Top

Published in:

Open Access 01-12-2023 | Research

Participant attention on the intervention target during repetitive passive movement improved spinal reciprocal inhibition enhancement and joint movement function

Authors: Ryo Hirabayashi, Mutsuaki Edama, Mai Takeda, Yuki Yamada, Hirotake Yokota, Chie Sekine, Hideaki Onishi

Published in: European Journal of Medical Research | Issue 1/2023

Abstract

This study aimed to evaluate the effects of the participant’s attention target during repetitive passive movement (RPM) intervention on reciprocal inhibition (RI) and joint movement function. Twenty healthy adults participated in two experiments involving four attention conditions [control (forward attention with no RPM), forward attention (during RPM), monitor attention (monitor counting task during RPM), ankle joint attention (ankle movement counting task during RPM)] during 10-min RPM interventions on the ankle joint. Counting tasks were included to ensure the participant’s attention remained on the target during the intervention. In Experiment 1, RI was measured before, immediately after, and 5, 10, 15, 20, and 30 min after the RPM intervention. In Experiment 2, we evaluated ankle joint movement function at the same time points before and after RPM intervention. The maximum ankle dorsiflexion movement (from 30° plantar flexion to 10° dorsiflexion) was measured, reflecting RI. In Experiment 1, the RI function reciprocal Ia inhibition was enhanced for 10 min after RPM under all attention conditions (excluding the control condition. D1 inhibition was enhanced for 20 min after RPM in the forward and monitor attention conditions and 30 min after RPM in the ankle joint attention condition. In Experiment 2, the joint movement function decreased under the forward and monitor attention conditions but improved under the ankle joint attention condition. This study is the first to demonstrate that the participant’s attention target affected the intervention effect of the RI enhancement method, which has implications for improving the intervention effect of rehabilitation.

Hayashi A, Kagamihara Y, Nakajima Y, Narabayashi H, Okuma Y, Tanaka R. Disorder in reciprocal innervation upon initiation of voluntary movement in patients with Parkinson’s disease. Exp Brain Res. 1988;70:437–40.PubMed

Kagamihara Y, Ohi K, Tanaka R. Disorder in reciprocal inhibition upon initiation of voluntary ankle dorsiflexion movement in cerebellar motor disorders. In M. Mano, I. Hamada, & M. Delong (Eds.), Role of the cerebellum and basal ganglia in voluntary movement. 1993;33–40. New York, NY: Elsevier Science.

Kagamihara Y, Tanaka R. Disorder of the reciprocal Ia inhibitory pathway in spasticity. In: Recent Advances in Clinical Neurophysiology. 1996;859–62.

Nagai K, Yamada M, Uemura K, Yamada Y, Ichihashi N, Tsuboyama T. Differences in muscle coactivation during postural control between healthy older and young adults. Arch Gerontol Geriatr. 2011;53:338–43.PubMed

Hortobagyi T, Solnik S, Gruber A, Rider P, Steinweg K, Helseth J, et al. Interaction between age and gait velocity in the amplitude and timing of antagonist muscle coactivation. Gait Posture. 2009;29:558–64.PubMed

Hortobagyi T, Devita P. Mechanisms responsible for the age-associated increase in coactivation of antagonist muscles. Exerc Sport Sci Rev. 2006;34:29–35.PubMed

Morita H, Shindo M, Yanagawa S, Yoshida T, Momoi H, Yanagisawa N. Progressive decrease in heteronymous monosynaptic Ia facilitation with human ageing. Exp Brain Res. 1995;104:167–70.PubMed

Morita H, Shindo M, Ikeda S, Yanagisawa N. Decrease in presynaptic inhibition on heteronymous monosynaptic Ia terminals in patients with Parkinson’s disease. Mov Disord. 2000;15:830–4.PubMed

Baudry S, Maerz AH, Enoka RM. Presynaptic modulation of Ia afferents in young and old adults when performing force and position control. J Neurophysiol. 2010;103:623–31.PubMed

10.

Bhagchandani N, Schindler-Ivens S. Reciprocal inhibition post-stroke is related to reflex excitability and movement ability. Clin Neurophysiol. 2012;123:2239–46.PubMedPubMedCentral

11.

Fung J, Barbeau H. A dynamic EMG profile index to quantify muscular activation disorder in spastic paretic gait. Electroencephalogr Clin Neurophysiol. 1989;73:233–44.PubMed

12.

Hirabayashi R, Edama M, Kojima S, Miyaguchi S, Onishi H. Effects of repetitive passive movement on ankle joint on spinal reciprocal inhibition. Exp Brain Res. 2019;237:3409–17.PubMed

13.

Hirabayashi R, Edama M, Kojima S, Miyaguchi S, Onishi H. Enhancement of spinal reciprocal inhibition depends on the movement speed and range of repetitive passive movement. Eur J Neurosci. 2020;52:3929–43.PubMed

14.

Hirabayashi R, Kojima S, Edama M, Onishi H. Activation of the supplementary motor areas enhances spinal reciprocal inhibition in healthy individuals. Brain Sci. 2020;10(9):587.PubMedPubMedCentral

15.

Perez MA, Field-Fote EC, Floeter MK. Patterned sensory stimulation induces plasticity in reciprocal ia inhibition in humans. J Neurosci. 2003;23:2014–8.PubMedPubMedCentral

16.

Roche N, Lackmy A, Achache V, Bussel B, Katz R. Impact of transcranial direct current stimulation on spinal network excitability in humans. J Physiol. 2009;587:5653–64.PubMedPubMedCentral

17.

Fujiwara T, Tsuji T, Honaga K, Hase K, Ushiba J, Liu M. Transcranial direct current stimulation modulates the spinal plasticity induced with patterned electrical stimulation. Clin Neurophysiol. 2011;122:1834–7.PubMed

18.

Roche N, Lackmy A, Achache V, Bussel B, Katz R. Effects of anodal transcranial direct current stimulation over the leg motor area on lumbar spinal network excitability in healthy subjects. J Physiol. 2011;589:2813–26.PubMedPubMedCentral

19.

Jessop T, DePaola A, Casaletto L, Englard C, Knikou M. Short-term plasticity of human spinal inhibitory circuits after isometric and isotonic ankle training. Eur J Appl Physiol. 2013;113:273–84.PubMed

20.

Kubota S, Hirano M, Morishita T, Uehara K, Funase K. Patterned sensory nerve stimulation enhances the reactivity of spinal Ia inhibitory interneurons. NeuroReport. 2015;26:249–53.PubMed

21.

Yamaguchi T, Fujiwara T, Tsai YA, Tang SC, Kawakami M, Mizuno K, et al. The effects of anodal transcranial direct current stimulation and patterned electrical stimulation on spinal inhibitory interneurons and motor function in patients with spinal cord injury. Exp Brain Res. 2016;234:1469–78.PubMedPubMedCentral

22.

Ritzmann R, Krause A, Freyler K, Gollhofer A. Acute whole-body vibration increases reciprocal inhibition. Hum Mov Sci. 2018;60:191–201.PubMed

23.

Yamaguchi T, Fujiwara T, Lin SC, Takahashi Y, Hatori K, Liu M, et al. Priming with intermittent theta burst transcranial magnetic stimulation promotes spinal plasticity induced by peripheral patterned electrical stimulation. Front Neurosci. 2018;12:508.PubMedPubMedCentral

24.

Takahashi Y, Fujiwara T, Yamaguchi T, Kawakami M, Mizuno K, Liu M. The effects of patterned electrical stimulation combined with voluntary contraction on spinal reciprocal inhibition in healthy individuals. NeuroReport. 2017;28:434–8.PubMed

25.

Takahashi Y, Kawakami M, Yamaguchi T, Idogawa Y, Tanabe S, Kondo K, et al. Effects of leg motor imagery combined with electrical stimulation on plasticity of corticospinal excitability and spinal reciprocal inhibition. Front Neurosci. 2019;13:149.PubMedPubMedCentral

26.

Passingham RE. Attention to action. Philos Trans R Soc Lond B Biol Sci. 1996;351:1473–9.PubMed

27.

Hazeltine E, Grafton ST, Ivry R. Attention and stimulus characteristics determine the locus of motor-sequence encoding. A PET study. Brain. 1997;120:123–40.PubMed

28.

Liao CM, Masters RS. Analogy learning: a means to implicit motor learning. J Sports Sci. 2001;19:307–19.PubMed

29.

Wulf G, Lewthwaite R. Optimizing performance through intrinsic motivation and attention for learning: the OPTIMAL theory of motor learning. Psychon Bull Rev. 2016;23:1382–414.PubMed

30.

Jueptner M, Stephan KM, Frith CD, Brooks DJ, Frackowiak RS, Passingham RE. Anatomy of motor learning. I. Frontal cortex and attention to action. J Neurophysiol. 1997;77:1313–24.PubMed

31.

Rowe J, Friston K, Frackowiak R, Passingham R. Attention to action: specific modulation of corticocortical interactions in humans. Neuroimage. 2002;17:988–98.PubMed

32.

Tsuiki S, Sasaki R, Pham MV, Miyaguchi S, Kojima S, Saito K, et al. Repetitive passive movement modulates corticospinal excitability: effect of movement and rest cycles and subject attention. Front Behav Neurosci. 2019;13:38.PubMedPubMedCentral

33.

Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G. Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kinesiol. 2000;10:361–74.PubMed

34.

Crone C, Hultborn H, Jespersen B, Nielsen J. Reciprocal Ia inhibition between ankle flexors and extensors in man. J Physiol. 1987;389:163–85.PubMedPubMedCentral

35.

Takada Y, Miyahara T, Tanaka T, Ohyama T, Nakamura Y. Modulation of H reflex of pretibial muscles and reciprocal Ia inhibition of soleus muscle during voluntary teeth clenching in humans. J Neurophysiol. 2000;83:2063–70.PubMed

36.

Mizuno Y, Tanaka R, Yanagisawa N. Reciprocal group I inhibition on triceps surae motoneurons in man. J Neurophysiol. 1971;34:1010–7.PubMed

37.

Nielsen J, Kagamihara Y. The regulation of disynaptic reciprocal Ia inhibition during co-contraction of antagonistic muscles in man. J Physiol. 1992;456:373–91.PubMedPubMedCentral

38.

Falconer K, Winter DA. Quantitative assessment of co-contraction at the ankle joint in walking. Electromyogr Clin Neurophysiol. 1985;25:135–49.PubMed

39.

Jankowska E, McCrea D, Rudomin P, Sykova E. Observations on neuronal pathways subserving primary afferent depolarization. J Neurophysiol. 1981;46:506–16.PubMed

40.

Meunier S, Pierrot-Deseilligny E. Cortical control of presynaptic inhibition of Ia afferents in humans. Exp Brain Res. 1998;119:415–26.PubMed

41.

Nielsen J, Petersen N, Deuschl G, Ballegaard M. Task-related changes in the effect of magnetic brain stimulation on spinal neurones in man. J Physiol. 1993;471:223–43.PubMedPubMedCentral

42.

Masakado Y, Muraoka Y, Tomita Y, Chino N. The effect of transcranial magnetic stimulation on reciprocal inhibition in the human leg. Electromyogr Clin Neurophysiol. 2001;41:429–32.PubMed

43.

Yamaguchi T, Moriya K, Tanabe S, Kondo K, Otaka Y, Tanaka S. Transcranial direct-current stimulation combined with attention increases cortical excitability and improves motor learning in healthy volunteers. J Neuroeng Rehabil. 2020;17:23.PubMedPubMedCentral

44.

Mirdamadi JL, Suzuki LY, Meehan SK. Attention modulates specific motor cortical circuits recruited by transcranial magnetic stimulation. Neuroscience. 2017;359:151–8.PubMed

45.

Teo WP, Rodrigues JP, Mastaglia FL, Thickbroom GW. Changes in corticomotor excitability and inhibition after exercise are influenced by hand dominance and motor demand. Neuroscience. 2012;210:110–7.PubMed

46.

Teo WP, Rodrigues JP, Mastaglia FL, Thickbroom GW. Post-exercise depression in corticomotor excitability after dynamic movement: a general property of fatiguing and non-fatiguing exercise. Exp Brain Res. 2012;216:41–9.PubMed

47.

Zanette G, Bonato C, Polo A, Tinazzi M, Manganotti P, Fiaschi A. Long-lasting depression of motor-evoked potentials to transcranial magnetic stimulation following exercise. Exp Brain Res. 1995;107:80–6.PubMed

48.

Bonato C, Zanette G, Polo A, Bongiovanni G, Manganotti P, Tinazzi M, et al. Cortical output modulation after rapid repetitive movements. Ital J Neurol Sci. 1994;15:489–94.PubMed

49.

Teo WP, Rodrigues JP, Mastaglia FL, Thickbroom GW. Modulation of corticomotor excitability after maximal or sustainable-rate repetitive finger movement is impaired in Parkinson’s disease and is reversed by levodopa. Clin Neurophysiol. 2014;125:562–8.PubMed

50.

Miyaguchi S, Onishi H, Kojima S, Sugawara K, Tsubaki A, Kirimoto H, et al. Corticomotor excitability induced by anodal transcranial direct current stimulation with and without non-exhaustive movement. Brain Res. 2013;1529:83–91.PubMed

51.

Miyaguchi S, Kojima S, Kirimoto H, Tamaki H, Onishi H. Do differences in levels, types, and duration of muscle contraction have an effect on the degree of post-exercise depression? Front Hum Neurosci. 2016 Apr 29;10:159. CrossRefPubMedPubMedCentral

52.

Sasaki R, Nakagawa M, Tsuiki S, Miyaguchi S, Kojima S, Saito K, et al. Regulation of primary motor cortex excitability by repetitive passive finger movement frequency. Neuroscience. 2017;357:232–40.PubMed

53.

Rosenkranz K, Rothwell JC. Differential effect of muscle vibration on intracortical inhibitory circuits in humans. J Physiol. 2003;551:649–60.PubMedPubMedCentral

54.

Tokimura H, Di Lazzaro V, Tokimura Y, Oliviero A, Profice P, Insola A, et al. Short latency inhibition of human hand motor cortex by somatosensory input from the hand. J Physiol. 2000;523:503–13.PubMedPubMedCentral

55.

Ziemann U, Lönnecker S, Steinhoff BJ, Paulus W. Effects of antiepileptic drugs on motor cortex excitability in humans: a transcranial magnetic stimulation study. Ann Neurol. 1996;40:367–78.PubMed

56.

Ziemann U, Lönnecker S, Steinhoff BJ, Paulus W. The effect of lorazepam on the motor cortical excitability in man. Exp Brain Res. 1996;109:127–35.PubMed

57.

Sasaki R, Tsuiki S, Miyaguchi S, Kojima S, Saito K, Inukai Y, et al. Repetitive Passive Finger Movement Modulates Primary Somatosensory Cortex Excitability. Front Hum Neurosci. 2018;12:332.PubMedPubMedCentral

Title: Participant attention on the intervention target during repetitive passive movement improved spinal reciprocal inhibition enhancement and joint movement function
Authors: Ryo Hirabayashi
Mutsuaki Edama
Mai Takeda
Yuki Yamada
Hirotake Yokota
Chie Sekine
Hideaki Onishi
Publication date: 01-12-2023
Publisher: BioMed Central
Published in: European Journal of Medical Research / Issue 1/2023
Electronic ISSN: 2047-783X
DOI: https://doi.org/10.1186/s40001-023-01418-7

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Participant attention on the intervention target during repetitive passive movement improved spinal reciprocal inhibition enhancement and joint movement function

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2023

Effects of low-level laser therapy on orthodontic miniscrew stability: a systematic review

The global prevalence of primary central nervous system tumors: a systematic review and meta-analysis

The prediction of in-hospital mortality in chronic kidney disease patients with coronary artery disease using machine learning models

Malaria amongst children under five in sub-Saharan Africa: a scoping review of prevalence, risk factors and preventive interventions

Characterization of genotypes and antimicrobial resistance profiles of clinical isolates of Shigella from patients in the southern region of Iran

Potential ‘anti-cancer’ effects of esketamine on proliferation, apoptosis, migration and invasion in esophageal squamous carcinoma cells