J Appl Biomed 17:157-166, 2019 | DOI: 10.32725/jab.2019.014
Reshaping cortical activity with subthalamic stimulation in Parkinson's disease during finger tapping and gait mapped by near infrared spectroscopy
- 1 Czech Technical University in Prague, Faculty of Biomedical Engineering, Department of Biomedical Informatics, Kladno, Czech Republic
- 2 Charles University, First Faculty of Medicine and General University Hospital, Department of Neurology, Prague, Czech Republic
- 3 University Medical Center Eppendorf, Department of Systems Neuroscience, Hamburg, Germany
- 4 Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
Exploration of motor cortex activity is essential to understanding the pathophysiology in Parkinson's Disease (PD), but only simple motor tasks can be investigated using a fMRI or PET. We aim to investigate the cortical activity of PD patients during a complex motor task (gait) to verify the impact of deep brain stimulation in the subthalamic nucleus (DBS-STN) by using Near-Infrared-Spectroscopy (NIRS). NIRS is a neuroimaging method of brain cortical activity using low-energy optical radiation to detect local changes in (de)oxyhemoglobin concentration. We used a multichannel portable NIRS during finger tapping (FT) and gait. To determine the signal activity, our methodology consisted of a pre-processing phase for the raw signal, followed by statistical analysis based on a general linear model. Processed recordings from 9 patients were statistically compared between the on and off states of DBS-STN. DBS-STN led to an increased activity in the contralateral motor cortex areas during FT. During gait, we observed a concentration of activity towards the cortex central area in the "stimulation-on" state. Our study shows how NIRS can be used to detect functional changes in the cortex of patients with PD with DBS-STN and indicates its future use for applications unsuited for PET and a fMRI.
Keywords: Deep brain stimulation; Gait; Near infrared spectroscopy; Neuroinformatics; Parkinson's disease; Subthalamic nucleus
Grants and funding:
This work was supported by the Czech Science foundation GACR 16-13323S; the Czech Ministry of Health (AZV Grant no. 16-28119a and no. 17-32318a).
Conflicts of interest:
The authors declare no conflict of interests in this article
Received: May 30, 2018; Accepted: August 19, 2019; Prepublished online: September 11, 2019; Published: September 18, 2019 Show citation
ACS | AIP | APA | ASA | Harvard | Chicago | Chicago Notes | IEEE | ISO690 | MLA | NLM | Turabian | Vancouver |
References
- Bae SJ, Jang SH, Seo JP, Chang PH (2017). The optimal speed for cortical activation of passive wrist movements performed by a rehabilitation robot: a functional NIRS study. Front Hum Neurosci 11: 194. DOI: 10.3389/fnhum.2017.00194.
Go to original source...
Go to PubMed...
- Bick SK, Folley BS, Mayer JS, Park S, Charles PD, Camalier CR, et al. (2016). Subthalamic nucleus deep brain stimulation alters prefrontal correlates of emotion induction. Neuromodulation 20(3): 233-237. DOI: 10.1111/ner.12537.
Go to original source...
Go to PubMed...
- Blinkenberg M, Bonde C, Holm S, Svarer C, Andersen J, Paulson OB, Law I (1996). Rate dependence of regional cerebral activation during performance of a repetitive motor task: a PET study. J Cereb Blood Flow Metab 16(5): 794-803. DOI: 10.1097/00004647-199609000-00004.
Go to original source...
Go to PubMed...
- Boushel R, Piantadosi CA (2000). Near-infrared spectroscopy for monitoring muscle oxygenation. Acta Physiol Scand 168(4): 615-622. DOI: 10.1046/j.1365-201x.2000.00713.x.
Go to original source...
Go to PubMed...
- Ceballos-Baumann AO, Boecker H, Bartenstein P, Falkenhayn I, Riescher H, Conrad B, et al. (1999). A positron emission tomographic study of subthalamic nucleus stimulation in Parkinson disease: enhanced movement-related activity of motor-association cortex and decreased motor cortex resting activity. Arch Neurol 56(8): 997-1003. DOI: 10.1001/archneur.56.8.997.
Go to original source...
Go to PubMed...
- Chang PH, Lee S-H, Gu K-M, Lee S-H, Jin S-H, Yeo SS, et al. (2014). The cortical activation pattern by a rehabilitation robotic hand: a functional NIRS study. Front Hum Neurosci 8: 49. DOI: 10.3389/fnhum.2014.00049.
Go to original source...
Go to PubMed...
- Cope M, Delpy DT (1988). System for long-term measurement of cerebral blood and tissue oxygenation on newborn infants by near infra-red transillumination. Med Biol Eng Comput 26(3): 289-294. DOI: 10.1007/BF02447083.
Go to original source...
Go to PubMed...
- Cui X, Bray S, Bryant DM, Glover GH, Reiss AL (2011). A quantitative comparison of NIRS and fMRI across multiple cognitive tasks. Neuroimage 54(4): 2808-2821. DOI: 10.1016/j.neuroimage.2010.10.069.
Go to original source...
Go to PubMed...
- Derosière G, Alexandre F, Bourdillon N, Mandrick K, Ward TE, Perrey S (2014). Similar scaling of contralateral and ipsilateral cortical responses during graded unimanual force generation. Neuroimage 85: 471-477. DOI: 10.1016/j.neuroimage.2013.02.006.
Go to original source...
Go to PubMed...
- Fazli S, Mehnert J, Steinbrink J, Curio G, Villringer A, Müller K-R, Blankertz B (2012). Enhanced performance by a hybrid NIRS-EEG brain computer interface. NeuroImage 59(1): 519-529. DOI: 10.1016/j.neuroimage.2011.07.084.
Go to original source...
Go to PubMed...
- Giacometti P, Diamond SG (2013). Compliant head probe for positioning electroencephalography electrodes and near-infrared spectroscopy optodes. J Biomed Opt 18(2): 27005. DOI: 10.1117/1.JBO.18.2.027005.
Go to original source...
Go to PubMed...
- Gilat M, Shine JM, Walton CC, O'Callaghan C, Hall JM, Lewis SJ (2015). Brain activation underlying turning in Parkinson's disease patients with and without freezing of gait: a virtual reality fMRI study. NPJ Parkinsons Dis 1: 15020. DOI: 10.1038/npjparkd.2015.20.
Go to original source...
Go to PubMed...
- Huang C, Chu H, Zhang Y, Wang X (2018). Deep brain stimulation to alleviate freezing of gait and cognitive dysfunction in Parkinson's disease: update on current research and future perspectives. Front Neurosci 12: 29. DOI: 10.3389/fnins.2018.00029.
Go to original source...
Go to PubMed...
- Kawashima R, Inoue K, Sugiura M, Okada K, Ogawa A, Fukuda H (1999). A positron emission tomography study of self-paced finger movements at different frequencies. Neuroscience 92(1): 107-112. DOI: 10.1016/s0306-4522(98)00744-1.
Go to original source...
Go to PubMed...
- Kim HY, Seo K, Jeon HJ, Lee U, Lee H (2017). Application of functional near-infrared spectroscopy to the study of brain function in humans and animal models. Mol Cells 40(8): 523-532. DOI: 10.14348/molcells.2017.0153.
Go to original source...
Go to PubMed...
- Koenraadt KL, Roelofsen EG, Duysens J, Keijsers NL (2014). Cortical control of normal gait and precision stepping: an fNIRS study. Neuroimage 85: 415-422. DOI: 10.1016/j.neuroimage.2013.04.070.
Go to original source...
Go to PubMed...
- Krupicka R, Viteckova S, Cejka V, Klempir O, Szabo Z, Ruzicka E (2017). BradykAn: A motion capture system for objectification of hand motor tests in Parkinson Disease. 2017 E-Health and Bioengineering Conference (EHB): 446-449. DOI: 10.1109/EHB.2017.7995457.
Go to original source...
- Limousin P, Greene J, Pollak P, Rothwell J, Benabid AL, Frackowiak R (1997). Changes in cerebral activity pattern due to subthalamic nucleus or internal pallidum stimulation in Parkinson's disease. Ann Neurol 42(3): 283-291. DOI: 10.1002/ana.410420303.
Go to original source...
Go to PubMed...
- Maidan I, Nieuwhof F, Bernad-Elazari H, Reelick MF, Bloem BR, Giladi N, et al. (2016). The role of the frontal lobe in complex walking among patients with Parkinson's Disease and healthy older adults: an fNIRS study. Neurorehabil Neural Repair 30(10): 963-971. DOI: 10.1177/1545968316650426.
Go to original source...
Go to PubMed...
- Martinu K, Nagano-Saito A, Fogel S, Monchi O (2014). Asymmetrical effect of levodopa on the neural activity of motor regions in PD. PLoS One 9(11): e111600. DOI: 10.1371/journal.pone.0111600.
Go to original source...
Go to PubMed...
- Miyai I, Tanabe HC, Sase I, Eda H, Oda I, Konishi I, et al. (2001). Cortical mapping of gait in humans: a near-infrared spectroscopic topography study. Neuroimage 14(5): 1186-1192. DOI: 10.1006/nimg.2001.0905.
Go to original source...
Go to PubMed...
- Morishita T, Higuchi M, Saita K, Tsuboi Y, Abe H, Inoue T (2016). Changes in motor-related cortical activity following deep brain stimulation for Parkinson's Disease detected by functional near infrared spectroscopy: a pilot study. Front Hum Neurosci 10: 629. DOI: 10.3389/fnhum.2016.00629.
Go to original source...
Go to PubMed...
- Payoux P, Brefel-Courbon C, Julian A, Durif F, Azulay JP, Blin O, et al. (2007). Motor activity in parkinsonism and levodopa effect: A PET study. J Nucl Med 48(Suppl. 2): 8P.
- Perrey S (2014). Possibilities for examining the neural control of gait in humans with fNIRS. Front Physiol 5: 204. DOI: 10.3389/fphys.2014.00204.
Go to original source...
Go to PubMed...
- Peterson DS, Pickett KA, Duncan RP, Perlmutter JS, Earhart GM (2014). Brain activity during complex imagined gait tasks in Parkinson disease. Clin Neurophysiol 125(5): 995-1005. DOI: 10.1016/j.clinph.2013.10.008.
Go to original source...
Go to PubMed...
- Piper SK, Krueger A, Koch SP, Mehnert J, Habermehl C, Steinbrink J, et al. (2014). A wearable multi-channel fNIRS system for brain imaging in freely moving subjects. Neuroimage 85: 64-71. DOI: 10.1016/j.neuroimage.2013.06.062.
Go to original source...
Go to PubMed...
- Rao SM, Bandettini PA, Binder JR, Bobholz JA, Hammeke TA, Stein EA, Hyde JS (1996). Relationship between finger movement rate and functional magnetic resonance signal change in human primary motor cortex. J Cereb Blood Flow Metab 16(6): 1250-1254. DOI: 10.1097/00004647-199611000-00020.
Go to original source...
Go to PubMed...
- Sabatini U, Boulanouar K, Fabre N, Martin F, Carel C, Colonnese C, et al. (2000). Cortical motor reorganization in akinetic patients with Parkinson's disease: a functional MRI study. Brain 123(Pt 2): 394-403. DOI: 10.1093/brain/123.2.394.
Go to original source...
Go to PubMed...
- Sadato N, Ibañez V, Campbell G, Deiber MP, Le Bihan D, Hallett M (1996). Frequency dependent changes of regional cerebral blood flow during finger movements. J Cereb Blood Flow Metab 16(1): 23-33. DOI: 10.1097/00004647-199601000-00003.
Go to original source...
Go to PubMed...
- Sakatani K, Katayama Y, Yamamoto T, Suzuki S (1999). Changes in cerebral blood oxygenation of the frontal lobe induced by direct electrical stimulation of thalamus and globus pallidus: a near infrared spectroscopy study. J Neurol Neurosurg Psychiatry 67(6): 769-773. DOI: 10.1136/jnnp.67.6.769.
Go to original source...
Go to PubMed...
- Scholkmann F, Kleiser S, Metz AJ, Zimmermann R, Mata Pavia J, Wolf U, Wolf M (2014). A review on continuous wave functional near-infrared spectroscopy and imaging instrumentation and methodology. Neuroimage 85: 6-27. DOI: 10.1016/j.neuroimage.2013.05.004.
Go to original source...
Go to PubMed...
- Strangman G, Culver JP, Thompson JH, Boas DA (2002). A quantitative comparison of simultaneous BOLD fMRI and NIRS recordings during functional brain activation. Neuroimage 17(2): 719-731. DOI: 10.1006/nimg.2002.1227.
Go to original source...
Go to PubMed...
- Tak S, Ye JC (2014). Statistical analysis of fNIRS data: A comprehensive review. Neuroimage 85: 72-91. DOI: 10.1016/j.neuroimage.2013.06.016.
Go to original source...
Go to PubMed...
- Tohka J, Foerde K, Aron AR, Tom SM, Toga AW, Poldrack RA (2008). Automatic independent component labeling for artifact removal in fMRI. Neuroimage 39(3): 1227-1245. DOI: 10.1016/j.neuroimage.2007.10.013.
Go to original source...
Go to PubMed...
- Torricelli A, Contini D, Pifferi A, Caffini M, Re R, Zucchelli L, Spinelli L (2014). Time domain functional NIRS imaging for human brain mapping. Neuroimage 85: 28-50. DOI: 10.1016/j.neuroimage.2013.05.106.
Go to original source...
Go to PubMed...
- Varriale P, Collomb-Clerc A, Van Hamme A, Perrochon A, Kemoun G, Sorrentino G, et al. (2018). Decreasing subthalamic deep brain stimulation frequency reverses cognitive interference during gait initiation in Parkinson's disease. Clin Neurophysiol 129(11): 2482-2491. DOI: 10.1016/j.clinph.2018.07.013.
Go to original source...
Go to PubMed...
- Wilson TW, Kurz MJ, Arpin DJ (2014). Functional specialization within the supplementary motor area: a fNIRS study of bimanual coordination. Neuroimage 85: 445-450. DOI: 10.1016/j.neuroimage.2013.04.112.
Go to original source...
Go to PubMed...
- Wu T, Long X, Wang L, Hallett M, Zang Y, Li K, Chan P (2011). Functional connectivity of cortical motor areas in the resting state in Parkinson's disease. Hum Brain Mapp 32(9): 1443-1457. DOI: 10.1002/hbm.21118.
Go to original source...
Go to PubMed...
- Xu J, Liu X, Zhang J, Li Z, Wang X, Fang F, Niu H (2015). FC-NIRS: A Functional Connectivity Analysis Tool for Near-Infrared Spectroscopy Data. Biomed Res Int 2015: 248724. DOI: 10.1155/2015/248724.
Go to original source...
Go to PubMed...
- Ye J, Tak S, Jang K, Jung J, Jang J (2009). NIRS-SPM: Statistical parametric mapping for near-infrared spectroscopy. Neuroimage 44(2): 428-447. DOI: 10.1016/j.neuroimage.2008.08.036.
Go to original source...
Go to PubMed...
- Zhang X, Noah JA, Hirsch J (2016). Separation of the global and local components in functional near-infrared spectroscopy signals using principal component spatial filtering. Neurophotonics 3(1): 015004. DOI: 10.1117/1.NPh.3.1.015004.
Go to original source...
Go to PubMed...
This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND 4.0), which permits non-comercial use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.