Skip to main content
Log in

Neural mechanism of selective finger movement independent of synergistic movement

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

Abstract

Muscle synergy is important for simplifying functional movement, which constitutes spatiotemporal patterns of activity across muscles. To execute selective finger movements that are independent of synergistic movement patterns, we hypothesized that inhibitory neural activity is necessary to suppress enslaved finger movement caused by synergist muscles. To test this hypothesis, we focused on a pair of synergist muscles used in the hand opening movement, namely the index finger abductor and little finger abductor (abductor digiti minimi; ADM), and examined whether inhibitory neural activity in ADM occurs during selective index finger abduction/adduction movements and/or its imagery using transcranial magnetic stimulation and F-wave analysis. During the index finger adduction movement, background EMG activity, F-wave persistence, and motor evoked potential (MEP) amplitude in ADM were elevated. However, during the index finger abduction movement, ADM MEP amplitude remained unchanged despite increased background EMG activity and F-wave persistence. These results suggest that increased spinal excitability in ADM is counterbalanced by cortical-mediated inhibition only during selective index finger abduction movement. This assumption was further supported by the results of motor imagery experiments. Although F-wave persistence in ADM increased only during motor imagery of index finger abduction, ADM MEP amplitude during motor imagery of index finger abduction was significantly lower than that during adduction. Overall, our findings indicate that cortical-mediated inhibition contributes to the execution of selective finger movements that are independent of synergistic hand movement patterns.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aoyama T, Kaneko F, Ohashi Y, Kohno Y (2019) Dissociation between cortical and spinal excitability of the antagonist muscle during combined motor imagery and action observation. Sci Rep 9:13120

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Beck S, Richardson SP, Shamim EA, Dang N, Schubert M, Hallett M (2008) Short intracortical and surround inhibition are selectively reduced during movement initiation in focal hand dystonia. J Neurosci 28:10363–10369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Capaday C, Devanne H, Bertrand L, Lavoie BA (1998) Intracortical connections between motor cortical zones controlling antagonistic muscles in the cat: a combined anatomical and physiological study. Exp Brain Res 120:223–232

    Article  CAS  PubMed  Google Scholar 

  • Capaday C, Ethier C, Brizzi L, Sik A, van Vreeswijk C, Gingras D (2009) On the nature of the intrinsic connectivity of the cat motor cortex: evidence for a recurrent neural network topology. J Neurophysiol 102:2131–2141

    Article  PubMed  Google Scholar 

  • Case LK, Pineda J, Ramachandran VS (2015) Common coding and dynamic interactions between observed, imagined, and experienced motor and somatosensory activity. Neuropsychologia 79:233–245

    Article  PubMed  PubMed Central  Google Scholar 

  • Cengiz B, Vuralli D, Zinnuroglu M et al (2018) Analysis of mirror neuron system activation during action observation alone and action observation with motor imagery tasks. Exp Brain Res 236:497–503

    Article  PubMed  Google Scholar 

  • Chang WH, Fried PJ, Saxena S, Jannati A, Gomes-Osman J, Kim YH, Pascual-Leone A (2016) Optimal number of pulses as outcome measures of neuronavigated transcranial magnetic stimulation. Clin Neurophysiol 127:2892–2897

    Article  PubMed  PubMed Central  Google Scholar 

  • Connolly KJ, Forssberg H (1997) Neurophysiology and neuropsychology of motor development. Cambridge University Press, Cambridge

    Google Scholar 

  • de Winter JC, Gosling SD, Potter J (2016) Comparing the Pearson and Spearman correlation coefficients across distributions and sample sizes: a tutorial using simulations and empirical data. Psychol Methods 21:273–290

    Article  PubMed  Google Scholar 

  • Decety J, Grezes J (1999) Neural mechanisms subserving the perception of human actions. Trends Cogn Sci 3:172–178

    Article  CAS  PubMed  Google Scholar 

  • Di Lazzaro V, Oliviero A, Saturno E et al (2001) The effect on corticospinal volleys of reversing the direction of current induced in the motor cortex by transcranial magnetic stimulation. Exp Brain Res 138:268–273

    Article  PubMed  Google Scholar 

  • Eaves DL, Riach M, Holmes PS, Wright DJ (2016) Motor imagery during action observation: a brief review of evidence, theory and future research opportunities. Front Neurosci 10:514

    Article  PubMed  PubMed Central  Google Scholar 

  • Ehrsson HH, Kuhtz-Buschbeck JP, Forssberg H (2002) Brain regions controlling nonsynergistic versus synergistic movement of the digits: a functional magnetic resonance imaging study. J Neurosci 22:5074–5080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ethier C, Brizzi L, Giguere D, Capaday C (2007) Corticospinal control of antagonistic muscles in the cat. Eur J Neurosci 26:1632–1641

    Article  PubMed  Google Scholar 

  • Fadiga L, Buccino G, Craighero L, Fogassi L, Gallese V, Pavesi G (1999) Corticospinal excitability is specifically modulated by motor imagery: a magnetic stimulation study. Neuropsychologia 37:147–158

    Article  CAS  PubMed  Google Scholar 

  • Goldsworthy MR, Hordacre B, Ridding MC (2016) Minimum number of trials required for within- and between-session reliability of TMS measures of corticospinal excitability. Neuroscience 320:205–209

    Article  CAS  PubMed  Google Scholar 

  • Hager-Ross C, Schieber MH (2000) Quantifying the independence of human finger movements: comparisons of digits, hands, and movement frequencies. J Neurosci 20:8542–8550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasegaw Y, Kasai T, Kinoshita H, Yahagi S (2001) Modulation of a motor evoked response to transcranial magnetic stimulation by the activity level of the first dorsal interosseous muscle in humans when grasping a stationary object with different grip widths. Neurosci Lett 299:1–4

    Article  CAS  PubMed  Google Scholar 

  • Jacobs KM, Donoghue JP (1991) Reshaping the cortical motor map by unmasking latent intracortical connections. Science 251:944–947

    Article  CAS  PubMed  Google Scholar 

  • Jeannerod M (1995) Mental imagery in the motor context. Neuropsychologia 33:1419–1432

    Article  CAS  PubMed  Google Scholar 

  • Kaneko K, Kawai S, Fuchigami Y, Morita H, Ofuji A (1996) The effect of current direction induced by transcranial magnetic stimulation on the corticospinal excitability in human brain. Electroencephalogr Clin Neurophysiol 101:478–482

    CAS  PubMed  Google Scholar 

  • Kaneko F, Murakami T, Onari K, Kurumadani H, Kawaguchi K (2003) Decreased cortical excitability during motor imagery after disuse of an upper limb in humans. Clin Neurophysiol 114:2397–2403

    Article  PubMed  Google Scholar 

  • Kaneko N, Masugi Y, Yokoyama H, Nakazawa K (2018) Difference in phase modulation of corticospinal excitability during the observation of the action of walking, with and without motor imagery. NeuroReport 29:169–173

    Article  PubMed  Google Scholar 

  • Kazennikov O, Solopova I, Talis V, Ioffe M (2008) Anticipatory postural adjustment: the role of motor cortex in the natural and learned bimanual unloading. Exp Brain Res 186:215–223

    Article  PubMed  Google Scholar 

  • Malouin F, Richards CL, Jackson PL, Lafleur MF, Durand A, Doyon J (2007) The kinesthetic and visual imagery questionnaire (KVIQ) for assessing motor imagery in persons with physical disabilities: a reliability and construct validity study. J Neurol Phys Ther 31:20–29

    Article  PubMed  Google Scholar 

  • McMorland AJ, Runnalls KD, Byblow WD (2015) A neuroanatomical framework for upper limb synergies after stroke. Front Hum Neurosci 9:82

    Article  PubMed  PubMed Central  Google Scholar 

  • Mouthon A, Ruffieux J, Walchli M, Keller M, Taube W (2015) Task-dependent changes of corticospinal excitability during observation and motor imagery of balance tasks. Neuroscience 303:535–543

    Article  CAS  PubMed  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

    Article  CAS  PubMed  Google Scholar 

  • Park J, Xu D (2017) Multi-finger interaction and synergies in finger flexion and extension force production. Front Hum Neurosci 11:318

    Article  PubMed  PubMed Central  Google Scholar 

  • Reilly KT, Hammond GR (2000) Independence of force production by digits of the human hand. Neurosci Lett 290:53–56

    Article  CAS  PubMed  Google Scholar 

  • Reilly KT, Schieber MH (2003) Incomplete functional subdivision of the human multitendoned finger muscle flexor digitorum profundus: an electromyographic study. J Neurophysiol 90:2560–2570

    Article  PubMed  Google Scholar 

  • Rozand V, Lebon F, Papaxanthis C, Lepers R (2015) Effect of mental fatigue on speed-accuracy trade-off. Neuroscience 297:219–230

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto M, Muraoka T, Mizuguchi N, Kanosue K (2009) Combining observation and imagery of an action enhances human corticospinal excitability. Neurosci Res 65:23–27

    Article  PubMed  Google Scholar 

  • Santello M, Baud-Bovy G, Jörntell H (2013) Neural bases of hand synergies. Front Comput Neurosci 7:23

    Article  PubMed  PubMed Central  Google Scholar 

  • Schieber MH (1991) Individuated finger movements of rhesus monkeys: a means of quantifying the independence of the digits. J Neurophysiol 65:1381–1391

    Article  CAS  PubMed  Google Scholar 

  • Schieber MH, Hibbard LS (1993) How somatotopic is the motor cortex hand area? Science 261:489–492

    Article  CAS  PubMed  Google Scholar 

  • Schneider C, Devanne H, Lavoie BA, Capaday C (2002) Neural mechanisms involved in the functional linking of motor cortical points. Exp Brain Res 146:86–94

    Article  CAS  PubMed  Google Scholar 

  • Shinoda Y, Yokota J, Futami T (1981) Divergent projection of individual corticospinal axons to motoneurons of multiple muscles in the monkey. Neurosci Lett 23:7–12

    Article  CAS  PubMed  Google Scholar 

  • Slobounov S, Johnston J, Chiang H, Ray WJ (2002) Motor-related cortical potentials accompanying enslaving effect in single versus combination of fingers force production tasks. Clin Neurophysiol 113:1444–1453

    Article  CAS  PubMed  Google Scholar 

  • Sohn YH, Hallett M (2004) Surround inhibition in human motor system. Exp Brain Res 158:397–404

    Article  PubMed  Google Scholar 

  • Stinear CM, Byblow WD (2003) Role of intracortical inhibition in selective hand muscle activation. J Neurophysiol 89:2014–2020

    Article  PubMed  Google Scholar 

  • Stinear CM, Byblow WD (2004) Impaired modulation of intracortical inhibition in focal hand dystonia. Cereb Cortex 14:555–561

    Article  PubMed  Google Scholar 

  • Suzuki T, Bunno Y, Onigata C, Tani M, Uragami S, Yoshida S (2014) Excitability of spinal neural function during motor imagery in Parkinson’s disease. Funct Neurol 29:263–267

    PubMed  PubMed Central  Google Scholar 

  • Thirugnanasambandam N, Khera R, Wang H, Kukke SN, Hallett M (2015) Distinct interneuronal networks influence excitability of the surround during movement initiation. J Neurophysiol 114:1102–1108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wright DJ, Williams J, Holmes PS (2014) Combined action observation and imagery facilitates corticospinal excitability. Front Hum Neurosci 8:951

    PubMed  PubMed Central  Google Scholar 

  • Yahagi S, Shimura K, Kasai T (1996) An increase in cortical excitability with no change in spinal excitability during motor imagery. Percept Mot Skills 83:288–290

    Article  CAS  PubMed  Google Scholar 

  • Yahagi S, Takeda Y, Ni Z et al (2005) Modulations of input-output properties of corticospinal tract neurons by repetitive dynamic index finger abductions. Exp Brain Res 161:255–264

    Article  PubMed  Google Scholar 

  • Zatsiorsky VM, Li ZM, Latash ML (1998) Coordinated force production in multi-finger tasks: finger interaction and neural network modeling. Biol Cybern 79:139–150

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by JSPS KAKENHI [Grant #16K16433 (T.A.)].

Author information

Authors and Affiliations

Authors

Contributions

TA: contributed to the design of the study, data collection, data analysis, and manuscript preparation; FK: contributed to the design of the study, data analysis, and manuscript preparation; YO: contributed to data analysis and manuscript preparation; YK: contributed to data collection, data analysis, and manuscript preparation.

Corresponding author

Correspondence to Toshiyuki Aoyama.

Ethics declarations

Conflict of interest

The authors declare no financial and non-financial competing interests.

Additional information

Communicated by Winston D Byblow.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Aoyama, T., Kaneko, F., Ohashi, Y. et al. Neural mechanism of selective finger movement independent of synergistic movement. Exp Brain Res 237, 3485–3492 (2019). https://doi.org/10.1007/s00221-019-05693-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-019-05693-x

Keywords

Navigation