch JG, Gandevia SC (1989) The distribution of muscular weakness in upper motor neuron lesions affecting the arm. Brain 112(Pt 3):749–763
Cramer SC (2008) Repairing the human brain after stroke: I mechanisms of spontaneous recovery. Ann Neurol 63:272–287
Cramer SC, Nelles G, Benson RR, Kaplan JD, Parker RA, Kwong KK, Kennedy DN, Finklestein SP, Rosen BR (1997) A functional MRI study of subjects recovered from hemiparetic stroke. Stroke 28:2518–2527
Davey NJ, Lisle RM, Loxton-Edwards B, Nowicky AV, McGregor AH (2002) Activation of back muscles during voluntary abduction of the contralateral arm in humans. Spine (Phila Pa 1976) 27:1355–1360
Dewald JP, Pope PS, Given JD, Buchanan TS, Rymer WZ (1995) Abnormal muscle coactivation patterns during isometric torque generation at the elbow and shoulder in hemiparetic subjects. Brain 118(Pt 2):495–510
Donoghue JP, Leibovic S, Sanes JN (1992) Organization of the forelimb area in squirrel monkey motor cortex: representation of digit, wrist, and elbow muscles. Exp Brain Res 89:1–19
Ejaz N, Xu J, Branscheidt M, Hertler B, Schambra H, Widmer M, Faria AV, Harran MD, Cortes JC, Kim N et al (2018) Evidence for a subcortical origin of mirror movements after stroke: a longitudinal study. Brain 141:837–847
Elsner B, Kugler J, Pohl M, Mehrholz J (2013) Transcranial direct current stimulation (tDCS) for improving function and activities of daily living in patients after stroke. Cochrane Database Syst Rev 11:CD009645
Favre I, Zeffiro TA, Detante O, Krainik A, Hommel M, Jaillard A (2014) Upper limb recovery after stroke is associated with ipsilesional primary motor cortical activity: a meta-analysis. Stroke 45:1077–1083
Fazekas F, Chawluk JB, Alavi A, Hurtig HI, Zimmerman RA (1987) MR signal abnormalities at 1.5 T in Alzheimer's dementia and normal aging. Am J Roentgenol 149:351–356
Fess E (1992) Grip strength. In: Casanova J (ed) Clinical assessment recommendations. American Society of Hand Therapists, Chicago, pp 41–45
Fries W, Danek A, Scheidtmann K, Hamburger C (1993) Motor recovery following capsular stroke. Role of descending pathways from multiple motor areas. Brain 116(Pt 2):369–382
Fugl-Meyer AR, Jaasko L, Leyman I, Olsson S, Steglind S (1975) The post-stroke hemiplegic patient. 1. A method for evaluation of physical performance. Scand J Rehabil Med 7:13–31
Fusco A, Assenza F, Iosa M, Izzo S, Altavilla R, Paolucci S, Vernieri F (2014) The ineffective role of cathodal tDCS in enhancing the functional motor outcomes in early phase of stroke rehabilitation: an experimental trial. Biomed Res Int 2014:547290
Gerloff C, Bushara K, Sailer A, Wassermann EM, Chen R, Matsuoka T, Waldvogel D, Wittenberg GF, Ishii K, Cohen LG et al (2006) Multimodal imaging of brain reorganization in motor areas of the contralesional hemisphere of well recovered patients after capsular stroke. Brain 129:791–808
Gladstone DJ, Danells CJ, Black SE (2002) The fugl-meyer assessment of motor recovery after stroke: a critical review of its measurement properties. Neurorehabil Neural Repair 16:232–240
Grafton ST (2010) The cognitive neuroscience of prehension: recent developments. Exp Brain Res 204:475–491
Hansson GA, Balogh I, Ohlsson K, Rylander L, Skerfving S (1996) Goniometer measurement and computer analysis of wrist angles and movements applied to occupational repetitive work. J Electromyogr Kinesiol 6:23–35
Hao Z, Wang D, Zeng Y, Liu M (2013) Repetitive transcranial magnetic stimulation for improving function after stroke. Cochrane Database Syst Rev 5:CD008862
Hochberg LR, Serruya MD, Friehs GM, Mukand JA, Saleh M, Caplan AH, Branner A, Chen D, Penn RD, Donoghue JP (2006) Neuronal ensemble control of prosthetic devices by a human with tetraplegia. Nature 442:164–171
Howard G, Goff DC (2012) Population shifts and the future of stroke: forecasts of the future burden of stroke. Ann N Y Acad Sci 1268:14–20
Hummel FC, Cohen LG (2006) Non-invasive brain stimulation: a new strategy to improve neurorehabilitation after stroke? Lancet Neurol 5:708–712
Hummel F, Kirsammer R, Gerloff C (2003) Ipsilateral cortical activation during finger sequences of increasing complexity: representation of movement difficulty or memory load? Clin Neurophysiol 114:605–613
Jean-Charles L, Nepveu JF, Deffeyes JE, Elgbeili G, Dancause N, Barthelemy D (2017) Interhemispheric interactions between trunk muscle representations of the primary motor cortex. J Neurophysiol 118:1488–1500
Johansen-Berg H, Dawes H, Guy C, Smith SM, Wade DT, Matthews PM (2002) Correlation between motor improvements and altered fMRI activity after rehabilitative therapy. Brain 125:2731–2742
Kalaska JF (2009) From intention to action: motor cortex and the control of reaching movements. Adv Exp Med Biol 629:139–178
Khedr EM, Abdel-Fadeil MR, Farghali A, Qaid M (2009) Role of 1 and 3 Hz repetitive transcranial magnetic stimulation on motor function recovery after acute ischaemic stroke. Eur J Neurol 16:1323–1330
Kim YH, You SH, Ko MH, Park JW, Lee KH, Jang SH, Yoo WK, Hallett M (2006) Repetitive transcranial magnetic stimulation-induced corticomotor excitability and associated motor skill acquisition in chronic stroke. Stroke 37:1471–1476
Kim SP, Simeral JD, Hochberg LR, Donoghue JP, Black MJ (2008) Neural control of computer cursor velocity by decoding motor cortical spiking activity in humans with tetraplegia. J Neural Eng 5:455–476
Kimberley TJ, Khandekar G, Borich M (2008) fMRI reliability in subjects with stroke. Exp Brain Res 186:183–190
Koch G, Ruge D, Cheeran B, Fernandez Del Olmo M, Pecchioli C, Marconi B, Versace V, Lo Gerfo E, Torriero S, Oliveri M et al (2009) TMS activation of interhemispheric pathways between the posterior parietal cortex and the contralateral motor cortex. J Physiol 587:4281–4292
Kuppuswamy A, Catley M, King NK, Strutton PH, Davey NJ, Ellaway PH (2008) Cortical control of erector spinae muscles during arm abduction in humans. Gait Posture 27:478–484
Langhorne P, Coupar F, Pollock A (2009) Motor recovery after stroke: a systematic review. Lancet Neurol 8:741–754
Langhorne P, Bernhardt J, Kwakkel G (2011) Stroke rehabilitation. Lancet 377:1693–1702
Latash M, Anson J (1996) What are “normal movements” in atypical populations? Behav Brain Sci 19:55–106
Lemon RN, Johansson RS, Westling G (1995) Corticospinal control during reach, grasp, and precision lift in man. J Neurosci 15:6145–6156
Levin MF, Feldman AG (1994) The role of stretch reflex threshold regulation in normal and impaired motor control. Brain Res 657:23–30
Levin MF, Kleim JA, Wolf SL (2009) What do motor “recovery” and “compensation” mean in patients following stroke? Neurorehabil Neural Repair 23:313–319
Lotze M, Markert J, Sauseng P, Hoppe J, Plewnia C, Gerloff C (2006) The role of multiple contralesional motor areas for complex hand movements after internal capsular lesion. J Neurosci 26:6096–6102
Maggiolini E, Viaro R, Franchi G (2008) Suppression of activity in the forelimb motor cortex temporarily enlarges forelimb representation in the homotopic cortex in adult rats. Eur J Neurosci 27:2733–2746
Mark LS, Nemeth K, Gardner D, Dainoff MJ, Paasche J, Duffy M, Grandt K (1997) Postural dynamics and the preferred critical boundary for visually guided reaching. J Exp Psychol Hum Percept Perform 23:1365–1379
McCrea PH, Eng JJ, Hodgson AJ (2005) Saturated muscle activation contributes to compensatory reaching strategies after stroke. J Neurophysiol 94:2999–3008
McDonnell MN, Stinear CM (2017) TMS measures of motor cortex function after stroke: a meta-analysis. Brain Stimul 10:721–734
McKiernan BJ, Marcario JK, Karrer JH, Cheney PD (1998) Corticomotoneuronal postspike effects in shoulder, elbow, wrist, digit, and intrinsic hand muscles during a reach and prehension task. J Neurophysiol 80:1961–1980
Michaelsen SM, Levin MF (2004) Short-term effects of practice with trunk restraint on reaching movements in patients with chronic stroke: a controlled trial. Stroke 35:1914–1919
Michaelsen SM, Luta A, Roby-Brami A, Levin MF (2001) Effect of trunk restraint on the recovery of reaching movements in hemiparetic patients. Stroke 32:1875–1883
Mohajerani MH, Aminoltejari K, Murphy TH (2011) Targeted mini-strokes produce changes in interhemispheric sensory signal processing that are indicative of disinhibition within minutes. Proc Natl Acad Sci USA 108:E183–191
Mohapatra S, Harrington R, Chan E, Dromerick AW, Breceda EY, Harris-Love M (2016) Role of contralesional hemisphere in paretic arm reaching in patients with severe arm paresis due to stroke: a preliminary report. Neurosci Lett 617:52–58
Mozaffarian D, Benjamin EJ, Go AS, Arnett DK, Blaha MJ, Cushman M, Das SR, de Ferranti S, Despres JP, Fullerton HJ et al (2016) Heart disease and stroke statistics-2016 update: a report from the American Heart Association. Circulation 133:e38–360
Murase N, Duque J, Mazzocchio R, Cohen LG (2004) Influence of interhemispheric interactions on motor function in chronic stroke. Ann Neurol 55:400–409
Murphy JT, Wong YC, Kwan HC (1985) Sequential activation of neurons in primate motor cortex during unrestrained forelimb movement. J Neurophysiol 53:435–445
Newton JM, Ward NS, Parker GJ, Deichmann R, Alexander DC, Friston KJ, Frackowiak RS (2006) Non-invasive mapping of corticofugal fibres from multiple motor areas–relevance to stroke recovery. Brain 129:1844–1858
Nowak DA, Grefkes C, Ameli M, Fink GR (2009) Interhemispheric competition after stroke: brain stimulation to enhance recovery of function of the affected hand. Neurorehabil Neural Repair 23:641–656
Nudo RJ (2013) Recovery after brain injury: mechanisms and principles. Front Hum Neurosci 7:887
Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113
Ovbiagele B, Goldstein LB, Higashida RT, Howard VJ, Johnston SC, Khavjou OA, Lackland DT, Lichtman JH, Mohl S, Sacco RL et al (2013) Forecasting the future of stroke in the United States: a policy statement from the American Heart Association and American Stroke Association. Stroke 44:2361–2375
Page SJ, Szaflarski JP, Eliassen JC, Pan H, Cramer SC (2009) Cortical plasticity following motor skill learning during mental practice in stroke. Neurorehabil Neural Repair 23:382–388
Platz T, Eickhof C, van Kaick S, Engel U, Pinkowski C, Kalok S, Pause M (2005) Impairment-oriented training or Bobath therapy for severe arm paresis after stroke: a single-blind, multicentre randomized controlled trial. Clin Rehabil 19:714–724
Platz T, van Kaick S, Mehrholz J, Leidner O, Eickhof C, Pohl M (2009) Best conventional therapy versus modular impairment-oriented training for arm paresis after stroke: a single-blind, multicenter randomized controlled trial. Neurorehabil Neural Repair 23:706–716
Rehme AK, Fink GR, von Cramon DY, Grefkes C (2011) The role of the contralesional motor cortex for motor recovery in the early days after stroke assessed with longitudinal FMRI. Cereb Cortex 21:756–768
Riecker A, Groschel K, Ackermann H, Schnaudigel S, Kassubek J, Kastrup A (2010) The role of the unaffected hemisphere in motor recovery after stroke. Hum Brain Mapp 31:1017–1029
Robertson JV, Roby-Brami A (2011) The trunk as a part of the kinematic chain for reaching movements in healthy subjects and hemiparetic patients. Brain Res 1382:137–146
Roby-Brami A, Feydy A, Combeaud M, Biryukova EV, Bussel B, Levin MF (2003) Motor compensation and recovery for reaching in stroke patients. Acta Neurol Scand 107:369–381
Saltzman E, Kelso JA (1987) Skilled actions: a task-dynamic approach. Psychol Rev 94:84–106
Schieber MH (1999) Somatotopic gradients in the distributed organization of the human primary motor cortex hand area: evidence from small infarcts. Exp Brain Res 128:139–148
Schouten EA, Schiemanck SK, Brand N, Post MW (2009) Long-term deficits in episodic memory after ischemic stroke: evaluation and prediction of verbal and visual memory performance based on lesion characteristics. J Stroke Cerebrovasc Dis 18:128–138
Schwerin S, Dewald JP, Haztl M, Jovanovich S, Nickeas M, MacKinnon C (2008) Ipsilateral versus contralateral cortical motor projections to a shoulder adductor in chronic hemiparetic stroke: implications for the expression of arm synergies. Exp Brain Res 185:509–519
Seniow J, Bilik M, Lesniak M, Waldowski K, Iwanski S, Czlonkowska A (2012) Transcranial magnetic stimulation combined with physiotherapy in rehabilitation of poststroke hemiparesis: a randomized, double-blind, placebo-controlled study. Neurorehabil Neural Repair 26:1072–1079
Shelton FN, Reding MJ (2001) Effect of lesion location on upper limb motor recovery after stroke. Stroke 32:107–112
Shibasaki H, Sadato N, Lyshkow H, Yonekura Y, Honda M, Nagamine T, Suwazono S, Magata Y, Ikeda A, Miyazaki M et al (1993) Both primary motor cortex and supplementary motor area play an important role in complex finger movement. Brain 116(Pt 6):1387–1398
Shimizu T, Hosaki A, Hino T, Sato M, Komori T, Hirai S, Rossini PM (2002) Motor cortical disinhibition in the unaffected hemisphere after unilateral cortical stroke. Brain 125:1896–1907
Sommerfeld DK, Eek EU, Svensson AK, Holmqvist LW, von Arbin MH (2004) Spasticity after stroke: its occurrence and association with motor impairments and activity limitations. Stroke 35:134–139
Soteropoulos DS, Williams ER, Baker SN (2012) Cells in the monkey ponto-medullary reticular formation modulate their activity with slow finger movements. J Physiol 590:4011–4027
Stewart JC, Cramer SC (2013) Patient-reported measures provide unique insights into motor function after stroke. Stroke 44:1111–1116
Swayne OB, Rothwell JC, Ward NS, Greenwood RJ (2008) Stages of motor output reorganization after hemispheric stroke suggested by longitudinal studies of cortical physiology. Cereb Cortex 18:1909–1922
Takeuchi N, Chuma T, Matsuo Y, Watanabe I, Ikoma K (2005) Repetitive transcranial magnetic stimulation of contralesional primary motor cortex improves hand function after stroke. Stroke 36:2681–2686
Takeuchi N, Tada T, Toshima M, Chuma T, Matsuo Y, Ikoma K (2008) Inhibition of the unaffected motor cortex by 1 Hz repetitive transcranical magnetic stimulation enhances motor performance and training effect of the paretic hand in patients with chronic stroke. J Rehabil Med 40:298–303
Takeuchi N, Tada T, Matsuo Y, Ikoma K (2012) Low-frequency repetitive TMS plus anodal transcranial DCS prevents transient decline in bimanual movement induced by contralesional inhibitory rTMS after stroke. Neurorehabil Neural Repair 26:988–998
Taub E, Miller NE, Novack TA, Cook EW 3rd, Fleming WC, Nepomuceno CS, Connell JS, Crago JE (1993) Technique to improve chronic motor deficit after stroke. Arch Phys Med Rehabil 74:347–354
Thielman G (2013) Insights into upper limb kinematics and trunk control one year after task-related training in chronic post-stroke individuals. J Hand Ther 26:156–160 (quiz 161)
Turton AJ, Cunningham P, Heron E, van Wijck F, Sackley C, Rogers C, Wheatley K, Jowett S, Wolf SL, van Vliet P (2013) Home-based reach-to-grasp training for people after stroke: study protocol for a feasibility randomized controlled trial. Trials 14:109
Vaidya M, Kording K, Saleh M, Takahashi K, Hatsopoulos NG (2015) Neural coordination during reach-to-grasp. J Neurophysiol 114:1827–1836
Vargas-Irwin CE, Shakhnarovich G, Yadollahpour P, Mislow JM, Black MJ, Donoghue JP (2010) Decoding complete reach and grasp actions from local primary motor cortex populations. J Neurosci 30:9659–9669
Velliste M, Perel S, Spalding MC, Whitford AS, Schwartz AB (2008) Cortical control of a prosthetic arm for self-feeding. Nature 453:1098–1101
Verstynen T, Diedrichsen J, Albert N, Aparicio P, Ivry RB (2005) Ipsilateral motor cortex activity during unimanual hand movements relates to task complexity. J Neurophysiol 93:1209–1222
Ward NS (2006) The neural substrates of motor recovery after focal damage to the central nervous system. Arch Phys Med Rehabil 87:S30–35
Ward NS, Cohen LG (2004) Mechanisms underlying recovery of motor function after stroke. Arch Neurol 61:1844–1848
Ward NS, Brown MM, Thompson AJ, Frackowiak RS (2003) Neural correlates of outcome after stroke: a cross-sectional fMRI study. Brain 126:1430–1448
Werhahn KJ, Conforto AB, Kadom N, Hallett M, Cohen LG (2003) Contribution of the ipsilateral motor cortex to recovery after chronic stroke. Ann Neurol 54:464–472
Wolf SL, Winstein CJ, Miller JP, Taub E, Uswatte G, Morris D, Giuliani C, Light KE, Nichols-Larsen D (2006) Effect of constraint-induced movement therapy on upper extremity function 3 to 9 months after stroke: the EXCITE randomized clinical trial. JAMA 296:2095–2104
Ziemann U, Ishii K, Borgheresi A, Yaseen Z, Battaglia F, Hallett M, Cincotta M, Wassermann EM (1999) Dissociation of the pathways mediating ipsilateral and contralateral motor-evoked potentials in human hand and arm muscles. J Physiol 518(Pt 3):895–906
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We thank Andrew Apostol for assistance with data analysis.
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This study was funded by American Heart Association (0860041Z to Dr. Cirstea). The Hoglund Brain Imaging Center is supported by a generous gift from Forrest and Sally Hoglund and National Institutes of Health (P30 AG035982, UL1 RR033179). There are no financial benefits to the authors. The authors declared that they have no conflict of interest.
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Bani-Ahmed, A., Cirstea, C.M. Ipsilateral primary motor cortex and behavioral compensation after stroke: a case series study. Exp Brain Res 238, 439–452 (2020). https://doi.org/10.1007/s00221-020-05728-8
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DOI: https://doi.org/10.1007/s00221-020-05728-8