Sensorimotor integration in health and after stroke

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In the article a modern view on structural and functional somatosensory system organization is discussed. It is outlined that not only a feedback mechanism based on sensory impulsation is an essential condition for fine motor movements, but also sensorimotor integration is involved. The processes of sensorimotor integration are based on lookahead/forestalling phenomena of the movement results. Whereas an existing movement program of lookahead/forestalling modulates the sensory system, afferent activity of which influences movement accuracy. The neurological deficit associated with stroke is determined by the involved area and adjacent conduction tracts and also by neural networks damage outside the ischemic area. Acute ischemic stroke not only results in functional and effective connections of connectome damage, but also changes dynamical characteristics (amplitude and frequency) of cortical oscillations that results in desynchronization. Cerebral perfusion normalization, activation of tracts close to the ischemic area and distant from it, and cortical excitability change are the basis for recovery after stroke. Stroke recovery is considerably determined by central nervous system multimodal integration and is not limited only by sensorimotor integration. Understanding of structural and functional basis for sensorimotor integration and its dynamic properties opens up new possibilities of interventions that will result in better recovery after stroke.

About the authors

I. V Damulin

I.M.Sechenov First Moscow State Medical University of the Ministry of Health of the Russian Federation

Email: damulin@mmascience.ru
д-р мед. наук, проф. каф. нервных болезней и нейрохирургии 119991, Russian Federation, Moscow, ul. Trubetskaia, d. 8, str. 2

References

  1. Glencross D.J. Motor control and sensory-motor integration. In: Motor Control and Sensory Motor Integration: Issues and Directions. Advances in Psychology. D.J Gleneross, J.P Piek (eds.). Ch.1. New York: Elsevier Science, 1995; p. 3-7.
  2. Lappe M. Information transfer between sensory and motor networks. In: Handbook of Biological Physics. F Moss, S Gielen (eds.). Vol. 4. Ch. 23. Amsterdam etc.: Elsevier Science, 2001; p. 1001-41.
  3. Piek J.P, Barrett N.C. Perspectives on motor control and sensory-motor integration. In: Motor Control and Sensory Motor Integration: Issues and Directions. Advances in Psychology. DJ Gleneross, J.P Piek (eds.). Ch.16. New York: Elsevier Science, 1995; p. 411-9.
  4. Kaas J.H. Functional implications of plasticity and reorganizations in the somatosensory and motor systems of developing and adult primates. In: The Somatosensory System. Deciphering the Brain’s Own Body Image. Ed. by RJ Nelson. Ch.14. Boca Raton etc: CRC Press, 2002; p. 375-89.
  5. Kaas J.H, Jain N, Qi H-X. The organization of the somatosensory system in primates. In: The Somatosensory System. Deciphering the Brain’s Own Body Image. Ed. by RJ Nelson. Ch.1. Boca Raton etc.: CRC Press, 2002; p. 18-42.
  6. Nunez A, Malmierca E. Corticofugal Modulation of Sensory Information. Berlin, Heidelberg: Springer-Verlag, 2007.
  7. Burton H. Cerebral cortical regions devoted to the somatosensory system: results from brain imaging studies in humans. In: The Somatosensory System. Deciphering the Brain’s Own Body Image. Ed. by R.J Nelson. Ch.2. Boca Raton etc.: CRC Press, 2002; p. 43-88.
  8. Wasaka T, Kakigi R. Sensorimotor Integration. In: Magnetoencephalography. From Signals to Dynamic Cortical Networks. S Supek, CJ Aine (eds.). Berlin, Heidelberg: Springer-Verlag, 2014; p. 727-42. https://doi.org/10.1007/978-3-642-33045-2_34
  9. Koziol L.F, Budding D.E, Chidekel D. Sensory integration, sensory processing, and sensory modulation disorders: putative functional neuroanatomic underpinnings. The Cerebellum 2011; 10 (4): 770-92. https://doi.org/10.1007/s12311-011-0288-8
  10. Yu X, Koretsky A.P. Interhemispheric plasticity protects the deafferented somatosensory cortex from functional takeover after nerve injury. Brain Connectivity 2014; 4 (9): 709-17. https://doi.org/10.1089/brain.2014.0259
  11. Jones C, Nelson A. Promoting plasticity in the somatosensory cortex to alter motor physiology. Translat Neurosci 2014; 5 (4): 260-8. https://doi.org/10.2478/s13380-014-0230-x
  12. Ostry D.J, Gribble P.L. Sensory plasticity in human motor learning. Trends Neurosci 2016; 39 (2): 114-23. https://doi.org/10.1016/j.tins.2015.12.006
  13. Hosp J.A, Luft A.R. Cortical plasticity during motor learning and recovery after ischemic stroke. Neural Plasticity 2011; 2011: 1-9. https://doi.org/10.1155/2011/871296
  14. Vahdat S, Darainy M, Ostry D.J. Structure of plasticity in human sensory and motor networks due to perceptual learning. J Neurosci 2014; 34 (7): 2451-63. https://doi.org/10.1523/jneurosci.4291-13.2014
  15. Mendelsohn A.I, Simon C.M, Abbott L.F. et al. Activity regulates the incidence of heteronymous sensory-motor connections. Neuron 2015; 87 (1): 111-23. https://doi.org/10.1016/j.neuron.2015.05.045
  16. Zhou L-J, Wang W, Zhao Y et al. Blood oxygenation level-dependent functional magnetic resonance imaging in early days: correlation between passive activation and motor recovery after unilateral striatocapsular cerebral infarction. J Stroke Cerebrovasc Dis 2017; 26 (11): 2652-61. https://doi.org/10.1016/j.jstrokecerebrovasdis.2017.06.036
  17. Lamichhane B, Dhamala M. The salience network and its functional architecture in a perceptual decision: an effective connectivity study. Brain Connectivity 2015; 5 (6): 362-70. https://doi.org/10.1089/brain.2014.0282
  18. Kann S, Zhang S, Manza P et al. Hemispheric lateralization of resting-state functional connectivity of the anterior insula: association with age, gender, and a novelty-seeking trait. Brain Connectivity 2016; 6 (9): 724-34. https://doi.org/10.1089/brain.2016.0443
  19. Killgore W.D.S, Schwab Z.J, Kipman M et al. Insomnia-related complaints correlate with functional connectivity between sensory-motor regions. Neuro Report 2013; 24 (5): 233-40. https://doi.org/10.1097/wnr.0b013e32835edbdd
  20. Koganemaru S, Domen K, Fukuyama H, Mima T. Negative emotion can enhance human motor cortical plasticity. Eur J Neurosci 2012; 35 (10): 1637-45. https://doi.org/10.1111/j.1460-9568.2012.08098.x
  21. Nakagawa K, Inui K, Kakigi R. Somatosensory System. Basic Function. In: Clinical Applications of Magnetoencephalography. S Tobimatsu, R Kakigi (eds.). Pt. III, Ch.3. Tokyo etc.: Springer 2016; p. 55-71.
  22. Smith M-C, Stinear C. Plasticity and motor recovery after stroke: Implications for physiotherapy. N Z J Physiother 2016; 44 (3): 166-73. https://doi.org/10.15619/nzjp/44.3.06
  23. Ward N.S. Using oscillations to understand recovery after stroke. Brain 2015; 138 (10): 2811-3. https://doi.org/10.1093/brain/awv265
  24. Dijkhuizen R.M, Zaharchuk G, Otte W.M. Assessment and modulation of resting-state neural networks after stroke. Curr Opin Neurol 2014; 27 (6): 637-43. https://doi.org/10.1097/wco.0000000000000150
  25. Grefkes C, Fink G.R. Reorganization of cerebral networks after stroke: new insights from neuroimaging with connectivity approaches. Brain 2011; 134 (5): 1264-76. https://doi.org/10.1093/brain/awr033
  26. Pineiro R, Pendlebury S.T, Smith S et al. Relating MRI changes to motor deficit after ischemic stroke by segmentation of functional motor pathways. Stroke 2000; 31 (3): 672-9. https://doi.org/10.1161/01.str.31.3.672
  27. Thiel A, Vahdat S. Structural and resting-state brain connectivity of motor networks after stroke. Stroke 2014; 46 (1): 296-301. https://doi.org/10.1161/strokeaha.114.006307
  28. Van Meer M.P.A, van der Marel K, Otte W.M et al. Correspondence between altered functional and structural connectivity in the contralesional sensorimotor cortex after unilateral stroke in rats: a combined resting-state functional MRI and manganese-enhanced MRI study. J Cereb Blood Flow Metab 2010; 30 (10): 1707-11. https://doi.org/10.1038/jcbfm.2010.124
  29. Rehme A.K, Grefkes C. Cerebral network disorders after stroke: evidence from imaging-based connectivity analyses of active and resting brain states in humans. J Physiol 2013; 591 (1): 17-31. https://doi.org/10.1113/jphysiol.2012.243469
  30. Kroll H, Zaharchuk G, Christen T et al. Resting-state BOLD MRI for perfusion and ischemia. Top Magn Reson Imaging 2017; 26 (2): 91-6. https://doi.org/10.1097/rmr.0000000000000119
  31. Zhang Y, Li K-S, Ning Y-Z et al. Altered structural and functional connectivity between the bilateral primary motor cortex in unilateral subcortical stroke. A multimodal magnetic resonance imaging study. Medicine 2016; 95 (31): e4534. https://doi.org/10.1097/md.0000000000004534
  32. Staines W.R, Bolton D.A.E, McIlroy W.E. Sensorimotor control after stroke. In: The Behavioral Consequences of Stroke. T.A Schweizer, R.L Macdonald (eds.). Ch.3. New York: Springer Science, 2014; p. 37-49.
  33. Seitz R.J. Cerebral reorganization after sensorimotor stroke. In: Recovery after Stroke. MP Barnes, BH Dobkin, J Bogousslavsky (eds.). Ch.4. Cambridge etc.: Cambridge University Press, 2005; p. 8-123.
  34. Stinear C.M, Petoe M.A, Byblow W.D. Primary motor cortex excitability during recovery after stroke: implications for neuromodulation. Brain Stimulation 2015; 8 (6): 1183-90. https://doi.org/10.1016/j.brs.2015.06.015
  35. Zemke A.C, Heagerty P.J, Lee C, Cramer S.C. Motor cortex organization after stroke is related to side of stroke and level of recovery. Stroke 2003; 34 (5): e23-e26. https://doi.org/10.1161/01.str.0000065827.35634.5e
  36. Jiang L, Xu H, Yu C. Brain connectivity plasticity in the motor network after ischemic stroke. Neural Plasticity 2013; 2013: 1-11. https://doi.org/10.1155/2013/924192
  37. Onishi H, Kameyama S. Somatosensory System. Clinical Applications. In: Clinical Applications of Magnetoencephalography. S Tobimatsu, R Kakigi (eds.). Pt. III, Ch. 4. Tokyo etc.: Springer, 2016; p. 73-93.
  38. La C, Nair V.A, Mossahebi P et al. Implication of the slow-5 oscillations in the disruption of the default-mode network in healthy aging and stroke. Brain Connectivity 2016; 6 (6): 482-95. https://doi.org/10.1089/brain.2015.0375
  39. Toschi N, Duggento A, Passamonti L. Functional connectivity in amygdalar-sensory/(pre)motor networks at rest: new evidence from the Human Connectome Project. Eur J Neurosci 2017; 45 (9): 1224-29. https://doi.org/10.1111/ejn.13544
  40. Rossiter H.E, Boudrias M-H, Ward N.S. Do movement-related beta oscillations change after stroke? J Neurophysiol 2014; 112 (9): 2053-8. https://doi.org/10.1152/jn.00345.2014
  41. Matsuura A, Karita T, Nakada N et al. Correlation between changes of contralesional cortical activity and motor function recovery in patients with hemiparetic stroke. Physical Ther Res 2017; 20 (2): 28-35. https://doi.org/10.1298/ptr.e9911
  42. Veldema J, Bosl K, Nowak D.A. Motor recovery of the affected hand in subacute stroke correlates with changes of contralesional cortical hand motor representation. Neural Plastic 2017; 2017: 1-13. https://doi.org/10.1155/2017/6171903
  43. Ludemann-Podubecka J, Bosl K, Nowak D.A. Inhibition of the contralesional dorsal premotor cortex improves motor function of the affected hand following stroke. Eur J Neurol 2016; 23 (4): 823-30. https://doi.org/10.1111/ene.12949
  44. Madhavan S, Rogers L.M, Stinear J.W. A paradox: after stroke, the non-lesioned lower limb motor cortex may be maladaptive. Eur J Neurosci 2010; 32 (6): 1032-9. https://doi.org/10.1111/j.1460-9568.2010.07364.x
  45. Dubovik S, Pignat J-M, Ptak R et al. The behavioral significance of coherent resting-state oscillations after stroke. NeuroImage 2012; 61 (1): 249-57. https://doi.org/10.1016/j.neuroimage.2012.03.024
  46. Shi Z, Rogers B.P, Chen L.M et al. Realistic models of apparent dynamic changes in resting-state connectivity in somatosensory cortex. Human Brain Mapping 2016; 37 (11): 3897-910. https://doi.org/10.1002/hbm.23284
  47. Smitha K.A, Raja K.A, Arun K.M et al. Resting state fMRI: A review on methods in resting state connectivity analysis and resting state networks. Neuroradiol J 2017; 30 (4): 305-17. https://doi.org/10.1177/1971400917697342
  48. Amemiya S, Kunimatsu A, Saito N, Ohtomo K. Cerebral hemodynamic impairment: assessment with resting-state functional MR imaging. Radiology 2014; 270 (2): 548-55. https://doi.org/10.1148/radiology.13130982
  49. Thompson G.J. Neural and metabolic basis of dynamic resting state fMRI. NeuroImage 2017 (Sept.): 1-63. https://doi.org/10.1016/j.neuroimage.2017.09.010
  50. Winder A.T, Echagarruga C, Zhang Q, Drew P.J. Weak correlations between hemodynamic signals and ongoing neural activity during the resting state. Nature Neuroscience 2017; 20 (12): 1761-9. https://doi.org/10.1038/s41593-017-0007-y
  51. Baxter B.S, Edelman B, Zhang X. et al. Simultaneous high-definition transcranial direct current stimulation of the motor cortex and motor imagery. In: 36th Annual International Conference of the IEEE Engineering in Medicine and Biology Society. Chicago 2014; 454-6. https://doi.org/10.1109/embc.2014.6943626
  52. Baxter B.S, He B. Simultaneous high-definition transcranial direct current stimulation and motor imagery acutely modulates activity in the motor cortex. Brain Stimulation 2017; 10 (1): e9. https://doi.org/10.1016/j.brs.2016.11.046
  53. Chen J.L, Schlaug G. Increased resting state connectivity between ipsilesional motor cortex and contralesional premotor cortex after transcranial direct current stimulation with physical therapy. Scientific Reports 2016; 6 (1): 1-7. https://doi.org/10.1038/srep23271
  54. Fox M.D, Halko M.A, Eldaief M.C, Pascual-Leone A. Measuring and manipulating brain connectivity with resting state functional connectivity magnetic resonance imaging (fcMRI) and transcranial magnetic stimulation (TMS). NeuroImage 2012; 62 (4): 2232-43. https://doi.org/10.1016/j.neuroimage.2012.03.035
  55. Gbadeyan O, McMahon K, Steinhauser M, Meinzer M. Stimulation of dorsolateral prefrontal cortex enhances adaptive cognitive control: a high-definition transcranial direct current stimulation study. J Neurosci 2016; 36 (50): 12530-6. https://doi.org/10.1523/jneurosci.2450-16.2016
  56. Keeser D. The effect of prefrontal transcranial direct current stimulation on resting state functional connectivity. Eur Psychiatry 2017; 41: S33-S34. https://doi.org/10.1016/j.eurpsy.2017.01.159
  57. Martin A.K, Dzafic I, Ramdave S, Meinzer M. High definition transcranial direct current stimulation over the dorsomedial prefrontal cortex increases the salience of others. Brain Stimulation 2017; 10(2): 422. https://doi.org/10.1016/j.brs.2017.01.252
  58. McLaughlin N.C.R, Conelea C, Blanchette B et al. Modulation of prefrontal function through transcranial direct current stimulation (tDCS). Brain Stimulation 2017; 10 (4): e37. https://doi.org/10.1016/j.brs.2017.04.062
  59. Nikolin S, Boonstra T.W, Loo C.K, Martin D. Prefrontal cortex transcranial direct current stimulation increases parasympathetic nerve activity. Brain Stimulation 2017; 10 (2): 432. https://doi.org/10.1016/j.brs.2017.01.286
  60. Pixa N.H, Steinberg F, Doppelmayr M. Influence of high-definition anodal transcranial direct current stimulation (HD-atDCS) on motor learning of a high-speed bimanual task. Brain Stimulation 2017; 10 (2): 398-99. https://doi.org/10.1016/j.brs.2017.01.182
  61. Worsching J, Padberg F, Helbich K et al. Test-retest reliability of prefrontal transcranial Direct Current Stimulation (tDCS) effects on functional MRI connectivity in healthy subjects. NeuroImage 2017; 155: 187-201. https://doi.org/10.1016/j.neuroimage.2017.04.052
  62. Besson P, Vergotte G, Muthalib M, Perrey S. Test-retest reliability of transcranial direct current stimulation-induced modulation of resting-state sensorimotor cortex oxygenation time course. Brain Stimulation 2017; 10 (2): 400. https://doi.org/10.1016/j.brs.2017.01.186
  63. Bachinger M, Moisa M, Polania R et al. Changing resting state connectivity measured by functional magnetic resonance imaging with transcranial alternating current stimulation. Brain Stimulation 2017; 10 (1): e5. https://doi.org/10.1016/j.brs.2016.11.033
  64. Lafleur L-P, Klees-Themens G, Lefebvre G et al. Connectivity and interhemispheric inhibition between motor cortices: a study with transcranial alternating current stimulation. Brain Stimulation 2017; 10 (2): 405. https://doi.org/10.1016/j.brs.2017.01.200
  65. Pixa N.H, Steinberg F, Doppelmayr M. High-definition transcranial direct current stimulation to both primary motor cortices improves unimanual and bimanual dexterity. Neuroscience Letters 2017; 643: 84-8. https://doi.org/10.1016/j.neulet.2017.02.033
  66. Saiote C, Tacchino A, Brichetto G et al. Resting-state functional connectivity and motor imagery brain activation. Human Brain Mapping 2016; 37 (11): 3847-57. https://doi.org/10.1002/hbm.23280
  67. Bonassi G, Biggio M, Bisio A et al. Provision of somatosensory inputs during motor imagery enhances learning-induced plasticity in human motor cortex. Scientific Reports 2017; 7 (1): 1-10. https://doi.org/10.1038/s41598-017-09597-0
  68. Carrasco D.G, Cantalapiedra J.A. Effectiveness of motor imagery or mental practice in functional recovery after stroke: a systematic review. Neurología (English Edition). 2016; 31 (1): 43-52. https://doi.org/10.1016/j.nrleng.2013.02.008
  69. Ruffino C, Papaxanthis C, Lebon F. Neural plasticity during motor learning with motor imagery practice: Review and perspectives. Neuroscience 2017; 341: 61-78. https://doi.org/10.1016/j.neuroscience.2016.11.023
  70. Wang L, Zhang J, Zhang Y et al. Motor cortex activation during motor imagery of the upper limbs in stroke patients. Digital Medicine 2016; 2 (2): 72-9. https://doi.org/10.4103/2226-8561.189523

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