Top

Journal of NeuroEngineering and Rehabilitation

Published in:

Open Access 01-12-2024 | Stroke | Research

Video mirror feedback induces more extensive brain activation compared to the mirror box: an fNIRS study in healthy adults

Authors: Julien Bonnal, Canan Ozsancak, Fabrice Prieur, Pascal Auzou

Published in: Journal of NeuroEngineering and Rehabilitation | Issue 1/2024

Abstract

Background

Mirror therapy (MT) has been shown to be effective for motor recovery of the upper limb after a stroke. The cerebral mechanisms of mirror therapy involve the precuneus, premotor cortex and primary motor cortex. Activation of the precuneus could be a marker of this effectiveness. MT has some limitations and video therapy (VT) tools are being developed to optimise MT. While the clinical superiority of these new tools remains to be demonstrated, comparing the cerebral mechanisms of these different modalities will provide a better understanding of the related neuroplasticity mechanisms.

Methods

Thirty-three right-handed healthy individuals were included in this study. Participants were equipped with a near-infrared spectroscopy headset covering the precuneus, the premotor cortex and the primary motor cortex of each hemisphere. Each participant performed 3 tasks: a MT task (right hand movement and left visual feedback), a VT task (left visual feedback only) and a control task (right hand movement only). Perception of illusion was rated for MT and VT by asking participants to rate the intensity using a visual analogue scale. The aim of this study was to compare brain activation during MT and VT. We also evaluated the correlation between the precuneus activation and the illusion quality of the visual mirrored feedback.

Results

We found a greater activation of the precuneus contralateral to the visual feedback during VT than during MT. We also showed that activation of primary motor cortex and premotor cortex contralateral to visual feedback was more extensive in VT than in MT. Illusion perception was not correlated with precuneus activation.

Conclusion

VT led to greater activation of a parieto-frontal network than MT. This could result from a greater focus on visual feedback and a reduction in interhemispheric inhibition in VT because of the absence of an associated motor task. These results suggest that VT could promote neuroplasticity mechanisms in people with brain lesions more efficiently than MT.

Clinical trial registration

NCT04738851.

Ramachandran VS, Rogers-Ramachandran D, Cobb S. Touching the phantom limb. Nature. 1995;377:489–90.PubMedCrossRef

Altschuler EL, Wisdom SB, Stone L, Foster C, Galasko D, Llewellyn DME, et al. Rehabilitation of hemiparesis after stroke with a mirror. Lancet. 1999;353:2035.PubMedCrossRef

Zeng W, Guo Y, Wu G, Liu X, Fang Q. Mirror therapy for motor function of the upper extremity in patients with stroke: a meta-analysis. J Rehabil Med. 2018;50:8–15.PubMedCrossRef

Thieme H, Morkisch N, Mehrholz J, Pohl M, Behrens J, Borgetto B et al. Mirror therapy for improving motor function after stroke. Cochrane Database Syst Rev [Internet]. 2018 [cited 2021 Apr 30];2018. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6513639/.

Colomer C, Noé E, Llorens R. Mirror therapy in chronic stroke survivors with severely impaired upper limb function: a randomized controlled trial. Eur J Phys Rehabil Med. 2016;52:8.

Arya KN, Pandian S. Vikas null, Puri V. Mirror Illusion for Sensori-Motor Training in Stroke: a Randomized Controlled Trial. J Stroke Cerebrovasc Dis. 2018;27:3236–46.PubMedCrossRef

Darbois N, Guillaud A, Pinsault N. Do Robotics and Virtual Reality Add Real Progress to Mirror Therapy Rehabilitation? A Scoping Review. Rehabil Res Pract [Internet]. 2018 [cited 2021 Apr 30];2018. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6120256/.

Giraux P, Sirigu A. Illusory movements of the paralyzed limb restore motor cortex activity. NeuroImage. 2003;20(Suppl 1):S107–111.PubMedCrossRef

Li Y, Wu C, Hsieh Y, Lin K, Yao G, Chen C, et al. The Priming effects of Mirror Visual feedback on bilateral Task Practice: a randomized controlled study. Occup Therapy Int. 2019;2019:e3180306.CrossRef

10.

Chang C-S, Lo Y-Y, Chen C-L, Lee H-M, Chiang W-C, Li P-C. Alternative Motor Task-Based Pattern Training With a Digital Mirror Therapy System Enhances Sensorimotor Signal Rhythms Post-stroke. Front Neurol [Internet]. 2019 [cited 2021 Jun 12];10. https://www.frontiersin.org/articles/https://doi.org/10.3389/fneur.2019.01227/full.

11.

Hoermann S, dos Santos LF, Morkisch N, Jettkowski K, Sillis M, Devan H, et al. Computerised mirror therapy with augmented Reflection Technology for early stroke rehabilitation: clinical feasibility and integration as an adjunct therapy. Disabil Rehabil. 2017;39:1503–14.PubMedCrossRef

12.

Inagaki Y, Seki K, Makino H, Matsuo Y, Miyamoto T, Ikoma K. Exploring Hemodynamic Responses Using Mirror Visual Feedback With Electromyogram-Triggered Stimulation and Functional Near-Infrared Spectroscopy. Front Hum Neurosci [Internet]. 2019 [cited 2021 May 28];13. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6399579/.

13.

Bai Z, Fong KNK, Zhang J, Hu Z. Cortical mapping of mirror visual feedback training for unilateral upper extremity: a functional near-infrared spectroscopy study. Brain Behav. 2020;10:e01489.PubMedCrossRef

14.

Saleh S, Adamovich SV, Tunik E. Mirrored feedback in chronic stroke: recruitment and effective connectivity of ipsilesional sensorimotor networks. Neurorehabil Neural Repair. 2014;28:344–54.PubMedCrossRef

15.

Cheng C-H, Lin S-H, Wu C-Y, Liao Y-H, Chang K-C, Hsieh Y-W. Mirror Illusion modulates M1 activities and functional connectivity patterns of perceptual-attention circuits during Bimanual movements: a Magnetoencephalography Study. Front Neurosci. 2019;13:1363.PubMedCrossRef

16.

Mehnert J, Brunetti M, Steinbrink J, Niedeggen M, Dohle C. Effect of a mirror-like illusion on activation in the precuneus assessed with functional near-infrared spectroscopy. J Biomed Opt. 2013;18:066001.PubMedPubMedCentralCrossRef

17.

Michielsen ME, Smits M, Ribbers GM, Stam HJ, van der Geest JN, Bussmann JBJ, et al. The neuronal correlates of mirror therapy: an fMRI study on mirror induced visual illusions in patients with stroke. J Neurol Neurosurg Psychiatry. 2011;82:393–8.PubMedCrossRef

18.

Dohle C, Stephan KM, Valvoda JT, Hosseiny O, Tellmann L, Kuhlen T, et al. Representation of virtual arm movements in precuneus. Exp Brain Res. 2011;208:543–55.PubMedCrossRef

19.

Brunetti M, Morkisch N, Fritzsch C, Mehnert J, Steinbrink J, Niedeggen M, et al. Potential determinants of efficacy of mirror therapy in stroke patients–A pilot study. Restor Neurol Neurosci. 2015;33:421–34.PubMedPubMedCentral

20.

Cavanna AE, Trimble MR. The precuneus: a review of its functional anatomy and behavioural correlates. Brain. 2006;129:564–83.PubMedCrossRef

21.

Wang J, Fritzsch C, Bernarding J, Holtze S, Mauritz K-H, Brunetti M, et al. A comparison of neural mechanisms in mirror therapy and movement observation therapy. J Rehabil Med. 2013;45:410–3.PubMedCrossRef

22.

Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971;9:97–113.PubMedCrossRef

23.

Leff DR, Orihuela-Espina F, Elwell CE, Athanasiou T, Delpy DT, Darzi AW, et al. Assessment of the cerebral cortex during motor task behaviours in adults: a systematic review of functional near infrared spectroscopy (fNIRS) studies. NeuroImage. 2011;54:2922–36.PubMedCrossRef

24.

Bae SJ, Jang SH, Seo JP, Chang PH. The Optimal Speed for Cortical Activation of Passive Wrist Movements Performed by a Rehabilitation Robot: A Functional NIRS Study. Front Hum Neurosci [Internet]. 2017 [cited 2021 May 3];11. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5398011/.

25.

Lancaster JL, Woldorff MG, Parsons LM, Liotti M, Freitas CS, Rainey L, et al. Automated Talairach atlas labels for functional brain mapping. Hum Brain Mapp. 2000;10:120–31.PubMedPubMedCentralCrossRef

26.

Ye JC, Tak S, Jang KE, Jung J, Jang J. NIRS-SPM: statistical parametric mapping for near-infrared spectroscopy. NeuroImage. 2009;44:428–47.PubMedCrossRef

27.

Hoshi Y. Hemodynamic signals in fNIRS. Prog Brain Res. 2016;225:153–79.PubMedCrossRef

28.

Strangman G, Culver JP, Thompson JH, Boas DA. A quantitative comparison of simultaneous BOLD fMRI and NIRS recordings during functional brain activation. NeuroImage. 2002;17:719–31.PubMedCrossRef

29.

Huppert TJ, Diamond SG, Franceschini MA, Boas DA. HomER: a review of time-series analysis methods for near-infrared spectroscopy of the brain. Appl Opt. 2009;48:D280–298.PubMedPubMedCentralCrossRef

30.

Kocsis L, Herman P, Eke A. The modified Beer-Lambert law revisited. Phys Med Biol. 2006;51:N91–98.PubMedCrossRef

31.

Scholkmann F, Spichtig S, Muehlemann T, Wolf M. How to detect and reduce movement artifacts in near-infrared imaging using moving standard deviation and spline interpolation. Physiol Meas. 2010;31:649–62.PubMedCrossRef

32.

Benjamini Y, Hochberg Y. Controlling the false Discovery rate: a practical and powerful Approach to multiple testing. J Roy Stat Soc: Ser B (Methodol). 1995;57:289–300.CrossRef

33.

Zama T, Shimada S. Simultaneous measurement of electroencephalography and near-infrared spectroscopy during voluntary motor preparation. Sci Rep. 2015;5:16438.PubMedPubMedCentralCrossRef

34.

Wang J, Fritzsch C, Bernarding J, Krause T, Mauritz K-H, Brunetti M, et al. Cerebral activation evoked by the mirror illusion of the hand in stroke patients compared to normal subjects. NeuroRehabilitation. 2013;33:593–603.PubMedCrossRef

35.

Fattori P, Breveglieri R, Marzocchi N, Filippini D, Bosco A, Galletti C. Hand Orientation during Reach-to-grasp movements modulates neuronal activity in the medial posterior parietal area V6A. J Neurosci. 2009;29:1928–36.PubMedPubMedCentralCrossRef

36.

Rossiter HE, Borrelli MR, Borchert RJ, Bradbury D, Ward NS. Cortical mechanisms of Mirror Therapy after Stroke. Neurorehabil Neural Repair. 2015;29:444–52.PubMedCrossRef

37.

Simon O, Mangin JF, Cohen L, Le Bihan D, Dehaene S. Topographical layout of hand, eye, calculation, and language-related areas in the human parietal lobe. Neuron. 2002;33:475–87.PubMedCrossRef

38.

Molenberghs P, Cunnington R, Mattingley JB. Brain regions with mirror properties: a meta-analysis of 125 human fMRI studies. Neurosci Biobehavioral Reviews. 2012;36:341–9.CrossRef

39.

Jitsuishi T, Yamaguchi A. Characteristic cortico-cortical connection profile of human precuneus revealed by probabilistic tractography. Sci Rep. 2023;13:1936.PubMedPubMedCentralCrossRef

40.

Bonnal J, Ozsancak C, Monnet F, Valery A, Prieur F, Auzou P. Neural Substrates for Hand and Shoulder Movement in Healthy Adults: A Functional near Infrared Spectroscopy Study. Brain Topogr [Internet]. 2023 [cited 2023 May 22]; https://doi.org/10.1007/s10548-023-00972-x.

41.

Gueugneau N, Bove M, Ballay Y, Papaxanthis C. Interhemispheric inhibition is dynamically regulated during action observation. Cortex. 2016;78:138–49.PubMedCrossRef

42.

Bisio A, Biggio M, Avanzino L, Ruggeri P, Bove M. Kinaesthetic illusion shapes the cortical plasticity evoked by action observation. J Physiol. 2019;597:3233–45.PubMedCrossRef

43.

Grefkes C, Eickhoff SB, Nowak DA, Dafotakis M, Fink GR. Dynamic intra- and interhemispheric interactions during unilateral and bilateral hand movements assessed with fMRI and DCM. NeuroImage. 2008;41:1382–94.PubMedCrossRef

44.

Murase N, Duque J, Mazzocchio R, Cohen LG. Influence of interhemispheric interactions on motor function in chronic stroke. Ann Neurol. 2004;55:400–9.PubMedCrossRef

45.

Carter AR, Astafiev SV, Lang CE, Connor LT, Rengachary J, Strube MJ, et al. Resting interhemispheric functional magnetic resonance imaging connectivity predicts performance after stroke. Ann Neurol. 2010;67:365–75.PubMedPubMedCentralCrossRef

46.

Bartur G, Pratt H, Dickstein R, Frenkel-Toledo S, Geva A, Soroker N. Electrophysiological manifestations of mirror visual feedback during manual movement. Brain Res. 2015;1606:113–24.PubMedCrossRef

47.

Liepert J, Dettmers C, Terborg C, Weiller C. Inhibition of ipsilateral motor cortex during phasic generation of low force. Clin Neurophysiol. 2001;112:114–21.PubMedCrossRef

48.

Belyk M, Banks R, Tendera A, Chen R, Beal DS. Paradoxical facilitation alongside interhemispheric inhibition. Exp Brain Res. 2021;239:3303–13.PubMedPubMedCentralCrossRef

49.

Rizzolatti G, Craighero L. The Mirror-Neuron System. Annu Rev Neurosci. 2004;27:169–92.PubMedCrossRef

50.

Hardwick RM, Caspers S, Eickhoff SB, Swinnen SP. Neural correlates of action: comparing meta-analyses of imagery, observation, and execution. Neurosci Biobehav Rev. 2018;94:31–44.PubMedCrossRef

51.

Ge S, Liu H, Lin P, Gao J, Xiao C, Li Z. Neural Basis of Action Observation and understanding from First- and third-person perspectives: an fMRI study. Front Behav Neurosci. 2018;12:283.PubMedPubMedCentralCrossRef

52.

Hamzei F, Dettmers C, Rijntjes M, Glauche V, Kiebel S, Weber B, et al. Visuomotor control within a distributed parieto-frontal network. Exp Brain Res. 2002;146:273–81.PubMedCrossRef

53.

Bönstrup M, Schulz R, Schön G, Cheng B, Feldheim J, Thomalla G, et al. Parietofrontal network upregulation after motor stroke. Neuroimage Clin. 2018;18:720–9.PubMedPubMedCentralCrossRef

54.

Hamzei F, Erath G, Kücking U, Weiller C, Rijntjes M. Anatomy of brain lesions after stroke predicts effectiveness of mirror therapy. Eur J Neurosci. 2020;52:3628–41.PubMedCrossRef

55.

Bello UM, Chan CCH, Winser SJ. Task Complexity and Image Clarity Facilitate Motor and Visuo-Motor activities in Mirror Therapy in Post-stroke patients. Front Neurol. 2021;12:722846.PubMedPubMedCentralCrossRef

56.

Solodkin A, Hlustik P, Noll DC, Small SL. Lateralization of motor circuits and handedness during finger movements. Eur J Neurol. 2001;8:425–34.PubMedCrossRef

57.

Yuan X, Li Q, Gao Y, Liu H, Fan Z, Bu L. Age-related changes in brain functional networks under multisensory-guided hand movements assessed by the functional near – infrared spectroscopy. Neurosci Lett. 2022;781:136679.PubMedCrossRef

58.

Bello UM, Kranz GS, Winser SJ, Chan CCH. Neural Processes Underlying Mirror-Induced Visual Illusion: An Activation Likelihood Estimation Meta-Analysis. Front Hum Neurosci [Internet]. 2020 [cited 2021 May 12];14. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7412952/.

Title: Video mirror feedback induces more extensive brain activation compared to the mirror box: an fNIRS study in healthy adults
Authors: Julien Bonnal
Canan Ozsancak
Fabrice Prieur
Pascal Auzou
Publication date: 01-12-2024
Publisher: BioMed Central
Keyword: Stroke
Published in: Journal of NeuroEngineering and Rehabilitation / Issue 1/2024
Electronic ISSN: 1743-0003
DOI: https://doi.org/10.1186/s12984-024-01374-1

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Video mirror feedback induces more extensive brain activation compared to the mirror box: an fNIRS study in healthy adults

Abstract

Background

Methods

Results

Conclusion

Clinical trial registration

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusion

Clinical trial registration

Please log in to get access to this content

Other articles of this Issue 1/2024

Reminiscent music therapy combined with robot-assisted rehabilitation for elderly stroke patients: a pilot study

Correction: Effectiveness and therapeutic compliance of digital therapy in shoulder rehabilitation: a randomized controlled trial

Freezing of gait assessment with inertial measurement units and deep learning: effect of tasks, medication states, and stops

Improving physical movement during stroke rehabilitation: investigating associations between sleep measured by wearable actigraphy technology, fatigue, and key biomarkers

Decoding hand and wrist movement intention from chronic stroke survivors with hemiparesis using a user-friendly, wearable EMG-based neural interface

Effects of multidisciplinary inpatient rehabilitation on everyday life physical activity and gait in patients with multiple sclerosis