Differential Effects of Sustained Manual Pressure Stimulation According to Site of Action

. 2019 ; 13 () : 722. [epub] 20190717

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid31379481

Sustained pressure stimulation of the body surface has been used in several physiotherapeutic techniques, such as reflex locomotion therapy. Clinical observations of global motor responses and subsequent motor behavioral changes after stimulation in certain sites suggest modulation of central sensorimotor control, however, the neuroanatomical correlates remain undescribed. We hypothesized that different body sites would specifically influence the sensorimotor system during the stimulation. We tested the hypothesis using functional magnetic resonance imaging (fMRI) in thirty healthy volunteers (mean age 24.2) scanned twice during intermittent manual pressure stimulation, once at the right lateral heel according to reflex locomotion therapy, and once at the right lateral ankle (control site). A flexible modeling approach with finite impulse response basis functions was employed since non-canonical hemodynamic response was expected. Subsequently, a clustering algorithm was used to separate areas with differential timecourses. Stimulation at both sites induced responses throughout the sensorimotor system that could be mostly separated into two anti-correlated subsystems with transient positive or negative signal change and rapid adaptation, although in heel stimulation, insulo-opercular cortices and pons showed sustained activation. In direct voxel-wise comparison, heel stimulation was associated with significantly higher activation levels in the contralateral primary motor cortex and decreased activation in the posterior parietal cortex. Thus, we demonstrate that the manual pressure stimulation affects multiple brain structures involved in motor control and the choice of stimulation site impacts the shape and amplitude of the blood oxygenation level-dependent response. We further discuss the relationship between the affected structures and behavioral changes after reflex locomotion therapy.

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Apkarian A. V., Bushnell M. C., Treede R.-D., Zubieta J.-K. (2005). Human brain mechanisms of pain perception and regulation in health and disease. Eur. J. Pain 9 463–484. 10.1016/j.ejpain.2004.11.001 PubMed DOI

Beissner F., Meissner K., Bär K.-J., Napadow V. (2013). The autonomic brain: an activation likelihood estimation meta-analysis for central processing of autonomic function. J. Neurosci. 33 10503–10511. 10.1523/JNEUROSCI.1103-13.2013 PubMed DOI PMC

Boorman L., Kennerley A. J., Johnston D., Jones M., Zheng Y., Redgrave P., et al. (2010). Negative blood oxygen level dependence in the rat: a model for investigating the role of suppression in neurovascular coupling. J. Neurosci. 30 4285–4294. 10.1523/JNEUROSCI.6063-09.2010 PubMed DOI PMC

Caliński T., Harabasz J. (1974). A dendrite method for cluster analysis. Commun. Stat. Theory Methods 3 1–27. 10.1080/03610927408827101 DOI

Chipchase L. S., Schabrun S. M., Hodges P. W. (2011). Peripheral electrical stimulation to induce cortical plasticity: a systematic review of stimulus parameters. Clin. Neurophysiol. 122 456–463. 10.1016/j.clinph.2010.07.025 PubMed DOI

Christova M., Rafolt D., Golaszewski S., Gallasch E. (2011). Outlasting corticomotor excitability changes induced by 25 Hz whole-hand mechanical stimulation. Eur. J. Appl. Physiol. 111 3051–3059. 10.1007/s00421-011-1933-0 PubMed DOI

Chung Y. G., Han S. W., Kim H.-S., Chung S.-C., Park J.-Y., Wallraven C., et al. (2014). Intra- and inter-hemispheric effective connectivity in the human somatosensory cortex during pressure stimulation. BMC Neurosci. 15:43. 10.1186/1471-2202-15-43 PubMed DOI PMC

Chung Y. G., Han S. W., Kim H.-S., Chung S.-C., Park J.-Y., Wallraven C., et al. (2015). Adaptation of cortical activity to sustained pressure stimulation on the fingertip. BMC Neurosci. 16:71. 10.1186/s12868-015-0207-x PubMed DOI PMC

Dale A. M. (1999). Optimal experimental design for event-related fMRI. Hum. Brain Mapp. 8 109–114. PubMed PMC

Desikan R. S., Ségonne F., Fischl B., Quinn B. T., Dickerson B. C., Blacker D., et al. (2006). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31 968–980. 10.1016/j.neuroimage.2006.01.021 PubMed DOI

Devor A., Hillman E. M. C., Tian P., Waeber C., Teng I. C., Ruvinskaya L., et al. (2008). Stimulus-induced changes in blood flow and 2-deoxyglucose uptake dissociate in ipsilateral somatosensory cortex. J. Neurosci. 28 14347–14357. 10.1523/JNEUROSCI.4307-08.2008 PubMed DOI PMC

Diedrichsen J., Maderwald S., Küper M., Thürling M., Rabe K., Gizewski E. R., et al. (2011). Imaging the deep cerebellar nuclei: a probabilistic atlas and normalization procedure. Neuroimage 54 1786–1794. 10.1016/j.neuroimage.2010.10.035 PubMed DOI

Dyson K. S., Miron J.-P., Drew T. (2014). Differential modulation of descending signals from the reticulospinal system during reaching and locomotion. J. Neurophysiol. 112 2505–2528. 10.1152/jn.00188.2014 PubMed DOI

Eickhoff S. B., Paus T., Caspers S., Grosbras M.-H., Evans A. C., Zilles K., et al. (2007). Assignment of functional activations to probabilistic cytoarchitectonic areas revisited. Neuroimage 36 511–521. 10.1016/j.neuroimage.2007.03.060 PubMed DOI

Foerster O. (1933). The dermatomes in man. Brain 56 1–39. 10.1093/brain/56.1.1 DOI

Gallasch E., Christova M., Kunz A., Rafolt D., Golaszewski S. (2015). Modulation of sensorimotor cortex by repetitive peripheral magnetic stimulation. Front. Hum. Neurosci. 9:407. 10.3389/fnhum.2015.00407 PubMed DOI PMC

Glover G. H. (1999). Deconvolution of impulse response in event-related BOLD fMRI. Neuroimage 9 416–429. 10.1006/nimg.1998.0419 PubMed DOI

Golaszewski S. M., Bergmann J., Christova M., Kunz A. B., Kronbichler M., Rafolt D., et al. (2012). Modulation of motor cortex excitability by different levels of whole-hand afferent electrical stimulation. Clin. Neurophysiol. 123 193–199. 10.1016/j.clinph.2011.06.010 PubMed DOI

Grabner G., Janke A. L., Budge M. M., Smith D., Pruessner J., Collins D. L. (2006). Symmetric atlasing and model based segmentation: an application to the hippocampus in older adults. Med. Image Comput. Comput. Assist. Interv. 9 58–66. 10.1007/11866763_8 PubMed DOI

Grillner S., Wallén P. (1985). Central pattern generators for locomotion, with special reference to vertebrates. Annu. Rev. Neurosci. 8 233–261. 10.1146/annurev.ne.08.030185.001313 PubMed DOI

Hao Y., Manor B., Liu J., Zhang K., Chai Y., Lipsitz L., et al. (2013). A novel MRI-compatible tactile stimulator for cortical mapping of foot sole pressure stimuli with fMRI. Magn. Reson. Med. 69 1194–1199. 10.1002/mrm.24330 PubMed DOI PMC

Hirschauer T. J., Buford J. A. (2015). Bilateral force transients in the upper limbs evoked by single-pulse microstimulation in the pontomedullary reticular formation. J. Neurophysiol. 113 2592–2604. 10.1152/jn.00852.2014 PubMed DOI PMC

Hlushchuk Y., Hari R. (2006). Transient suppression of ipsilateral primary somatosensory cortex during tactile finger stimulation. J. Neurosci. 26 5819–5824. 10.1523/JNEUROSCI.5536-05.2006 PubMed DOI PMC

Hok P., Opavský J., Kutín M., Tüdös Z., Kaňovský P., Hluštík P. (2017). Modulation of the sensorimotor system by sustained manual pressure stimulation. Neuroscience 348 11–22. 10.1016/j.neuroscience.2017.02.005 PubMed DOI

Hu D., Huang L. (2015). Negative hemodynamic response in the cortex: evidence opposing neuronal deactivation revealed via optical imaging and electrophysiological recording. J. Neurophysiol. 114 2152–2161. 10.1152/jn.00246.2015 PubMed DOI PMC

Hu L., Zhang L., Chen R., Yu H., Li H., Mouraux A. (2015). The primary somatosensory cortex and the insula contribute differently to the processing of transient and sustained nociceptive and non-nociceptive somatosensory inputs. Hum. Brain Mapp. 36 4346–4360. 10.1002/hbm.22922 PubMed DOI PMC

Huffman K. J., Krubitzer L. (2001). Thalamo-cortical connections of areas 3a and M1 in marmoset monkeys. J. Comp. Neurol. 435 291–310. 10.1002/cne.1031 PubMed DOI

Ide M., Hidaka S., Ikeda H., Wada M. (2016). Neural mechanisms underlying touch-induced visual perceptual suppression: an fMRI study. Sci. Rep. 6:37301. 10.1038/srep37301 PubMed DOI PMC

Igelström K. M., Graziano M. S. A. (2017). The inferior parietal lobule and temporoparietal junction: a network perspective. Neuropsychologia 105 70–83. 10.1016/j.neuropsychologia.2017.01.001 PubMed DOI

Jahn K., Deutschländer A., Stephan T., Kalla R., Wiesmann M., Strupp M., et al. (2008). Imaging human supraspinal locomotor centers in brainstem and cerebellum. Neuroimage 39 786–792. 10.1016/j.neuroimage.2007.09.047 PubMed DOI

Jenkinson M. (2003). Fast, automated, N-dimensional phase-unwrapping algorithm. Magn. Reson. Med. 49 193–197. 10.1002/mrm.10354 PubMed DOI

Jenkinson M., Bannister P., Brady M., Smith S. (2002). Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17 825–841. 10.1006/nimg.2002.1132 PubMed DOI

Jenkinson M., Beckmann C. F., Behrens T. E. J., Woolrich M. W., Smith S. M. (2012). FSL. Neuroimage 62 782–790. 10.1016/j.neuroimage.2011.09.015 PubMed DOI

Johansson R. S., Flanagan J. R. (2009). Coding and use of tactile signals from the fingertips in object manipulation tasks. Nat. Rev. Neurosci. 10 345–359. 10.1038/nrn2621 PubMed DOI

Jung M. W., Landenberger M., Jung T., Lindenthal T., Philippi H. (2017). Vojta therapy and neurodevelopmental treatment in children with infantile postural asymmetry: a randomised controlled trial. J. Phys. Ther. Sci. 29 301–306. 10.1589/jpts.29.301 PubMed DOI PMC

Kaelin-Lang A., Luft A. R., Sawaki L., Burstein A. H., Sohn Y. H., Cohen L. G. (2002). Modulation of human corticomotor excitability by somatosensory input. J. Physiol. 540 623–633. 10.1113/jphysiol.2001.012801 PubMed DOI PMC

Kawashima R., O’Sullivan B. T., Roland P. E. (1995). Positron-emission tomography studies of cross-modality inhibition in selective attentional tasks: closing the “mind’s eye”. Proc. Natl. Acad. Sci. U.S.A. 92 5969–5972.10.1073/pnas.92.13.5969 PubMed DOI PMC

Kayalioglu G. (2009). “Chapter 10 - Projections from the Spinal Cord to the Brain,” in The Spinal Cord, eds Watson C., Paxinos G., Kayalioglu G. (San Diego, CA: Academic Press; ), 148–167. 10.1016/B978-0-12-374247-6.50014-6 DOI

Kurth F., Zilles K., Fox P. T., Laird A. R., Eickhoff S. B. (2010). A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis. Brain Struct. Funct. 214 519–534. 10.1007/s00429-010-0255-z PubMed DOI PMC

la Fougère C., Zwergal A., Rominger A., Förster S., Fesl G., Dieterich M., et al. (2010). Real versus imagined locomotion: a [18F]-FDG PET-fMRI comparison. Neuroimage 50 1589–1598. 10.1016/j.neuroimage.2009.12.060 PubMed DOI

Laufens G., Poltz W., Jugelt E., Prinz E., Reimann G., Van Slobbe T. (1995). Motor improvements in multiple-sclerosis patients by Vojta physiotherapy and the influence of treatment positions. Phys. Med. Rehab. Kuror 5 115–119.

Laufens G., Seitz S., Staenicke G. (1991). Vergleichend biologische Grundlagen zur angeborenen Lokomotion insbesondere zum “reflektorischen Kriechen” nach Vojta. Krankengymnastik 43 448–456.

Leung Y. Y., Bensmaïa S. J., Hsiao S. S., Johnson K. O. (2005). Time-course of vibratory adaptation and recovery in cutaneous mechanoreceptive afferents. J. Neurophysiol. 94 3037–3045. 10.1152/jn.00001.2005 PubMed DOI PMC

Lewis L. D., Setsompop K., Rosen B. R., Polimeni J. R. (2018). Stimulus-dependent hemodynamic response timing across the human subcortical-cortical visual pathway identified through high spatiotemporal resolution 7T fMRI. Neuroimage 181 279–291. 10.1016/j.neuroimage.2018.06.056 PubMed DOI PMC

Liu J., Duffy B. A., Bernal-Casas D., Fang Z., Lee J. H. (2017). Comparison of fMRI analysis methods for heterogeneous BOLD responses in block design studies. Neuroimage 147 390–408. 10.1016/j.neuroimage.2016.12.045 PubMed DOI PMC

Long X., Goltz D., Margulies D. S., Nierhaus T., Villringer A. (2014). Functional connectivity-based parcellation of the human sensorimotor cortex. Eur. J. Neurosci. 39 1332–1342. 10.1111/ejn.12473 PubMed DOI

Marconi B., Filippi G. M., Koch G., Pecchioli C., Salerno S., Don R., et al. (2008). Long-term effects on motor cortical excitability induced by repeated muscle vibration during contraction in healthy subjects. J. Neurol. Sci. 275 51–59. 10.1016/j.jns.2008.07.025 PubMed DOI

Marxen M., Cassidy R. J., Dawson T. L., Ross B., Graham S. J. (2012). Transient and sustained components of the sensorimotor BOLD response in fMRI. Magn. Reson. Imaging 30 837–847. 10.1016/j.mri.2012.02.007 PubMed DOI PMC

Merabet L. B., Swisher J. D., McMains S. A., Halko M. A., Amedi A., Pascual-Leone A., et al. (2007). Combined activation and deactivation of visual cortex during tactile sensory processing. J. Neurophysiol. 97 1633–1641. 10.1152/jn.00806.2006 PubMed DOI

Miura N., Akitsuki Y., Sekiguchi A., Kawashima R. (2013). Activity in the primary somatosensory cortex induced by reflexological stimulation is unaffected by pseudo-information: a functional magnetic resonance imaging study. BMC Compl. Altern. Med. 13:114. 10.1186/1472-6882-13-114 PubMed DOI PMC

Müller H. (1974). Comment on V.Vojta’s: early diagnosis and therapy of cerebral disturbances of motility in infancy (author’s transl). Z Orthop Ihre Grenzgeb 112 361–364. PubMed

Mullinger K. J., Mayhew S. D., Bagshaw A. P., Bowtell R., Francis S. T. (2014). Evidence that the negative BOLD response is neuronal in origin: a simultaneous EEG-BOLD-CBF study in humans. Neuroimage 94 263–274. 10.1016/j.neuroimage.2014.02.029 PubMed DOI

Nieuwenhuys R., Voogd J., van Huijzen C. (2008). The Human Central Nervous System. New York, NY: Springer.

Oldfield R. C. (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9 97–113. 10.1016/0028-3932(71)90067-4 PubMed DOI

Opavský J., Šlachtová M., Kutín M., Hok P., Uhlír̃ P., Opavská H., et al. (2018). The effects of sustained manual pressure stimulation according to Vojta Therapy on heart rate variability. Biomed. Pap. Med. Fac. Univ. Palacky Olomouc Czech Repub 162 206–211. 10.5507/bp.2018.028 PubMed DOI

Powell J., Pandyan A. D., Granat M., Cameron M., Stott D. J. (1999). Electrical stimulation of wrist extensors in poststroke hemiplegia. Stroke 30 1384–1389. 10.1161/01.str.30.7.1384 PubMed DOI

Pruim R. H. R., Mennes M., Buitelaar J. K., Beckmann C. F. (2015a). Evaluation of ICA-AROMA and alternative strategies for motion artifact removal in resting state fMRI. Neuroimage 112 278–287. 10.1016/j.neuroimage.2015.02.063 PubMed DOI

Pruim R. H. R., Mennes M., van Rooij D., Llera A., Buitelaar J. K., Beckmann C. F. (2015b). ICA-AROMA: a robust ICA-based strategy for removing motion artifacts from fMRI data. Neuroimage 112 267–277. 10.1016/j.neuroimage.2015.02.064 PubMed DOI

Qiu K., Jing M., Sun R., Yang J., Liu X., He Z., et al. (2016). The status of the quality control in acupuncture-neuroimaging studies. Evid. Based Compl. Alternat. Med. 2016:3685785. 10.1155/2016/3685785 PubMed DOI PMC

Rencher A. C., Christensen W. F. (2012). “Cluster Analysis,” in Methods of Multivariate Analysis, eds Rencher A. C., Christensen W. F. (Hoboken, NJ: Wiley-Blackwell; ), 501–554. 10.1002/9781118391686.ch15 DOI

Rosenkranz K., Rothwell J. C. (2003). Differential effect of muscle vibration on intracortical inhibitory circuits in humans. J. Physiol. 551 649–660. 10.1113/jphysiol.2003.043752 PubMed DOI PMC

Sanz-Esteban I., Calvo-Lobo C., Ríos-Lago M., Álvarez-Linera J., Muñoz-García D., Rodríguez-Sanz D. (2018). Mapping the human brain during a specific Vojta’s tactile input: the ipsilateral putamen’s role. Medicine 97:e0253. 10.1097/MD.0000000000010253 PubMed DOI PMC

Smith C. A., Levett K. M., Collins C. T., Dahlen H. G., Ee C. C., Suganuma M. (2018). Massage, reflexology and other manual methods for pain management in labour. Cochrane Database Syst. Rev. 3:CD009290. 10.1002/14651858.CD009290.pub3 PubMed DOI PMC

Smith S. M. (2002). Fast robust automated brain extraction. Hum. Brain Mapp. 17 143–155. 10.1002/hbm.10062 PubMed DOI PMC

Takakusaki K. (2013). Neurophysiology of gait: from the spinal cord to the frontal lobe. Mov. Disord. 28 1483–1491. 10.1002/mds.25669 PubMed DOI

Tal Z., Geva R., Amedi A. (2017). Positive and negative somatotopic BOLD responses in contralateral versus ipsilateral penfield homunculus. Cereb. Cortex 27 962–980. 10.1093/cercor/bhx024 PubMed DOI PMC

Uddin L. Q. (2015). Salience processing and insular cortical function and dysfunction. Nat. Rev. Neurosci. 16 55–61. 10.1038/nrn3857 PubMed DOI

Usichenko T. I., Wesolowski T., Lotze M. (2015). Verum and sham acupuncture exert distinct cerebral activation in pain processing areas: a crossover fMRI investigation in healthy volunteers. Brain Imaging Behav. 9 236–244. 10.1007/s11682-014-9301-4 PubMed DOI

Vazquez A. L., Fukuda M., Kim S.-G. (2018). Inhibitory neuron activity contributions to hemodynamic responses and metabolic load examined using an inhibitory optogenetic mouse model. Cereb. Cortex 28 4105–4119. 10.1093/cercor/bhy225 PubMed DOI PMC

Vojta V. (1973). Early diagnosis and therapy of cerebral movement disorders in childhood. C. Reflexogenous locomotion - reflex creeping and reflex turning. C1. The kinesiologic content and connection with the tonic neck reflexes. Z Orthop Ihre Grenzgeb 111 268–291. PubMed

Vojta V., Peters A. (2007). Das Vojta-Prinzip: Muskelspiele in Reflexfortbewegung und motorischer Ontogenese. 3., vollst. überarb. Aufl. Berlin: Springer.

Wall M. E., Rechtsteiner A., Rocha L. M. (2003). “Singular value decomposition and principal component analysis,” in A Practical Approach to Microarray Data Analysis, eds Berrar D. P., Dubitzky W., Granzow M. (Berlin: Springer; ), 91–109. 10.1007/0-306-47815-3_5 DOI

Wong J. J., Shearer H. M., Mior S., Jacobs C., Côté P., Randhawa K., et al. (2016). Are manual therapies, passive physical modalities, or acupuncture effective for the management of patients with whiplash-associated disorders or neck pain and associated disorders? An update of the bone and joint decade task force on neck pain and its associated disorders by the OPTIMa collaboration. Spine J. 16 1598–1630. 10.1016/j.spinee.2015.08.024 PubMed DOI

Woolrich M. W., Behrens T. E. J., Beckmann C. F., Jenkinson M., Smith S. M. (2004). Multilevel linear modelling for FMRI group analysis using Bayesian inference. Neuroimage 21 1732–1747. 10.1016/j.neuroimage.2003.12.023 PubMed DOI

Woolrich M. W., Ripley B. D., Brady M., Smith S. M. (2001). Temporal autocorrelation in univariate linear modeling of FMRI data. Neuroimage 14 1370–1386. 10.1006/nimg.2001.0931 PubMed DOI

Worsley K. J. (2001). “Statistical analysis of activation images,” in Functional MRI: an Introduction to Methods, eds Jezzard P., Matthews P. M., Smith S. M. (New York, NY: Oxford University Press; ).

Wu M.-T., Sheen J.-M., Chuang K.-H., Yang P., Chin S.-L., Tsai C.-Y., et al. (2002). Neuronal specificity of acupuncture response: a fMRI study with electroacupuncture. Neuroimage 16 1028–1037. 10.1006/nimg.2002.1145 PubMed DOI

Yin H., Liu Y., Li M., Hu D. (2011). Hemodynamic observation and spike recording explain the neuronal deactivation origin of negative response in rat. Brain Res. Bull. 84 157–162. 10.1016/j.brainresbull.2010.12.004 PubMed DOI

Ziemann U., Lönnecker S., Steinhoff B. J., Paulus W. (1996). Effects of antiepileptic drugs on motor cortex excitability in humans: a transcranial magnetic stimulation study. Ann. Neurol. 40 367–378. 10.1002/ana.410400306 PubMed DOI

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